B&AH nº 28 [2014]

Revista EspaĂąola de HerpetologĂ­a

Journal of the Spanish Herpetological Society (AHE) Volume 28 (2014) http://bah.herpetologica.es bah@herpetologica.org

BASIC & APPLIED HERPETOLOGY REVISTA ESPAÑOLA DE HERPETOLOGÍA

Spanish Herpetological Society (AHE) President: Juan Manuel Pleguezuelos Gómez General Secretary: Íñigo Martínez Solano Treasurer: Xavier Santos Santiró Vocals: Jaime Bosch Pérez (Monitoring programs) Andrés Egea Serrano (Editor, Boletín de la AHE) Adolfo Marco Llorente (Marine turtles) Manuel E. Ortiz Santaliestra (Editor, Basic & Applied Herpetology) Ana Perera Leg (Editor, Basic & Applied Herpetology) Alex Richter Boix (Editor, Boletín de la AHE) Jorge Sánchez Ballibrea (Conservation) Xavier Santos Santiró (Editor, Boletín de la AHE) Daniel Villero Pi (Geographical database and SIARE server)

Editorial Board, Basic and Applied Herpetology Editors in Chief Manuel E. Ortiz Santaliestra (amphibians) Institute for Environmental Sciences University of Koblenz-Landau Fortstraße 7 76829 Landau (Germany) ortiz@uni-landau.de

Ana Perera Leg (reptiles) CIBIO-Universidade do Porto.

Campus Agrário de Vairão.

Rua Padre Armando Quintas-Castro 4485-661 Vairão (Portugal) perera@cibio.up.pt

Associate Editors Ylenia Chiari (University of South Alabama, USA) Antigoni Kaliontzopoulou (Universidade do Porto, Portugal) Íñigo Martínez-Solano (Doñana Biological Station-CSIC, Spain) Neftalí Sillero (Universidade do Porto, Portugal) Mirco Solé (Universidade Estadual de Santa Cruz, Brazil)

Asociación Herpetológica Española Museo Nacional de Ciencias Naturales Cl. José Guitiérrez Abascal, 2 28006 Madrid http://www.herpetologica.es

ISSN 2255 - 1468 Impresión: igrafic. Url: www.igrafic.com

Depósito Legal: M-38882-2012 Maquetación: Marcos Pérez de Tudela. Url: www.marcos-pdt.com

BASIC & APPLIED HERPETOLOGY REVISTA ESPAÑOLA DE HERPETOLOGÍA

CONTENTS Volume 28 (2014) Reviews Interference competition between native Iberian turtles and the exotic Trachemys scripta N. Polo-Cavia, P. López, J. Martín

Pag. 5

Research papers The escape behaviour of wild Greek tortoises Testudo graeca with an emphasis on geometrical shape discrimination A. Glavaschi, E.S. Beaumont Effect of prey availability on growth-rate trajectories of an aquatic predator, the viperine snake Natrix maura A. Filippakopoulou, X. Santos, M. Feriche, J.M. Pleguezuelos, G.A. Llorente Diversity of a community of Anolis (Iguania: Dactyloidae) in the central rainforest, department of Choco, Colombia J.T. Rengifo M., F.C. Herrera, F.J. Purroy A new species of Liolaemus of the L. nigromaculatus group (Iguania: Liolaemidae) from Atacama Region, Chile Y. Marambio-Alfaro, J. Troncoso-Palacios Blood differential count and effect of haemoparasites in wild populations of Pyrenean lizard Iberolacerta aurelioi (Arribas, 1994) A. Martinez-Silvestre, O. Arribas Teeth number variation and cranial morphology within Vipera aspis group M.A.L. Zuffi Atlas of the distribution of reptiles in the Parc National du Banc d’Arguin, Mauritania A.S. Sow, F. Martínez-Freiría, P.-A. Crochet, P. Geniez, I. Ineich, H. Dieng, S. Fahd, J.C. Brito Herpetofauna of Fragas do Eume Natural Park (A Coruña): distribution, conservation status and threats P. Galán

21

35

51

65

79

87 99 113

Short notes Variation in the erythrocyte size among larvae, juveniles and adults of Hypsiboas cordobae (Anura, Hylidae) M. Baraquet, N.E. Salas, A.L. Martino Data on nesting, incubation, and hatchling emergence in the two native aquatic turtle species (Emys orbicularis and Mauremys leprosa) from Doñana National Park C. Díaz-Paniagua, A.C. Andreu, A. Marco, M. Nuez, J. Hidalgo-Vila, N. Perez-Santigosa Helminths from the red-eared slider Trachemys scripta elegans (Chelonia: Emydidae) in marshes from the eastern Iberian Peninsula: first report of Telorchis attenuata (Digenea: Telorchiidae) J. Cardells, M.M. Garijo, C. Marín, S. Vega

137

Book reviews

161

145

153

Cover illustration: Schreiber’s Green Lizard (Lacerta schreiberi) male showing nuptial colouration.

Cambre, A Coruña (see article by Galán in this volume). Author: Pedro Galán.

BASIC & APPLIED HERPETOLOGY REVISTA ESPAÑOLA DE HERPETOLOGÍA

CONTENIDOS Volumen 28 (2014) Revisiones Interferencias competitivas entre los galápagos nativos ibéricos y el galápago exótico Trachemys scripta N. Polo-Cavia, P. López, J. Martín

Pag. 5

Artículos de investigación Conducta de fuga en tortugas moras Testudo graeca salvajes con énfasis en la discriminación de formas geométricas A. Glavaschi, E.S. Beaumont Efecto de la disponibilidad de presas en las trayectorias de crecimiento de un depredador acuático, la culebra viperina Natrix maura A. Filippakopoulou, X. Santos, M. Feriche, J.M. Pleguezuelos, G.A. Llorente Diversidad de una comunidad de Anolis (Iguania: Dactyloidae) en la selva pluvial central, departamento del Chocó, Colombia J.T. Rengifo M., F.C. Herrera, F.J. Purroy Una nueva especie de Liolaemus del grupo de L. nigromaculatus (Iguania: Liolaemidae) para la Región de Atacama, Chile Y. Marambio-Alfaro, J. Troncoso-Palacios Recuento diferencial y efecto de los hemoparásitos en la sangre de poblaciones silvestres de lagartija pirenaica Iberolacerta aurelioi (Arribas, 1994) A. Martinez-Silvestre, O. Arribas Variación en el número de dientes y morfología craniana del grupo Vipera aspis M.A.L. Zuffi Atlas de distribución de los reptiles del Parque Nacional Banc d’Arguin, Mauritania A.S. Sow, F. Martínez-Freiría, P.-A. Crochet, P. Geniez, I. Ineich, H. Dieng, S. Fahd, J.C. Brito Herpetofauna del Parque Natural das Fragas do Eume (A Coruña): distribución, estado de conservación y amenazas P. Galán

21

35

51

65

79

87 99 113

Notas breves Variación en el tamaño de los eritrocitos entre larvas, juveniles y adultos de Hypsiboas cordobae (Anura, Hylidae) M. Baraquet, N.E. Salas, A.L. Martino Nidos, incubación y emergencia de crías en las dos especies de quelonios acuáticos (Emys orbicularis y Mauremys leprosa) del Parque Nacional de Doñana C. Díaz-Paniagua, A.C. Andreu, A. Marco, M. Nuez, J. Hidalgo-Vila, N. Perez-Santigosa Helmintos del galápago Trachemys scripta elegans (Chelonia: Emydidae) en los marjales de la Comunidad Valenciana: primera cita de Telorchis attenuata (Digenea: Telorchiidae) J. Cardells, M.M. Garijo, C. Marín, S. Vega

137

Recensiones bibliográficas

161

145

153

Ilustración de portada: Macho de lagarto verdinegro (Lacerta schreiberi) mostrando coloración nupcial.

Cambre, A Coruña (véase artículo de Galán en este volumen). Autor: Pedro Galán.

Basic and Applied Herpetology 28 (2014): 5-20

Interference competition between native Iberian turtles and the exotic Trachemys scripta Nuria Polo-Cavia1,*, Pilar López2, José Martín2 1 2

Departamento de Biología, Universidad Autónoma de Madrid, Madrid, Spain.

Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain.

* Correspondence: Departamento de Biología, Universidad Autónoma de Madrid, Ciudad Universitaria de Cantoblanco, 28049 Madrid, Spain. Phone: +34 914976775, Fax: +34 914978344, E-mail: nuria.polo@uam.es

Received: 15 September 2013; received in revised form: 20 June 2014; accepted: 23 September 2014.

The red-eared slider, Trachemys scripta elegans, is a worldwide invasive species, currently introduced in most freshwater habitats as a consequence of the exotic pet trade. In the Iberian Peninsula, this American turtle is competing and displacing the Iberian turtles, Emys orbicularis and Mauremys leprosa. Recent studies have pointed out to diverse competitive advantages of sliders over Iberian terrapins. For instance, native turtles avoid chemical cues from T. scripta, which is more aggressive and dominant in direct competition for food and basking places. This avoidance behaviour displayed by Iberian terrapins might serve as a spacing mechanism to avoid unfavourable competitive interactions with the introduced species. Sliders also benefit from morphological and thermoregulatory advantages: they are more spherical, thus presenting a less surface to volume ratio and a greater thermal inertia that facilitates heat retention. On the other hand, introduced turtles show a more accurate assessment of predatory risk in altered habitats, and are more efficient predators of local prey than native species. These inter-specific asymmetries could contribute jointly to the greater competitive ability of introduced T. scripta, thus facilitating the expansion of this alien species in detriment of native populations of Iberian terrapins.

Key words: biological invasions; chemical communication; competition; Iberian turtles; morphology; thermal biology.

Interferencias competitivas entre los galápagos nativos ibéricos y el galápago exótico Trachemys scripta. El galápago de Florida, Trachemys scripta elegans, es una especie invasora a nivel mundial, introducida en la mayor parte de los ecosistemas acuáticos como consecuencia del comercio masivo de mascotas. En la Península Ibérica, este galápago americano compite y desplaza a los galápagos ibéricos, Emys orbicularis y Mauremys leprosa. Estudios recientes han puesto de manifiesto la existencia de diversas ventajas competitivas del galápago de Florida sobre los galápagos nativos ibéricos. Por ejemplo, los galápagos nativos evitan ocupar espacios donde detectan secreciones químicas de los galápagos exóticos, quienes se muestran más agresivos y dominantes en la competencia directa por la comida y los recursos de asoleamiento. Este comportamiento aversivo podría ser utilizado por las especies nativas para evitar las interacciones competitivas desfavorables con la especie invasora. Los galápagos de Florida se benefician también de ventajas morfológicas y termorreguladoras: presentan una forma más esférica y por tanto una menor relación superficie-volumen y una mayor inercia térmica que facilita la retención de calor. Por otra parte, los galápagos exóticos muestran un mejor ajuste del riesgo de depredación en hábitats alterados y poseen ventajas en la captura de presas nativas. Estas asimetrías inter-específicas podrían contribuir conjuntamente a una mayor habilidad competitiva del galápago de Florida, facilitando la expansión de esta especie invasora en detrimento de las poblaciones nativas de galápagos ibéricos.

Key words: biología térmica; competencia; comunicación química; galápagos ibéricos; invasiones biológicas; morfología.

DOI: http://dx.doi.org/10.11160/bah.13014/

6

POLO-CAVIA ET AL.

The introduction of alien species outside their natural distribution ranges represents, after habitat destruction, the second greatest threat to biodiversity (wILCOVE et al., 1998; GUREVITCH & PADILLA, 2004). Introduced species have caused severe alterations in terrestrial and aquatic ecosystems, altering energy flows and displacing native organisms from their ecological niches (HERBOLD & MOYLE, 1986; wILLIAMSON, 1996; MOONEY & HOBBS, 2000; LOCKwOOD et al., 2007). Competition for resources is one of the most habitual ways alien species may impact native populations (SHIGESADA & KAwASAKI, 1997; LOCKwOOD et al., 2007).

The red-eared slider (Trachemys scripta elegans wied, 1839) is a chelonian belonging to the family Emydidae. Native from Southeast USA and Northeast Mexico, the species has become introduced worldwide, especially in Mediterranean countries, as a result of the massive exotic pet trade occurred during the last decades (LUISELLI et al., 1997; CHEN & LUE, 1998; PLEGUEzUELOS, 2002). Trachemys scripta is a semiaquatic turtle, generalist and ubiquitous, with a great adaptive capacity (GIBBONS, 1990).

In the Iberian Peninsula, a large number of young red-eared sliders have been imported from the USA and released in the natural environment, causing a great expansion of the species. Many populations have become naturalized in marshes and wetlands of the littoral, as well as in dispersed points inland (PLEGUEzUELOS, 2002). These populations may cause important impacts on the ecosystems and eventually the displacement of native fauna (DA SILVA & BLASCO, 1995; PLEGUEzUELOS, 2002; VILà et al., 2008; LINDSAY et al., 2013).

Field observations have pointed out the existence of competitive interactions between T. scripta and the two species of Iberian turtles,

the European pond turtle, Emys orbicularis, and the Spanish terrapin, Mauremys leprosa. These two native species have suffered a considerable recession of their populations and a reduction of their distribution ranges (Figs. 1a,b) during the last decades, both being currently considered as endangered (TORTOISE & FRESHwATER TURTLE SPECIALIST GROUP, 1996; VAN DIJK et al., 2004). Habitat destruction and human pressure are major factors responsible for this decline, but competition with exotic introduced turtles might be worsening the state of the remaining populations (Fig. 1c).

Competition for food, basking places or nesting sites is likely to occur (CRUCITTI et al., 1990; CADI & JOLY, 2003, 2004), since both introduced sliders and native terrapins overlap in diet and feeding areas, devote a high percentage of their time budget to bask and coincide in the timing of reproductive seasons (GIBBONS, 1990; ANDREU & LóPEz-JURADO, 1998; KELLER & BUSACK, 2001; PLEGUEzUELOS, 2002).

Transmission of pathogens between introduced turtles and native ones is another interaction likely occurring in syntopic populations (HIDALGO-VILA et al., 2009; VERNEAU et al., 2011). Potential advantages of T. scripta over native Iberian turtles might be a larger adult body size, a more diverse diet, a higher fecundity and a greater tolerance to pollution and human presence (PLEGUEzUELOS, 2002). Also, the origin of T. scripta in environments with saturated fauna where a great number of competitive turtle species coexist, compared to the few competitors of Iberian turtles, might endow the introduced species with competitive advantages in Mediterranean habitats.

Here we review some biological, ecological and behavioural aspects of introduced sliders and Iberian turtles, especially focu-

7

COMPETITION BETWEEN NATIVE AND EXOTIC TURTLES

a

c

sing on T. scripta and M. leprosa, which may contribute to explain competitive interactions between freshwater turtle species. we firstly examine the effect of direct competition with T. scripta on three key factors affecting the ecology and behaviour of M. leprosa: use of space, feeding efficiency and basking efficiency. Subsequently, we compare the specific morphology and thermal biology of the native and invasive species, which might have consequences for the outcome of competition. Finally, we examine other potential advantages that antipredatory behaviour (i.e. inter-specific differences in risk assessment) and predator efficiency (i.e. the inability of prey to recognise introduced predators) might confer to invasive turtle species.

b

Figure 1: Distribution range of (a) Emys orbicularis, (b) Mauremys leprosa, and (c) the exotic Trachemys scripta, in the Iberian Peninsula (adapted from ANDREU & LรณPEz-JURADO, 1998; PLEGUEzUELOS, 2002; LOUREIRO et al., 2008).

DIRECT COMPETITION Chemical Avoidance Experiments studying direct competition between native and introduced turtles have demonstrated that different functions and activities of native terrapins are limited in presence of red-eared sliders. Moreover, semiochemicals (chemical substances conveying a signal for communication between organisms) seem to play an important role in inter-specific competition between native and exotic turtles. In an experiment comparing the use by M. leprosa and T. scripta of pools with clean water and pools with water containing chemical cues from conspecific or heterospecific turtles, M. leprosa preferred

8

POLO-CAVIA ET AL.

water with chemical stimuli from conspecifics and avoided water with chemical cues from T. scripta, whereas T. scripta neither avoided nor preferred water pools with chemical cues from native M. leprosa (POLOCAVIA et al., 2009a; Fig. 2). This suggests that M. leprosa is able to discriminate water-borne cues from introduced T. scripta and modify their use of space to avoid the costs of potential encounters with T. scripta. If scents of T. scripta result aversive for native turtles, dispersal would be a logical consequence in natural environments. On the other hand, the lack of chemosensory responses by T. scripta towards chemical cues of native terrapins –due to its inability to detect heterospecific cues, or simply to that, although detected, these cues do not represent a threat for them–, might further favour the expansion of the invasive species.

Feeding Competition Alteration in space use by M. leprosa in presence of T. scripta seems to respond to the negative effects of direct competition with the invasive species for limited resources. The two species are likely to compete for feeding areas in nature, given that both native and introduced turtles mainly consume animal matter, though they also feed on plants (KELLER & BUSACK, 2001; PLEGUEzUELOS, 2002). Trachemys scripta individuals are aggressive omnivores with high preferences for a carnivorous diet (PARMENTER, 1980; GIBBONS, 1990), capable of threatening or biting other individuals during competitive activities such as feeding (ARVY & SERVAN, 1998; LINDEMAN, 1999). Given that the access to resources is

Figure 2: Percent time (mean ± SE) that exotic red-eared sliders and native turtles spent in experimental ponds with water-borne chemical cues from conspecifics (open rectangles) and heterospecifics (barred rectangles). Native turtles prefer water with cues from conspecifics and avoid water with cues from introduced turtles (adapted from POLO-CAVIA et al., 2009a).

constrained by dominant individuals when competition between foragers is asymmetrical (HOLMGREN, 1995; MOODY & HOUSTON, 1995; SPENCER et al., 1995), a higher level of aggressiveness displayed by introduced sliders during feeding might lead M. leprosa to the displacement from areas with more profitable feeding resources.

Recent findings indicate that feeding competition between native M. leprosa and introduced T. scripta follows an asymmetrical pattern (POLO-CAVIA et al., 2011). Food ingestion of M. leprosa and T. scripta were compared in the laboratory under situations of intra- and inter-specific competition, analysing the frequency of aggressive interactions between individual turtles of similar size, and observing that, when the two turtle species were forced to forage together, the access of M. leprosa to feeding resources was severely restricted by T. scripta, which ingested a greater percentage of the

COMPETITION BETWEEN NATIVE AND EXOTIC TURTLES

9

Basking Competition

Figure 3: Percentage of food (mean ± SE) ingested by exotic red-eared sliders and native turtles under situations of intra- (open rectangles) and interspecific (barred rectangles) feeding competition. when native and introduced turtles are forced to forage together the exotic species restrict the access of native turtles to food resources (adapted from POLO-CAVIA et al., 2011).

supplied food (POLO-CAVIA et al., 2011; Fig. 3). As expected, aggressions occurred more frequently between heterospecific individuals and were more frequently inflicted by introduced T. scripta than by native M. leprosa. This high percentage of aggressions directed from T. scripta to M. leprosa suggests that the former is a more aggressive species and dominant over the latter.

Furthermore, the percentage of food ingested by M. leprosa under inter-specific competition correlated positively with the level of suffered aggressiveness, thus indicating that daring M. leprosa which incurred in active competition for food were harshly punished by aggressive sliders, whereas shier individuals that displayed a subordinate role were less attacked (POLO-CAVIA et al., 2011). These findings suggest the existence for M. leprosa of a trade-off between feeding efficiency and costs of aggressive competition with T. scripta.

Competition for basking sites is another important matter concerning direct competition between freshwater turtle species. Aerial basking serves to activate metabolism by attaining optimal body temperatures that maximize the efficiency of physiological processes (JACKSON, 1971; KEPENIS & MCMANUS, 1974; CRAwFORD et al., 1983; HAMMOND et al., 1988; BEN-EzRA et al., 2008; DUBOIS et al., 2008), favours dermal synthesis of vitamin D (PRITCHARD & GREENHOOD, 1968; AVERY, 1982), and allows conditioning of the skin and the shell (CAGLE, 1950; NEILL & ALLEN, 1954; BOYER, 1965). Thus, both native terrapins and T. scripta spend a large amount of their diel activity basking (MEEK, 1983; GIBBONS, 1990; ANDREU & LóPEz-JURADO, 1998). However, appropriate basking sites such as logs and stones emerging in deep water are limited, and therefore, T. scripta may monopolize optimal basking resources, displacing native terrapins to less preferred sites, and ultimately causing deficiencies in their basking behaviour and thermoregulation (DÍAzPANIAGUA et al., 2002; CADI & JOLY, 2003; POLO-CAVIA et al., 2010a). In a long-term competition experiment, native M. leprosa subjected to inter-specific competition with T. scripta reduced basking activity, basked for shorter periods than sliders, and avoided sharing platforms with exotic turtles (POLOCAVIA et al., 2010a; Fig. 4). Likewise, CADI & JOLY (2003) reported that native E. orbicularis sharing experimental ponds with T. scripta were reluctant to climb onto solaria that were already occupied by T. scripta, shifting instead to basking places of lower quality. Also, field observations of the western pond turtle, Emys

10

POLO-CAVIA ET AL.

Figure 4: Percent time (mean Âą SE) that exotic redeared sliders and native turtles spent basking under intra-specific (open rectangles) and inter-specific competition (barred rectangles). when native and introduced turtles compete for basking sites native turtles significantly reduce the time devoted to bask (adapted from POLO-CAVIA et al., 2010a).

marmorata, sharing basking sites with T. scripta indicate that introduced sliders are much more selective in habitat use than native terrapins (LAMBERT et al., 2013). This avoidance and subordinate behaviour and the consequent detriment in basking activity might lead native turtles to a loss in the efficiency of their physiological functions associated with ineffective thermoregulation, thus favouring the expansion of the invasive species.

MORPHOLOGICAL AND THERMAL ADVANTAGES OF EXOTIC SLIDERS Body shape has been established as a critical factor in the ability of organisms to thermoregulate (BOGERT, 1949; GOULD, 1966).

Hence, morphological differences between native and exotic turtles, resulting from adaptation to different original habitats, might also confer thermoregulatory advantages to introduced sliders in the new environments

in which they are introduced, in detriment of native terrapins. Compared to M. leprosa, T. scripta turtles present a more rounded shell shape that confers them a low surface-tovolume ratio and a greater thermal inertia (POLO-CAVIA et al., 2009b; Fig. 5), thus facilitating heat retention and favouring the efficiency of physiological functions such as aquatic foraging or digestion (HUEY & SLATKIN, 1976; DUNHAM et al., 1989). In temperate zones, mechanisms for conserving body heat could have selective advantages in aquatic turtles, since individuals that have achieved high body temperatures through aerial basking may suddenly be exposed to very cool conditions when entering the water (BARTHOLOMEw, 1982). Consequently, slight differences in thermal inertia between species might favour introduced T. scripta in Mediterranean habitats. For instance, in the Iberian Peninsula, T. scripta specimens have been observed to be active at lower water temperatures than native terrapins, and therefore, they can start earlier their annual cycle (ACEITUNO , 2001). Such adaptation is consistent with the higher thermal inertia of T. scripta observed in the laboratory. In contrast, the more flattened shell shape and lower thermal buffering of M. leprosa compared to T. scripta may entail a difficulty for retention of body heat that, with the presence of a new competitor species interfering in their basking activity, might result in the achievement of suboptimal body temperatures, subsequently causing reduced locomotor activity and food intake, or altered digestive function (POLO-CAVIA et al., 2009b).

In particular, a reduced body temperature negatively influences righting performance of turtles. Turtles may result overturned acci-

COMPETITION BETWEEN NATIVE AND EXOTIC TURTLES

11

Figure 5: Inter-specific differences in thermal exchange rates between exotic red-eared sliders (solid lines) and native turtles (dotted lines), following exposure to step changes of ambient temperature in air and water (adapted from POLO-CAVIA et al., 2009b).

dentally while climbing to basking sites, during male fights, or as consequence of predatory attacks (CORTI & zUFFI, 2003; STANCHER et al., 2006). In these cases, righting behaviour is critical to survival, since turtles in an upside-down position may suffer increased predation exposure, changes in body temperature and dehydration, as well as experience difficulties to breathe (FINKLER, 1999; STEYERMARK & SPOTILA, 2001; MARTร N et al., 2005). At suboptimal temperatures, both native and exotic terrapins were found to increase the time needed to turn themselves over (POLO-CAVIA et al., 2012a).

Consequently, turtles that attain and maintain optimal body temperatures will increase their survival possibilities. Thus, the high thermal inertia of T. scripta is also advantage-

ous insofar as it favours the performance and reduces the risks of exposure to potential predators and overheating while overturning (CARR 1952; wYNEKEN et al., 2008; POLOCAVIA et al., 2009b). Also, the domed shape of the shell facilitates mechanical righting in T. scripta, which needs shorter times on average to turn right-side up than M. leprosa (DOMOKOS & VรกRKONYI, 2008; POLO-CAVIA et al., 2012a).

Experiments comparing bioenergetics of M. leprosa and T. scripta also revealed that the two turtle species differ in thermal requirements (POLO-CAVIA et al., 2012b).

Thus, the upper set point body temperature (i.e. the body temperature at which turtles cease basking and dip into the water; KINGSBURY, 1993, 1999; TOSINI & AVERY,

12

POLO-CAVIA ET AL.

1994; BEN-EzRA et al., 2008; DUBOIS et al., 2008; POLO-CAVIA et al., 2012b) is 5ºC higher on average in M. leprosa compared to T. scripta. This suggests that native M. leprosa, more flattened and with higher surfaceto-volume ratio than T. scripta, might compensate their greater tendency to loss body heat by attaining higher optimal temperatures during basking. Also, individuals with higher surface-to-volume ratios have been observed to bask until attaining higher set point body temperatures, suggesting a close relation between specific thermal requirements and carapace morphology of each species. On the other hand, in response to starvation, the two turtle species similarly reduce their set point temperatures, which points out to the existence of an adaptive energy saving mechanism during periods of low food availability (POLO-CAVIA et al., 2012b). As a result, interferences of T. scripta on feeding and basking behaviour of native terrapins might ultimately cause a reduction in their metabolic rates and a general depression of their physiological functions (PARMENTER, 1981; SIEVERT et al., 1988; GIANOPULOS & ROwE, 1999). Such negative effects may explain the loss of weight and decreased survival rates found in E. orbicularis after long term competition with T. scripta (CADI & JOLY, 2004).

PREDATORY RISK IN ALTERED HABITATS when a predator approaches, turtles typically flee to safe refuges such as deep water or dense vegetation (LóPEz et al., 2005). However, if the predator gets close enough, turtles tend to withdraw inside the shell with the legs, tail and head hidden

(GREENE, 1988; HUGIE, 2003). Then, the decision of when to emerge is accurately adjusted basing on risk factors such as the perceived predation threat, the persistence of the predator or the probability of reaching a safer refuge, vs. the costs of remaining within the shell (i.e. overheating risk, interruption of basking, loss of foraging or mating opportunities, etc.) (SIH et al., 1998; MARTÍN et al., 2005; POLO-CAVIA et al., 2008). In these cases, the high thermal inertia of T. scripta protects turtles from desiccation (CARR, 1952; wYNEKEN et al., 2008; POLO-CAVIA et al., 2009b) and its spherical shell shape reduces the risk of successful predatory attacks, as it hampers the capture by snapping jaws or avian predators (PRITCHARD, 1979; JANzEN et al., 2000). In contrast, M. leprosa hidden within the shell are more prone than T. scripta to overheating or predation due to their more flattened shape. Thus, as expected, M. leprosa escapes quickly to the water when facing a terrestrial threat while T. scripta tends to remain for longer in land, hidden inside the shell (POLO-CAVIA et al., 2008). These inter-specific differences in response to predation risk between native and introduced turtles may result advantageous for the introduced species in altered habitats where human pressure has considerably reduced the risk of predation by natural predator species. In such environments, where T. scripta is mainly introduced, the costs derived from interruption of basking and repeated unnecessary flees to water due to human disturbance (DILL & FRASER, 1997; SIH, 1997; MARTÍN & LóPEz, 1999) might suppose a disadvantage for native turtles when competing with introduced sliders.

COMPETITION BETWEEN NATIVE AND EXOTIC TURTLES

13

INTERACTIONS wITH TADPOLE PREY

SYNTHESIS AND FUTURE RESEARCH

Human alteration of ecosystems may cause disruption of the antipredatory behaviour of native turtles, but may also affect their predatory efficiency by means of introducing a competitor species that fed on the same prey and benefit from an evolutionary release. Antipredatory responses of prey are expected to be adaptive in the specific habitats in which they evolved, but however, prey may not be innately equipped to cope with suddenly introduced predators with which they have not shared a long evolutionary past (SCHLAEPFER et al., 2002, 2005).

For this reason, native prey are generally unable to detect or adequately respond to the hunting tactics of novel predators, which do not experience some of the difficulties of finding prey that keep working for native predators (L AwLER et al., 1999; KIESECKER et al., 2001; BABER & BABBITT, 2003). This is the case of tadpoles of several Iberian anuran species, which are common prey of both native and introduced turtles.

These tadpoles have been observed to innately respond to predator chemical cues from the two Iberian turtles, E. orbicularis and M. leprosa, but contrarily, tadpoles are not able to recognise exotic predatory turtles of the genera Trachemys or Graptemys (POLOCAVIA et al., 2010b). Consequently, exotic turtles may easily capture larval amphibian prey outcompeting native Iberian turtles.

The advantage of an evolutionary release may explain the paradox of why invasive species sometimes prosper better in their new habitats than native adapted species (BLOSSEY & NรถTzOLD, 1995; SHEA & CHESSON, 2002; ALLENDORF & LUNDQUIST, 2003).

The studies to date analysing interference competition between native Iberian turtles and T. scripta suggest a greater competitive ability of the exotic T. scripta in vying for resources. In direct competition, native turtles seem to rely on water-borne chemical cues to discriminate between conspecifics and heterospecifics, thus avoiding potential costly interactions with exotic turtles, deserting resources or displacing to less preferred areas (POLO-CAVIA et al., 2009a). Thus, the higher aggressiveness and dominance of sliders in competition for food or basking sites may lead native terrapins to a detriment in their nutritional state and thermoregulatory behaviour (POLO-CAVIA et al., 2010a, 2011).

On the other hand, species-specific traits such as a more spherical shell shape and a greater thermal buffering may confer additional competitive advantages to exotic T. scripta in comparison to turtles native to the new habitats where they are introduced. Hence, the high thermal inertia of T. scripta facilitates heat retention and favours physical and physiological performances (POLO-CAVIA et al., 2009b, 2012a). Also, a greater thermal buffering reduces overheating and dehydration risks in situations in which turtles have lost the behavioural control of their body temperature (e.g. if they result overturned or suffer a predatory attack) (CARR, 1952; wYNEKEN et al., 2008).

Inter-specific differences in risk perception between introduced T. scripta and native Iberian turtles may also benefit the former in anthropogenically disturbed environments in which they are mainly introduced. In these habitats, where terrestrial predators are reduced and human pre-

14

POLO-CAVIA ET AL.

sence carries little risk of actual predation, T. scripta could avoid unnecessary flees to water and subsequently basking interruptions by remaining hidden in the shell (POLO-CAVIA et al., 2008).

These findings emphasise the importance of further studies linking habitat conservation with invasion success. Likewise, comprehension of adaptive evolutionary responses of native and introduced species is essential in understanding competition processes, given that alien introduced species create new ecological contexts in which adaptive responses of native organisms may loss functionality (CALLAwAY & ASCHEHOUG, 2000; SHEA & CHESSON, 2002). Hence, the inability of amphibian tadpoles to innately recognise chemical cues from exotic predatory turtles may represent a further competitive advantage for introduced turtles over native ones in the Iberian Peninsula (POLO-CAVIA et al., 2010b). However, the magnitude and impact of this evolutionary release on native populations of Iberian turtles remains uncertain, as amphibian prey might acquire learned recognition of novel competitive predators and enhance survival (MIRzA & CHIVERS, 2000; GAzDEwICH & CHIVERS, 2002; POLO-CAVIA & GOMEz-MESTRE, 2014).

Native organisms have been observed to alter morphology and/or behaviour as a result of their interactions with exotic species (REzNICK & ENDLER 1982; MAGURRAN, 1989; SINGER et al., 1993; CARROLL et al., 1997, 1998). Thus, under favourable circumstances, native species may induce or evolve mechanisms to cope with invasions and maintain their populations (MEYERS & BULL, 2002). However, despite the existing cases of induced plasticity and rapid evolution in response to sudden environmental changes (ASHLEY et al., 2003; RICE & EMERY, 2003; STOCKwELL et al., 2003; SHINE, 2012), the

evolutionary processes are hardly ever incorporated into conservation plans (SCHLAEPFER et al., 2005). The studies reviewed here evidence the necessity of managing biological invasions basing on evolutionary dynamics, behaviour and plasticity of native species, with the purpose of guaranteeing the conservation goal of long-term persistence (ASHLEY et al., 2003; STOCKwELL et al., 2003; SHINE, 2012).

In conclusion, the existing asymmetries in morphology, ecology and behavioural responses of native Iberian turtles and introduced redeared sliders, resulting from adaptation to their respective natural habitats, seem to be jointly responsible for the greater competitive ability of exotic T. scripta. These inter-specific differences might favour the displacement of native turtles to suboptimal resources and facilitate the expansion of introduced sliders in their new habitats. Future investigations comparing native populations of Iberian turtles in coexistence and free from introduced turtle competitors will help to evaluate the ability of native terrapins to resist the invasion in a long-term scenario (wILLIAMSON, 1996; JOLY, 2000), enabling the design of management strategies that support native populations long enough to allow them to adapt to the new challenges posed by invasive turtle species (ASHLEY et al., 2003; SCHLAEPFER et al., 2005; SHINE, 2012).

Acknowledgement we thank the scientific committee of the “International Symposium on Freshwater Turtles Conservation� for their invitation to submit this review and two anonymous reviewers for their helpful comments. The European LIFE project LIFE09 NAT/ES/000529 supported N. P.-C. attendance to the meeting. Research on

COMPETITION BETWEEN NATIVE AND EXOTIC TURTLES

competition between turtles was performed at El Ventorrillo MNCN Field Station and supported by the projects MCI-CGL200802119/BOS and MICIIN-CGL201124150/BOS. REFERENCES ACEITUNO, J. (2001). La Población del Galápago de Florida (Trachemys scripta elegans) en la Desembocadura del Río CofioEmbalse de San Juan (Madrid). Unpublished report, Asociación Herpetológica Española, Madrid, Spain.

ALLENDORF, F.w. & LUNDQUIST, L.L. (2003). Introduction: population biology, evolution, and control of invasive species.

Conservation Biology 17: 24-30.

ANDREU, A.C. & LóPEz-JURADO, L.F. (1998).

Mauremys leprosa (Schweigger, 1812), In A. Salvador (coord.) Reptiles. Series: Fauna Ibérica, Vol. 10 (M.A. Ramos, ed.). Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, Spain, pp. 103-108.

ARVY, C. & SERVAN, J. (1998). Imminent competition between Trachemys scripta and Emys orbicularis in France.

Mertensiella 10: 33-40.

ASHLEY, M.V.; wILLSON, M.F.; PERGAMS, O.R.w.; O’DOwD, D.J.; GENDE, S.M. & BROwN, J.S. (2003). Evolutionarily enlightened management. Biological Conservation 111: 115-123.

AVERY, R.A. (1982). Field studies of body temperatures and thermoregulation, In C. Gans & F.H. Pough (eds.) Biology of the Reptilia, Volume 12, Physiology C, Physiological Ecology. Academic Press, New York, NY, USA, pp. 93-166.

15

BABER, M.J. & BABBITT, K.J. (2003). The relative impacts of native and introduced predatory fish on a temporary wetland tadpole assemblage. Oecologia 136: 289-295.

BARTHOLOMEw, G.A. (1982). Physiological control of body temperature, In C. Gans & F.H. Pough (eds.) Biology of the Reptilia, Volume 12, Physiology C, Physiological Ecology. Academic Press, New York, NY, USA, pp. 167-212.

BEN-EzRA, E.; BULTé, G. & BLOUINDEMERS, G. (2008). Are locomotor performances coadapted to preferred basking temperature in the Northern Map Turtle (Graptemys geographica)? Journal of Herpetology 42: 322-331.

BLOSSEY, B. & NöTzOLD, R. (1995).

Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology 83: 887-889.

BOGERT, C.M. (1949). Thermoregulation in reptiles, a factor in evolution. Evolution 3: 195-211.

BOYER, D.R. (1965). Ecology of the basking habit in turtles. Ecology 46: 99-118.

CADI, A. & JOLY, P. (2003). Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Canadian Journal of Zoology 81: 1392-1398.

CADI, A. & JOLY, P. (2004). Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodiversity and Conservation 13: 2511-2518.

CAGLE, F.R. (1950). The life history of the slider turtle, Pseudemys scripta troostii (Hoolbrook).

Ecological Monographs 20: 31-54.

16

POLO-CAVIA ET AL.

CALLAwAY, R.M. & ASCHEHOUG, E.T. (2000). Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290: 521-523.

CARR, A.F. (1952). Handbook of Turtles. The Turtles of the United States, Canada, and Baja California. Cornell University Press, Ithaca, NY, USA. CARROLL, S.P.; DINGLE, H. & KLASSEN, S.P. (1997). Genetic differentiation of fitnessassociated traits among rapidly evolving populations of the soapberry bug.

Evolution 51: 1182-1188.

CARROLL, S.P.; KLASSEN, S.P. & DINGLE, H. (1998). Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug. Evolutionary Ecology 12: 955-968.

CHEN, T.-H. & LUE, K.-Y. (1998).

Ecological notes on feral populations of Trachemys scripta elegans in northern Taiwan. Chelonian Conservation and Biology 3: 87-90.

CORTI. C. & zUFFI, M.A.L. (2003). Aspects of population ecology of Testudo hermanni hermanni from Asinara Island, Nw Sardinia (Italy, western Mediterranean Sea): preliminary data. Amphibia-Reptilia 24: 441-447.

CRAwFORD, K.M.; SPOTILA, J.R. & STANDORA, E.A. (1983). Operative environmental temperatures and basking behavior of the turtle Pseudemys scripta.

Ecology 64: 989-999.

CRUCITTI, P.; CAMPESER, A. & MALORI, M. (1990). Populazioni sintopiche di Emys orbicularis e Mauremys caspica nella Tracia, Grecia Orientale (Reptilia, Testudines: Emydidae). Bollettino del Museo Regionale di Scienze Naturali di Torino 8: 187-196.

DA SILVA,

E. & BLASCO, M. (1995) Trachemys scripta elegans in Southwestern Spain.

Herpetological Review 26: 133-134.

DÍAz-PANIAGUA, C.; MARCO, A.; ANDREU, A.C.; SáNCHEz, C.; PEñA, L.; ACOSTA, M. & MOLINA, I. (2002). Trachemys scripta en Doñana. Unpublished report, Asociación Herpetológica Española, Sevilla, Spain.

DILL, L.M. & FRASER, A.H.G. (1997). The worm re-turns: hiding behavior of a tubedwelling marine polychaete, Serpula vermicularis. Behavioural Ecology 8: 186-193.

DOMOKOS, G. & VáRKONYI, P.L. (2008).

Geometry and self-righting of turtles.

Proceedings of the Royal Society B 275: 11-17.

DUBOIS, Y.; BLOUIN-DEMERS, G. & THOMAS, D. (2008). Temperature selection in wood turtles (Glyptemys insculpta) and its implications for energetics.

Ecoscience 15: 398-406.

DUNHAM, A.E.; GRANT, B.w. & OVERALL, K.L. (1989). Interfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ectotherms.

Physiological Zoology 62: 335-355.

FINKLER, M.S. (1999). Influence of water availability during incubation on hatchling size, body composition, desiccation tolerance, and terrestrial locomotor performance in the snapping turtle Chelydra serpentina. Physiological and Biochemical Zoology 72: 714-722.

GAzDEwICH, K.J. & CHIVERS, D.P. (2002).

Acquired predator recognition by fathead minnows: influence of habitat characteristics on survival. Journal of Chemical Ecology 28: 439-445.

GIANOPULOS, K.D. & ROwE, J.w. (1999).

Effects of short-term water temperature variation on food consumption in painted turtles

COMPETITION BETWEEN NATIVE AND EXOTIC TURTLES

(Chrysemys picta marginata). Chelonian Conservation and Biology 3: 504-507.

GIBBONS, w.J. (1990). The slider turtle, IN w.J. Gibbons (ed.) Life History and Ecology of the Slider Turtle. Smithsonian Institution Press, washington, DC, USA, pp. 3-18.

GOULD, S.J. (1966). Allometry and size in ontogeny and phylogeny. Biological Reviews 41: 587-640.

GREENE, H.w. (1988). Antipredator mechanisms in reptiles, In C. Gans & R.B. Huey (eds.) Biology of the Reptilia, Volume 16, Ecology B, Defense and Life History. Academic Press, New York, NY, USA, pp. 1-152.

GUREVITCH, J. & PADILLA, D.K. (2004). Are invasive species a major cause of extinctions?

Trends in Ecology and Evolution 19: 470-474.

HAMMOND, K.A.; SPOTILA, J.R. & STANDORA, E.A. (1988). Basking behavior of the turtle Pseudemys scripta: Effects of digestive state, acclimation temperature, sex and season.

Physiological Zoology 61: 69-77.

HERBOLD, B. & MOYLE, P.B. (1986).

Introduced species and vacant niches. The American Naturalist 128: 751-760.

HIDALGO-VILA, J.; DÍAz-PANIAGUA, C.; RIBAS, A.; FLORENCIO, M.; PéREzSANTIGOSA, N. & CASANOVA, J.C. (2009). Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in southwestern Spain: Transmission from native turtles. Research in Veterinary Science 86: 463-465.

HOLMGREN, N. (1995). The ideal free distribution of unequal competitors: predictions from a behaviour-based functional response.

Journal of Animal Ecology 64: 197-212.

HUEY, R.B. & SLATKIN, M. (1976). Cost and benefits of lizard thermoregulation. The Quarterly Review of Biology 51: 363-384.

17

HUGIE, D.M. (2003). The waiting game: a “battle of waits” between predator and prey. Behavioural Ecology 14: 807-817.

JACKSON, D.C. (1971). The effect of temperature on ventilation in the turtle, Pseudemys scripta elegans. Respiration Physiology 12: 131-140.

JANzEN, F.J.; TUCKER, J.K. & PAUKSTIS, G.L. (2000). Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles. Journal of Evolutionary Biology 13: 947-954.

JOLY, P. (2000). Invasions biologiques: état de l’art et perspectives. Revue d’Ecologie (La Terre et la Vie) Suppl. 7: 21-35.

KELLER, C. & BUSACK, S.D. (2001).

Mauremys leprosa (Schweigger, 1812) ‒ Maurische Bachschildkröte, In U. Fritz (ed.) Handbuch der Reptilien und Amphibien Europas, Band 3/IIIA, Schildkröten (Testudines) I. Aula-Verlag, wiesbaden, Germany, pp. 57-88.

KEPENIS, V. & MCMANUS, J.J. (1974).

Bioenergetics of young painted turtles, Chrysemys picta. Comparative Biochemistry and Physiology A 48: 309-317.

KIESECKER, J.M.; BLAUSTEIN, A.R. & MILLER, C.L. (2001). Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82: 1964-1970.

KINGSBURY, B.A. (1993). Thermoregulatory set points of the eurythermic lizard Elgaria multicarinata. Journal of Herpetology 27: 241-247.

KINGSBURY, B.A. (1999). An experimental design for examining thermoregulatory set points in ectothermic animals. The American Biology Teacher 61: 448-452.

18

POLO-CAVIA ET AL.

LAMBERT, M.R.; NIELSEN, S.N.; wRIGHT, A.N.; THOMSON, R.C. & SHAFFER, H.B. (2013).

Habitat features determine the basking distribution of introduced Red-Eared Sliders and native western Pond Turtles. Chelonian Conservation and Biology 12: 192-199.

LAwLER, S.P.; DRITz, D.; STRANGE, T. & HOLYOAK, M. (1999). Effects of introduced mosquitofish and bullfrogs on the threatened California red-legged frog.

Conservation Biology 13: 613-622.

LINDEMAN, P.V. (1999). Aggressive interactions during basking among four species of emydid turtles. Journal of Herpetology 33: 214-219.

LINDSAY, M.K.; zHANG, Y.; FORSTNER, M.R.J. & HAHN, D. (2013). Effects of the freshwater turtle Trachemys scripta elegans on ecosystem functioning: an approach in experimental ponds. AmphibiaReptilia 34: 75-84.

LOCKwOOD, J.L.; HOOPES, M.F. & MARCHETTI, M.P. (2007). Invasion Ecology. Blackwell Publishing, Oxford, UK. LóPEz, P.; MARCOS, I. & MARTÍN, J. (2005).

Effects of habitat-related visibility on escape decisions of the Spanish terrapin Mauremys leprosa. Amphibia-Reptilia 26: 557-561.

LOUREIRO, A.; FERRAND DE ALMEIDA, N.; CARRETERO, M.A. & PAULO, O.S. (2008) Atlas dos Anfíbios e Répteis de Portugal.

Instituto da Conservação da Natureza e da Biodiversidade, Lisboa, Portugal.

LUISELLI, L.; CAPULA, M.; CAPIzzI, D.; FILIPPI, E.; TRUJILLO, J.V. & ANIBALDI, C. (1997).

Problems for conservation of pond turtles (Emys orbicularis) in central Italy: is the introduced red-eared turtle (Trachemys scripta) a serious threat? Chelonian Conservation and Biology 2: 417-419.

MAGURRAN, A.E. (1989). Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus). Ethology 82: 216-223.

MARTÍN, J. & LóPEz, P. (1999). An experimental test of the costs of antipredatory refuge use in the wall lizard, Podarcis muralis. Oikos 84: 499-505.

MARTÍN, J.; MARCOS, I. & LóPEz, P. (2005). when to come out from your own shell: risk-sensitive hiding decisions in terrapins. Behavioural Ecology and Sociobiology 57: 405-411.

MEEK, R. (1983). Body temperatures of a desert population of the stripe-necked terrapin, Mauremys caspica. British Journal of Herpetology 6: 335-337.

MEYERS, L.A. & BULL, J.J. (2002). Fighting change with change: adaptive variation in an uncertain world. Trends in Ecology and Evolution 17: 551-557.

MIRzA, R.S. & CHIVERS, D.P. (2000). Predatorrecognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Canadian Journal of Zoology 78: 2198-2208.

MOODY, A.L. & HOUSTON, A.I. (1995).

Interference and the ideal free distribution. Animal Behaviour 49: 1065-1072.

MOONEY, H.A. & HOBBS, R.J. (2000).

Invasive Species in a Changing World.

Island Press, washington, DC, USA. NEILL, w.T. & ALLEN, E.R. (1954). Algae on turtles: some additional considerations.

Ecology 35: 581-584.

PARMENTER, R.R. (1980). Effects of food availability and water temperature on the feeding ecology of pond sliders (Chrysemys s. scripta). Copeia 1980: 503-514.

PARMENTER, R.R. (1981). Digestive turnover rates in freshwater turtles: the influence of

COMPETITION BETWEEN NATIVE AND EXOTIC TURTLES

temperature and body size. Comparative Biochemistry and Physiology A 70: 235-238.

PLEGUEzUELOS, J.M. (2002). Las especies introducidas de anfibios y reptiles, In J.M. Pleguezuelos, R. Márquez & M. Lizana (eds.) Atlas y Libro Rojo de los Anfibios y Reptiles de España. Asociación Herpetológica Española-Ministerio de Medio Ambiente, Madrid, Spain, pp. 501-532.

POLO-CAVIA, N. & GOMEz-MESTRE, I. (2014). Learned recognition of introduced predators determines survival of tadpole prey. Functional Ecology 28: 432-439.

POLO-CAVIA, N.; LóPEz, P. & MARTÍN, J. (2008). Interspecific differences in responses to predation risk may confer competitive advantages to invasive freshwater turtle species. Ethology 114: 115-123.

POLO-CAVIA, N.; LóPEz, P. & MARTÍN, J. (2009a). Interspecific differences in chemosensory responses of freshwater turtles: consequences for competition between native and invasive species. Biological Invasions 11: 431-440.

POLO-CAVIA, N.; LóPEz, P. & MARTÍN, J. (2009b). Interspecific differences in heat exchange rates may affect competition between introduced and native freshwater turtles. Biological Invasions 11: 1755-1765.

POLO-CAVIA, N.; LóPEz, P. & MARTÍN, J. (2010a). Competitive interactions during basking between native and invasive freshwater turtle species. Biological Invasions 12: 2141-2152.

POLO-CAVIA, N.; GONzALO, A.; LóPEz, P. & MARTÍN, J. (2010b). Predator recognition of native but not invasive turtle predators by naïve anuran tadpoles. Animal Behaviour 80: 461-466.

19

POLO-CAVIA, N.; LóPEz, P. & MARTÍN, J. (2011).

Aggressive interactions during feeding between native and invasive freshwater turtles.

Biological Invasions 13: 1387-1396.

POLO-CAVIA, N.; LóPEz, P. & MARTÍN, J. (2012a). Effects of body temperature on righting performance of native and invasive freshwater turtles: consequences for competition. Physiology and Behaviour 108: 28-33.

POLO-CAVIA, N.; LóPEz, P. & MARTÍN, J. (2012b). Feeding status and basking requirements of freshwater turtles in an invasion context. Physiology and Behaviour 105: 1208-1213.

PRITCHARD, P.C.H. (1979). Encyclopedia of Turtles.

TFH Publications, Neptune, NJ, USA. PRITCHARD, P.C.H. & GREENHOOD, w.F. (1968). The sun and the turtle.

International Turtle and Tortoise Society Journal 2: 20-25.

REzNICK, D. & ENDLER, J.A. (1982). The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36: 160-177.

RICE, K.J. & EMERY, N.C. (2003). Managing microevolution: restoration in the face of global change. Frontiers in Ecology and the Environment 1: 469-478.

SCHLAEPFER, M.A.; RUNGE, M.C. & SHERMAN, P.w. (2002). Ecological and evolutionary traps. Trends in Ecology and Evolution 17: 474-480.

SCHLAEPFER, M.A.; SHERMAN, P.w.; BLOSSEY, B. & RUNGE, M.C. (2005).

Introduced species as evolutionary traps.

Ecology Letters 8: 241-246.

SHEA, K. & CHESSON, P. (2002).

Community ecology theory as a framework for biological invasions. Trends in Ecology and Evolution 17: 170-176.

20

POLO-CAVIA ET AL.

SHIGESADA, N. & KAwASAKI, K. (1997).

Biological invasions: Theory and practice.

Oxford University Press, Oxford, UK. SHINE, R. (2012). Invasive species as drivers of evolutionary change: cane toads in tropical Australia. Evolutionary Applications 5: 107-116.

SIEVERT, L.M.; SIEVERT, G.A. & CUPP, P.V., JR. (1988). Metabolic rate of feeding and fasting juvenile midland painted turtles, Chrysemys picta marginata. Comparative Biochemistry and Physiology A 90: 157-159.

SIH, A. (1997). To hide or not to hide? Refuge use in a fluctuating environment. Trends in Ecology and Evolution 12: 375-376.

SIH, A.; ENGLUND, G. & wOOSTER, D. (1998). Emergent impacts of multiple predators on prey. Trends in Ecology and Evolution 13: 350-355.

SINGER, M.C.; THOMAS, C.D. & PARMESAN, C. (1993). Rapid human-induced evolution of insect-host associations. Nature 366: 681-683.

SPENCER, H.G.; KENNEDY, M. & GRAY, R.D. (1995). Patch choice with competitive asymmetries and perceptual limits: the importance of history. Animal Behaviour 50: 497-508.

STANCHER, G.; CLARA, E.; REGOLIN, L. & VALLORTIGARA, G. (2006). Lateralized righting behaviour in the tortoise (Testudo hermanni). Behavioural Brain Research 173: 315-319.

STEYERMARK, A.C. & SPOTILA, J.R. (2001).

Body temperature and maternal identity affect snapping turtle (Chelydra serpentina) righting response. Copeia 2001: 1050-1057.

STOCKwELL, C.A.; HENDRY, A.P. & KINNISON, M.T. (2003). Contemporary evolution meets conservation biology. Trends in Ecology and Evolution 18: 94-101.

TORTOISE & FRESHwATER TURTLE SPECIALIST GROUP (1996). Emys orbicularis, In The IUCN Red List of Threatened Species. Version 2014.3.

International Union for Conservation of Nature and Natural Resources, Gland, Switzerland. Available at: http://www.iucnredlist.org/details/7717/0.

Retrieved on 01/08/2015.

TOSINI, G. & AVERY, R. (1994). Diel variation in thermoregulatory set points of the lizard Podarcis muralis. Amphibia-Reptilia 15: 93-96.

VAN DIJK, P.P.; MATEO MIRAS, J.A.; CHEYLAN, M.; JOGER, U.; Sá-SOUSA, P. & PéREzMELLADO, V. (2004). Mauremys leprosa, In The IUCN Red List of Threatened Species.

Version 2014.3. International Union for Conservation of Nature and Natural Resources, Gland, Switzerland. Available at: http://www.iucnredlist.org/details/158468/ 1. Retrieved on 01/08/2015.

VERNEAU, O.; PALACIOS, C.; PLATT, T.; ALDAY, M.; BILLARD, E.; ALLIENNE, J.-F.; BASSO, C. & DU PREEz, L.H. (2011). Invasive species threat: parasite phylogenetics reveals patterns and processes of host-switching between non-native and native freshwater turtles.

Parasitology 138: 1778-1792.

VILà, M.; VALLADARES, F.; TRAVESET, A.; SANTAMARÍA, L. & CASTRO, P. (2008).

Invasiones Biológicas. Consejo Superior de Investigaciones Científicas, Madrid, Spain. wILCOVE, D.S.; ROTHSTEIN, D.; DUBOw, J.; PHILLIPS, A. & LOSOS, E. (1998).

Quantifying threats to imperilled species in the United States. BioScience 48: 607-615. wILLIAMSON, M. (1996). Biological Invasions.

Chapman and Hall, London, UK. wYNEKEN, J.; GODFREY, M.H.; BELS, V. (2008). Biology of Turtles. CRC Press, Boca Raton, FL, USA.

Basic and Applied Herpetology 28 (2014): 21-33

The escape behaviour of wild Greek tortoises Testudo graeca with an emphasis on geometrical shape discrimination Alexandra Glavaschi, Ellen S. Beaumont* Department of Biological and Forensic Sciences, University of Derby, Derby, UK. * Correspondence: Department of Biological and Forensic Sciences, University of Derby, Kedleston Road, Derby, DE22 1GB, UK. Phone: +44 (01332) 591156, E-mail:e.beaumont@derby.ac.uk

Received: 17 December 2013; received in revised form: 11 July 2014; accepted:14 July 2014.

Geometrical shape discrimination has been shown to play an important role in the spatial orientation of a wide variety of mammals and birds, while the study of this ability in particular and of cognitive processes in general has been rather neglected in reptiles. The present experiment aims to investigate the ability of wild Greek tortoises Testudo graeca from Topolog forest, Tulcea County, Romania, to discriminate between simple geometrical shapes. Forty-two adult tortoises were subjected to a task consisting of escaping from a square arena through one of the four available doors, each with a geometrical shape attached. Thirty-one individuals completed 10 consecutive trials, requiring significantly less time for the last trial than for the first. This trend suggests that Greek tortoises developed and used an escape strategy, most likely relying on the geometrical shapes provided as cues. This experiment is the first to explore the cognitive processes of this species and further work should expand on the ecological significance of this ability.

Key words: cognitive abilities; navigation; orientation; Romania; Tulcea; visual cues.

Conducta de fuga en tortugas moras Testudo graeca salvajes con énfasis en la discriminación de formas geométricas. Se ha visto que la discriminación de formas geométricas juega un papel importante en la orientación especial de una gran variedad de mamíferos y aves, pero el estudio en reptiles de esta capacidad en particular, y de los procesos cognitivos en general, ha recibido poca atención. El experimento que aquí se presenta tiene por objeto investigar la capacidad de tortugas moras Testudo graeca salvajes procedentes del bosque Topolog, distrito de Tulcea, Rumanía, de discriminar entre formas geométricas simples. Cuarenta y dos tortugas adultas fueron sometidas a una prueba para escapar de un espacio cuadrado mediante una de las cuatro puertas disponibles, cada una de las cuales tenía pegada una forma geométrica. Treinta y un individuos completaron tres intentos consecutivos, necesitando para el último intento un tiempo significativamente inferior que para el primero. Esta tendencia sugiere que las tortugas moras desarrollaron y utilizaron una estrategia de fuga, muy probablemente dependiente de las formas geométricas proporcionadas como señales. Este experimento es el primero en explorar el proceso cognitivo de esta especie, y el significado ecológico de esta capacidad deberá ser investigado en próximos estudios.

Key words: capacidades cognitivas; navegación; orientación; Rumanía; señales visuales; Tulcea.

Efficient navigation is of obvious importance in an animal’s daily activities and relies on different orientation mechanisms that make use of a wide variety of cues, including the sun, moon, stars, polarized light, auditory, chemical, electrical and visual cues (ABLE, 1991). Two types of DOI: http://dx.doi.org/10.11160/bah.13019/

visual cues are recognized in studies of spatial orientation: geometrical cues (the overall shape of the environment, the distinction between left and right, angles and distances), and non-geometrical or featural cues (including colour, texture and brightness) (CHENG, 1986).

22

GLAVASCHI & BEAUMONT

As shown for species like rats (CHENG, 1986), human children (HERMER & SPELKE, 1996), rhesus monkeys Macaca mulatta (GOUTEUX et al., 2001), red tails plitfins Xenotoca eiseni (SOVRANO et al., 2002, 2003), or Neotropical ants Gygantiops destructor (wYSTRACH & BEUGNON, 2009), the overall geometry of the environment is used primarily in orientation tasks. The importance of global geometry for spatial orientation makes sense from an ecological point of view. In an animal’s natural environment, the overall layout (shapes and distances between important landmarks) remains unchanged across seasons, whereas more local cues such as colours, textures, and brightness may change (for example, due to season change). Thus, the global geometry is more reliable for animal orientation (CHENG & GALLISTEL, 1984; GALLISTEL, 1990; HERMER & SPELKE, 1996).

However, smaller, more local cues cannot be ignored. The ability to use geometric properties of more specific objects, as opposed to the geometry of the environment discussed so far, must be adaptive, as it provides animals with vital information for everyday activity. Various species have been studied in terms of their perception of geometrical shapes and visual discrimination ability. Sand fiddler crabs (Uca pugilator) with no previous training that were presented simultaneously with stationary geometrical shapes of equal surface areas exhibited various response strengths, in descending order as follows: vertical rectangle > horizontal rectangle >triangle > square > circle (L ANGDON & HERRNKIND, 1985). Moreover, chemically stimulated heaping fiddler crabs (Uca cumulanta) navigated away from striped rectangles that resembled seagrass meadows inhabited

by predators, and orientated towards vertical ovals perceived as refuge sites (CHIUSSI & DIAz, 2002). Similarly, some species of hermit crabs and mangrove crabs can learn to associate geometrical shapes with either shelters (represented by gastropod shells of various qualities) or predators, depending on the size and the angle at which the shape is positioned (ORIHUELA et al., 1992; DIAz et al., 1994, 1995). Cotton-top tamarins (Saguinus oedipus) subjected to a foraging task in an artificial jungle were not affected by changes in the overall shape of the environment whereas alterations of the landmark shape resulted in significant performance disturbance (DEIPOLYI et al., 2001).

Geometrical shape discrimination is also reported in several species of fish, such as the African cichlid Pseudotropheus sp., which could distinguish between two-dimensional geometrical shapes of various sizes and differentiate between two categories of objects, “fish” and “snail” (SCHLUESSEL et al., 2012) and the Ambon damselfish, Pomacentrus amboinensis, which could rapidly learn to discriminate between bi-dimensional and tridimensional objects (SIEBECK et al., 2009).

The experimental design ensured a gradual reduction of the number of stimuli until only overall shape remained, which was still enough for the fish to discriminate accurately (SIEBECK et al., 2009).

It has long been assumed that amphibians and reptiles are not capable of learning to an extent comparable to mammals and birds, mainly due to the lack of anatomical structures involved in advanced cognitive processes (SUBOSKI, 1992). However, the interest in reptile intelligence has a relatively long history (reviewed in Burghardt, 1977, cited in wILKINSON

GEOMETRICAL SHAPE DISCRIMINATION IN GREEK TORTOISES

et al., 2007). Reptiles have been found to perform similarly to mammals and birds in spatial orientation tasks (LóPEz et al., 2000, 2001) and there is a growing body of evidence suggesting that the medial cortex of reptiles is equivalent to mammalian and avian hippocampus in terms of its role in spatial memory (RODRÍGUEz et al., 2002; LóPEz et al., 2003).

The most recent information concerning cognitive aspects of chelonians comes from the study of the red-footed tortoise, Chelonoidis carbonarius. The animals performed above chance in an eight-arm radial maze, never re-entering an arm they just exited from (wILKINSON et al., 2007) and, when available, using extra-maze cues to orient (wILKINSON et al., 2009). Although a solitary species, red-footed tortoises are able to learn to navigate by observing conspecifics (wILKINSON et al., 2010) and have the capacity to discriminate between real objects and pictures of them (wILKINSON et al., 2013).

The Greek tortoise, Testudo graeca, has been studied in terms of population structure and dynamics (LAMBERT, 1982; zNARI et al., 2005), diet (EL MOUDEN et al., 2006) and other biological aspects, such as the influence of testosterone on male reproductive behaviour and space use (SEREAU et al., 2010), but there is a lack of literature concerning cognitive aspects of this species.

The present study focuses on the ability of the Greek tortoise to orient using proximal visual cues in order to escape from a square enclosure. It has been already confirmed for other chelonians that the visual system plays an important role in their daily activities (MäTHGER et al., 2007; NARAzAKI et al., 2013) and related spatial orientation abilities have been described for the red-footed tortoise

23

Chelonoidis carbonarius (wILKINSON et al., 2007, 2009, 2013). when provided with geometrical shapes attached to a curtain surrounding the test maze, the red-footed tortoise did not use them to navigate (wILKINSON et al., 2009). By designing a maze of appropriate complexity and testing a large enough sample to compensate for the limited control, this experiment aims to assess whether the ability to discriminate between simple geometrical shapes actually exists in tortoises and explores the hypothesis that the subjects will require gradually less time to complete a trial-and-error test involving escaping from a box with three “false” and one “true” exit.

MATERIALS AND METHODS Animals and area of study The Greek tortoise inhabits temperate and Mediterranean areas and is unevenly distributed in south-east Romania, following mixed deciduous forests (TORTOISE & FRESHwATER TURTLE SPECIALIST GROUP, 1996; COVACIU-MARCOV et al., 2006). The population found in Topolog forest in Tulcea County has never been surveyed, but sightings are frequently reported by locals (the forest is exploited for timber and the surroundings are used as pastures) between mid-March and late October (A. Glavaschi, personal observation). An area of approximately 10 ha in SE Romania (Tulcea county, 44°50’N, 28°25’E) was surveyed in August 2012.A total of 42 adult specimens (32 males, 10 females) of unknown life histories and health conditions, though all experimentally naïve, were tested. The number of annuli and the overall carapace aspect were used to

24

GLAVASCHI & BEAUMONT

approximate age. Males and females were differentiated according to plastron characteristics: males showed wider openings around the legs, a concavity around the suture between the abdominal scutes, a convex supracaudal scute with the cavity above the tail and the tips of the anal scutes relatively wide apart, whereas in females the leg openings are narrower and the plastron is flat, as well as the supracaudal scute, and the distance between the tips of anal scutes being considerably smaller (LAMBERT, 1982; see CARRETERO et al., 2005, for a schematic representation of the tortoise carapace and plastron).

Figure 1: Schematic representation of the box showing dimensions and the position of each geometrical shape relative to the other three. Door edges not shown.

The experimental device

Procedure

A 45 x 45 x 31 cm cardboard box (square base) was manufactured. The walls were of the same lengths to prevent tortoises from orientating by the shape of the environment, as described above. To reduce the differences to the geometrical shapes available for orientation, a 27 cm wide, 20 cm high door was cut through each wall at equal distances to the corners. Geometrical shapes of similar surface areas were attached on the inside of each door as follows, in a clockwise order when viewed from above: triangle, circle, rectangle and square (Fig. 1). All shapes were made from standard printing paper and painted solid black with watercolors. Paper glue was used for attachment. Because all geometrical shapes used as visual cues were regular and equally unlikely to be encountered in nature, the triangle was randomly selected to be attached to the “true� exit. The door could easily be pushed outwards so that the tortoises could escape. All the other doors were blocked on the outside with adhesive tape.

Tortoises were encountered throughout the day, between 08:00 and 18:00. At the moment of encounter, the individuals were allowed to become familiar of being in close proximity to the experimenter for approximately 20 minutes during which time the experimental setup took place. The box was placed on the nearest flat, shaded area. In some cases, extraneous cues such as tree branches, plants, clouds and stones were visible from inside the box.

Tortoises were always placed in the centre of the box, facing the rectangle (with the correct exit directly behind them). A standard digital stopwatch was used to measure the time needed to locate and operate the correct door. Any other movements performed inside the box were timed and noted. Air temperature was measured using a digital thermometer. The animals were observed from a minimum distance of 1.5 m in order to minimize experimenter effects.

Once outside, each individual was allowed to walk approximately 5m away from the box, while the box was set again for the next trial,

GEOMETRICAL SHAPE DISCRIMINATION IN GREEK TORTOISES

then the animal was placed back inside the box in the same orientation as originally. A trial was considered completed when half of the animal was outside the box. A test consisted of ten consecutive trials for each individual. A fresh piece of apple was placed in front of the correct door as a food reward; however, on no occasion were the tortoises interested in it. Perfume-free wet wipes were used to wipe the walls and floor of the box after each individual had finished the test, to minimize any scent trials that might have influenced subsequent subjects.

The overall time needed to complete the trials, comprising the latency to the first movement and the active search time, were analyzed to determine any decrease that would indicate that learning has occurred.

A trial was considered failed if the animal could not find the exit after 15 minutes of moving around the box or was inactive for 10 minutes, in which case the door was fixed open and the animal allowed to escape. In some cases, the individuals had to be handled so that they faced the open door. An individual was allowed to fail three consecutive trials. If the fourth trial was also unsuccessful, the specimen was not subjected to further testing. The test was also abandoned if the subject showed clear signs of stress (such as urinating, defecating, gular pumping or retracting for more than five minutes) at any stage of the test. To avoid false replicas, tested individuals were marked on the plastron using blue nail polish. After marking, animals were released in the exact location and orientation they were encountered in.

Handling was limited to placing individuals in the box after each completed trial, marking, photographing and, in a few cases, placing the animal facing the correct exit, and this was done with maximum caution.

25

Statistics To assess whether the performance improved between the beginning and the end of the test, differences between the first and last trial were calculated for all variables: latency to the first movement, active search time and overall time. The data set was tested for normality and homogeneity of variance using Shapiro-wilk tests and graphical methods (results not shown). According to these results, wilcoxon signed-rank tests were used to compare between the times (median numbers of seconds) needed for the first, fifth and last trial, to explore the variation in performance. The results from the other trials were not used in statistical tests to avoid any potential errors. Spearman’s correlations were conducted in order to assess whether the latency to the first movement, the active search time and the overall time varied independently from one another or whether there were any interactions.

Potential effects of the activity at the moment of encounter were examined.

Individuals found walking, digging burrows or interacting with conspecifics were classified as being involved in a “high” level of activity, whereas tortoises found hidden under leaves, drinking, feeding or basking were included in the “low” level of activity category. wilcoxon signed-rank tests were conducted to see whether search time was influenced by the activity at the moment of encounter.

To determine whether the subjects actually used the geometrical shapes as a guidance strategy as opposed to simply remembering what direction to follow, the percentage of times the first successful movement was repeated was calculated. Similarly to the method used by RODRÍGUEz et al. (2002),

26

GLAVASCHI & BEAUMONT

the tortoises in the present experiment were considered to follow a certain pattern if 80% (8 out of 10) of the first movements were identical with each other and the first successful movement.

The temperature effects were examined by comparing the results of successful individuals below and above 30°C and by looking for significant differences between the temperatures experienced by successful and unsuccessful individuals. Again, the distribution was explored using Shapiro-wilk tests and wilcoxon signed-rank tests were used for the analyses.

The results were considered statistically significant at a P value of 0.05. All calculations were performed using R statistics package (R DEVELOPMENT CORE TEAM, 2008).

RESULTS Thirty-one of the 42 individuals tested were successful (25 males and six females), i.e. completed 10 trials with or without additional failed trials, and were used in statistical tests. Six of the successful individuals (five males and one female) failed between one and three trials.

The mean difference between the overall time needed to complete the first and last trial is well above 0 (210 ± 195 s).The overall time spent inside the box decreased as the test progressed. Significant differences can be observed between the first and fifth trials (wilcoxon signed-rank test: w = 487, P< 0.001, N = 31; first trial: median time = 269 ± 233 s; fifth trial: median time = 96± 106 s) and also between the first and tenth trials (w = 456, P< 0.001, N = 31; first trial: median time = 269 ± 233 s; tenth trial: median time = 94 ± 155 s).

The performance remained constant during

the second half of the test, as reflected by the lack of significant difference between the fifth and tenth trial (w = 193, P = 0.603, N = 31; fifth trial: median time = 96 ± 106 s; tenth trial: median time = 94 ± 155 s). As illustrated by the error bars in Fig. 2a, individual subjects exhibited different levels of activity.

The main source of variation in the overall time is represented by its second component, the time used to actively explore the box.

Similarly, this decreases significantly during the first part of the test (w = 480, P<0.001, N = 31; first trial: median time = 220 ± 235 s; fifth trial: median time = 55 ± 114 s) and the performance is maintained until the end (w = 470.5, P<0.001, N = 31; first trial: median time = 55 ± 114 s; tenth trial: median time = 45 ± 150 s), with no significant improvement between the fifth and tenth trial (w = 188, P = 0.530, N = 31; fifth trial: median time = 55 ± 114 s; tenth trial: median time = 45 ± 150 s) (Fig. 2b). Although not as obviously as the other variables, latency also decreases. At the beginning ofthe fifth trial, tortoises take less time to start exploring the box than in the first trial (w = 288, P = 0.004, N = 31; first trial, median latency = 26 ± 53.5 s; fifth trial: median latency = 0 ± 45.5 s) and the performance remains the same until the tenth trial (w = 110, P = 0.603, N = 31; fifth trial: median latency = 0 ± 45.5 s; tenth trial: median latency = 10 ± 35 s) (Fig. 2c). As illustrated by the error bars in Figs. 2a-c, wide variation between individual performances was observed. when all the variables are plotted together (Fig. 2d) it is readily visible that the overall time and the active search time vary similarly whereas the latency remains constant.

This final point is further supported by the strong correlation reported by Spearman’s test

GEOMETRICAL SHAPE DISCRIMINATION IN GREEK TORTOISES

27

Figure 2: Variation of the time spent inside the box across the 10 trials. As error bars representing standard errors suggest, wide variation between individuals in the overall time, latency and search time was observed. (a) Overall time, between the moment of release and the moment of escape. (b) Time passed until the individual’s first action. Detraction was not considered a “first movement”. (c) Time spent actively exploring the enclosure, after the first movement and until escape. (d) All before-mentioned variables plotted together for comparison purposes.

(Fig. 3a) (rs= 0.951, P< 0.001). Analysis of the relationship between the overall time and latency also returns a positive correlation, but not as strong as the one between overall search time and active search time (rs= 0.697, P = 0.029; Fig. 3b). No statistically significant relationship was found between latency and active search time (rs= 0.55, P = 0.099; Fig. 3c).

Performance (measured by variation in the search time) was not influenced by the activity at the moment of encounter at any stage of the test. Individuals involved in a high level of activity (median search time: 276 ± 282 s, N = 19) did not perform better than those less active (median search time: 206.5 ± 126 s, N = 12) during the first trial

28

GLAVASCHI & BEAUMONT

(w = 118, P = 0.889) and this was maintained for the fifth trial (w = 131.5, P = 0.490; high level of activity: median = 88 ± 127 s, N = 19; low level of activity: median = 49.5 ± 80 s, N = 12) and for the tenth trial (w = 135.5, P = 0.394; high level of activity: median = 81 ± 77 s, N = 19; low level of activity: median = 41.5 ± 82 s, N = 12).

Only 11 of the 31 subjects showed consistency in the path followed after being reintroduced in the box, i.e. the first successful movement was repeated for at least eight trials. One of these subjects was a female and the rest were males.

The air temperature did not seem to influence whether the subjects completed or failed the trials, as successful individuals did not perform the test at a significantly different temperature than unsuccessful ones (w = 203, P = 0.359; successful individuals: median temperature = 30.1°C, N = 31; unsuccessful individuals: median temperature = 30.1°C, N = 11).

DISCUSSION

Figure 3: Correlations between variables collected during trials. (a) Graph showing strong positive correlation between the overall time needed to complete the trials and the time spent actively exploring the box. (b) Graph showing weak positive correlation between overall time needed to complete the trials and latency to the first movement. (c) Graph showing independent variation of the active search time and latency to the first movement.

This study demonstrates that Greek tortoises are capable of finding and operating the correct door in order to escape from the experimental set-up used. For all but two subjects, the time needed to complete the tenth trial was less than the time needed to complete the first trial, which is the first indication of the development of a strategy of some sort. Although the overall time needed to complete the trials decreases in a fashion that readily suggests the acquisition and learning of a certain escape mechanism, the active search time is a better indicator of an improvement in performance variation.

Latency remained relatively constant throug-

GEOMETRICAL SHAPE DISCRIMINATION IN GREEK TORTOISES

hout the tests (Figs. 2b and 2d) owing to the fact that the subjects were reluctant to perform any movements soon after being placed (back) into the box. Therefore, latency represents an increasingly higher proportion of the overall time as the active search time decreases. The active search time shows a more realistic variation of the tortoises’ performance and thus gives a more reliable measurement.

The fact that tortoises spent significantly less time exploring the box as the tests progressed clearly suggests that they have learned and used a strategy. At some point during the test, each individual stood immobile in front of each wall, looking directly forwards, suggesting that they were scanning the surroundings. The square shape of the enclosure prevented orientation according to large scale geometry, as reported for a wide variety of species (see above), thus the local cues (i.e. the geometrical shapes attached to the walls) are likely to have been used.

As illustrated in Figs. 2c and 2d, there is a slight increase in the search time during the last trial compared to the previous five trials, and the same trend reflects on the overall time (Figs. 2a and 2d). It is suggested for other reptile species that when an increase in familiarity of the environment is accompanied by a decrease in activity, this could be attributed to the fact that the subjects become comfortable within the enclosure (HOLTzMAN et al., 1999; Chiszar et al., 1976, cited in HOLTzMAN et al., 1999). It is very unlikely that this is the case here. Certain individuals showed clear signs of stress, such as urinating, defecating, fighting vigorously when handled and retracting when being placed back inside the box after the completion of a trial, which is expected from wild, expe-

29

rimentally naïve animals. This slight increase during the last part of the test is probably due to exhaustion, as most of the individuals moved around the box constantly, climbing and scratching the walls.

The use of extra-maze cues during orientation tasks is reported for other species, including chelonians (LóPEz et al., 2000, 2001, 2003; wILKINSON et al., 2009). In the present study, as it was impossible to completely isolate the box from the surroundings, elements of the environment, such as tree branches and tall plants, were visible from within. A common behaviour was climbing the walls, usually at the corners, leaning against with the front limbs, looking outside and trying to escalate. Thus, the hypothesis that tortoises used the environmental cues as a guidance strategy cannot be ruled out.

The activity at the moment of encounter was expected to reflect on the subjects’ behaviour inside the box. Individuals involved in a less energy demanding activity (resting, basking, feeding) were expected to require a longer time to complete the trials, while more active individuals (walking) were expected to complete the trials faster since they were already involved in a navigation process. This hypothesis was not supported, suggesting that the ability to use geometrical shapes to navigate is part of a set of cognitive processes that can be employed whenever the circumstances require it.

The fact that less than half of the successful individuals met the significance criterion of 80% first movements identical to the first successful one suggests that repeated transfers back into the box are disorienting and the subjects cannot maintain a constant path, requiring a certain amount of time to compute the spatial arrangement of the arena.

30

GLAVASCHI & BEAUMONT

There is evidence of different learning abilities and spatial use between sexes, which is possibly accentuated during breeding season (JACOBS, 1996). Male Greek tortoises do not use colours, vocalisations or any other advertisements to attract mates but have to actively search for them and consequently are expected to perform better in spatial tasks than females. A biased sex ratio towards males (24 out of the 31 subjects), while not necessarily unusual (see MEEK, 1985 for a Hermann’s tortoise population survey), did not allow this assumption to be tested.

Tests for the importance of olfaction in reptile spatial tasks have provided mixed results (GRAHAM et al., 1996; wILKINSON et al., 2013). Gular pumping, which is linked to the use of olfaction (GRAHAM et al., 1996) was observed in a few cases. The paint used for the geometrical shapes had a characteristic smell, however this was uniformly spread. Although the procedure was designed to minimize odour trails between individuals, no measures were taken to eliminate any odour traces between the trials of the same test, so the possibility that the tortoises oriented according to their own odour traces cannot be ignored.

It has been reported for desert tortoises, Gopherus agassizii, that at temperatures higher than 29°C a change in behaviour towards seeking cover occurs (HINDERLE, 2011).

Exposure to environmental temperatures higher that 40°C for more than one hour are unsafe for Greek tortoises, and body temperatures higher than 38°C for prolonged periods hasten dehydration (LAGARDE et al., 2012). In this particular study, temperature did not influence the outcome of the test (failed/completed), but a more detailed impact on the subjects’ performance is not readily obvious.

Due to its nature, the present study has a series of inevitable limitations, as with all behavioural studies conducted on wild animals.

Although it can be approximated with sufficient confidence whether the tortoises were adults or juveniles, the exact age was not known. Also, nothing was known about the life histories of the individuals or their health conditions. It has been shown for other species that certain diseases, in the infective phase, impair learning abilities (JACOBS, 1996). There is a high chance that the majority of tortoises in this study have never encountered humans before. The carapaces and plastrons of some specimens showed signs of accidents that may have left traumas.

The low degree of comfort around humans is also reflected by the fact that all individuals ignored the food reward, as their only interest once outside was to move as far away as possible.

The heterogeneity of the sample is best reflected by the number of individuals that failed the test completely (26% of the entire sample), firstly, and secondly by the widely variable behaviour of the successful individuals, from different points of view. Many different levels of performances were observed, as seen in Fig. 2. The lack of training prior to the tests is most likely responsible for the fact that seven individuals needed between one and three extra trials before being able to find the exit by themselves.

Unlike other animals tested for geometrical shape determination, such as the fiddler crabs (LANGDON & HERRNKIND, 1985) or hermit crabs (DIAz et al., 1995) which were assigned ecologically-relevant tasks, the Greek tortoises in the present experiment were tested in an artificial environment. They are not faced with similar tasks in their natural habitat, but the trials provide insights into their cognitive processes, including learning and memory.

GEOMETRICAL SHAPE DISCRIMINATION IN GREEK TORTOISES

This study supports the idea that reptiles are capable of performing similarly to mammals and birds in spatial tasks. From a spatial orientation point of view, chelonians are unique among reptiles in that they tend to navigate more similarly to birds and mammals than other reptilian groups (wILKINSON & HUBER, 2012). Since their position within the reptile group is uncertain (mitochondrial DNA analysis suggests chelonians are closely related to birds and crocodiles while morphological features point towards a closer relatedness to lizards and snakes (zARDOYA & MEYER, 2001; wILKINSON & HUBER, 2012), studies of cognitive abilities might provide further insights into the group’s evolutionary history.

Our experiment supports the hypothesis that Greek tortoises are able to discriminate between simple geometrical shapes. Further studies should focus on the importance of this ability for navigation in the species’ natural environment.

Acknowledgement The study was approved by the University of Derby bioethics committee and all data collection procedures complied with animal welfare legislation. The authors thank the academic and technical staff of the School of Biological Sciences at the University of Derby and field assistants, A. and C. Pandrea for volunteering to help with data collection.

REFERENCES ABLE, K.P. (1991). Common themes and variation in animal orientation systems.

American Zoologist 31:157-167.

CARRETERO, M.A.; zNARI, M.; HARRIS, D.J. & MACé, J.C. (2005). Morphological

31

divergence among population of Testudo graeca from west-central Morocco. Animal Biology 55:259-279.

CHENG, K. (1986) A purely geometric module in the rat’s spatial representation.

Cognition 23:149-178.

CHENG, K. & GALLISTEL, C.R. (1984).

Testing the geometric power of an animal’s spatial representation, In H.L. Roitblat, T.G. Bever & H.S. Terrace (eds.) Animal Cognition. Erlbaum Associates, Hillsdale, NJ, USA, pp. 409-423.

CHIUSSI, R. & DIAz, H. (2002). Orientation of the fiddler crab, Uca cumulanta: responses to chemical and visual cues. Journal of Chemical Ecology 28:1787-1796.

COVACIU-MARCOV, S.-D.; GHIRA, I.; CICORTLUCACIU, A.-Ş.; SAS, I.; STRUGARIU, A. & BOGDAN, H.V. (2006). Contributions to knowledge regarding the geographical distribution of the herpetofauna of Dobrudja, Romania. North-Western Journal of Zoology 2:88-125.

DEIPOLYI, A.; SANTOS, L. & HAUSER, M.D. (2001). The role of landmarks in cottontop tamarin spatial foraging: evidence for geometric and non-geometric features.

Animal Cognition 4:99-108.

DIAz, H.; FORwARD, R.B., JR.; ORIHUELA, B. & RITTSCHOF, D. (1994). Chemically stimulated visual orientation and shape discrimination by the hermit crab Clibanarius vittatus (Bosc). Journal of Crustacean Biology 14:20-26.

DIAz, H.; ORIHUELA, B. & FORwARD, R.B., JR. (1995). Visual orientation of postlarval and juvenile mangrove crabs. Journal of Crustacean Biology 15:671-678.

EL MOUDEN, E.H.; SLIMANI, T.; BEN KADDOUR, K.; LAGARDE, F.; OUHAMMOU,

32

GLAVASCHI & BEAUMONT

A. & BONNET, X. (2006). Testudo graeca graeca feeding ecology in an arid and overgrazed zone in Morocco. Journal of Arid Environments 64:422-435.

GALLISTEL, C.R. (1990). The Organization of Learning. The MIT Press, Cambridge, MA, USA. GOUTEUX, S.; THINUS-BLANC, C. & VAUCLAIR, J. (2001). Rhesus monkeys use geometric and nongeometric information during a reorientation task. Journal of Experimental Psychology: General 130:505-519.

GRAHAM, T.; GEORGES, A. & MCELHINNEY, N. (1996). Terrestrial orientation by the Eastern Long-necked Turtle, Chelodina longicollis, from Australia. Journal of Herpetology 30:467-477.

HERMER, L. & SPELKE, E. (1996). Modularity and development: the case of spatial reorientation. Cognition 61:195-232.

HINDERLE, D. (2011). Desert Tortoises (Gopherus agassizii) and Translocation: Homing, Behavior, Habitat and Shell Temperature Experiments. M.Sc. Thesis, San Diego State University, San Diego, CA, USA. D.A.; HARRIS, T.w.; HOLTzMAN, ARANGUREN, G. & BOSTOCK, E. (1999).

Spatial learning of an escape task by young corn snakes, Elaphe guttata guttata.

Animal Behaviour 57:51-60.

JACOBS, L.F. (1996). Sexual selection and the brain.

Trends in Ecology and Evolution 11:82-86.

LAGARDE, F.; LOUzIzI, T.; SLIMANI, T.; EL MOUDEN, H.; BEN KADDOUR, K.; MOULHERAT, S. & BONNET, X. (2012).

Bushes protect tortoises from lethal overheating in arid areas of Morocco. Environmental Conservation 39:172-182.

LAMBERT, M.R.K. (1982). Studies on the growth, structure and abundance of the

Mediterranean spur-thighed tortoise, Testudo graeca in field populations.

Journal of Zoology 196:165-189.

LANGDON J.w. & HERRNKIND, w.F. (1985).

Visual shape discrimination in the fiddler crab, Uca pugilator. Marine Behavior and Physiology 11:315-325.

LóPEz, J.C.; RODRÍGUEz, F.; GóMEz, Y.; VARGAS, J.P.; BROGLIO, C. & SALAS, C. (2000). Place and cue learning in turtles.

Animal Learning and Behavior 28:360-372.

LóPEz, J.C.; GóMEz, Y.; RODRÍGUEz, F.; BROGLIO, C.; VARGAS, J.P. & SALAS, C. (2001). Spatial learning in turtles. Animal Cognition 4:49-59.

LóPEz, J.C.; VARGAS, J.P.; GóMEz, Y. & SALAS, C. (2003). Spatial and non-spatial learning in turtles: the role of medial cortex.

Behavioural Brain Research 143:109-120.

MäTHGER, L.M.; LITHERLAND, L. & FRITSCHES, K.A. (2007). An anatomical study of the visual capabilities of the green turtle, Chelonia mydas. Copeia 2007: 169-179.

MEEK, R. (1985). Aspects of the ecology of Testudo hermanni in southern Yugoslavia.

British Journal of Herpetology 6:437-445.

NARAzAKI, T.; SATO, K.; ABERNATHY, K.J.; MARSHALL, G.J. & MIYAzAKI, N. (2013).

Loggerhead turtles (Caretta caretta) use vision to forage on gelatinous prey in mid-water. PLoS ONE 8: e66043.

ORIHUELA, B.; DÍAz, H.; FORwARD, R.B., JR. & RITTSCHOF, D. (1992). Orientation of the hermit crab Clibanarius vittatus (Bosc) to visual cues: effects of mollusc chemical cues. Journal of Experimental Marine Biology and Ecology 164:193-208.

R DEVELOPMENT CORE TEAM (2008). R: A Language and Environment for Statistical Computing: An Online Reference. R

GEOMETRICAL SHAPE DISCRIMINATION IN GREEK TORTOISES

Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.rproject.org/. Retrieved on 07/17/2013.

RODRÍGUEz, F.; LóPEz, J.C.; VARGAS, J.P.; GóMEz, Y.; BROGLIO, C. & SALAS, C. (2002). Conservation of spatial memory function in the pallial forebrain of reptiles and ray-finned fishes. Journal of Neuroscience 22:2894-2903.

SCHLUESSEL, V.; FRICKE, G. &BLECKMANN, H. (2012). Visual discrimination and object categorization in the cichlid Pseudotropheus sp. Animal Cognition 15:525-534.

SEREAU, M.; LAGARDE, F.; BONNET, X.; EL MOUDEN, E.H.; SLIMANI, T.; DUBROCA, L.; TROUVé, C.; DANO, S. & LACROIX, A. (2010). Does testosterone influence activity budget in the male Greek tortoise (Testudo graeca graeca)? General and Comparative Endocrinology 167:181-189.

SIEBECK, U.E.; LITHERLAND, L. & wALLIS, G.M. (2009). Shape learning and discrimination in reef fish. Journal of Experimental Biology 212:2113-2119.

V.A.; BISAzzA, A. & SOVRANO, VALLORTIGARA, G. (2002). Modularity and spatial reorientation in a simple mind: encoding of geometric and nongeometric properties of a spatial environment by fish. Cognition 85: B51-B59.

SOVRANO, V.A.; BISAzzA, A., & VALLORTIGARA, G. (2003). Modularity as a fish (Xenotoca eiseni) views it: conjoining geometric and nongeometric information for spatial reorientation. Journal of Experimental Psychology: Animal Behavior Processes 29:199-210.

SUBOSKI, M.D. (1992). Releaser-induced recognition learning by amphibians and reptiles.

Animal Learning and Behavior 20:63-82.

33

TORTOISE AND FRESHwATER TURTLE SPECIALIST GROUP (1996). Testudo graeca.

The IUCN Red List of Threatened Species, Gland, Switzerland. Available at: http://www.iucnredlist.org/details/full/21 646/0. Retrieved on 07/17/2013. wILKINSON, A. & HUBER, L. (2012) Cold-blooded cognition: reptile cognitive abilities, In T.K. Shackelford & J. Vonk (eds.) The Oxford Handbook of Comparative Evolutionary Psychology, Oxford University Press, Oxford, UK, pp. 129-144. wILKINSON, A.; CHAN, H.-M. & HALL, G. (2007). Spatial learning and memory in the tortoise (Geochelone carbonaria). Journal of Comparative Psychology 121:412-418. wILKINSON, A.; COwARD, S. &HALL, G. (2009). Visual and response-based navigation in the tortoise (Geochelone carbonaria). Animal Cognition 12:779-787. wILKINSON, A.; KUENSTNER, K.; MUELLER, J. & HUBER, L. (2010). Social learning in a non-social reptile (Geochelone carbonaria). Biology Letters 6:614-616. wILKINSON, A.; MUELLER-PAUL, J. & HUBER, L. (2013). Picture-object recognition in the tortoise Chelonoidis carbonaria.

Animal Cognition16:99-107. wYSTRACH, A. & BEUGNON, G. (2009). Ants learn geometry and features. Current Biology 19:61-66. zARDOYA, R. & MEYER, A. (2001). The evolutionary position of turtles revised.

Naturwissenschaften 88:193-200. zNARI, M.; GERMANO, D.J. & MACé, J.-C. (2005). Growth and population structure of the Moorish Tortoise (Testudo graeca graeca) in westcentral Morocco: possible effects of over-collecting for the tourist trade. Journal of Arid Environments 62:55-74.

34

Basic and Applied Herpetology 28 (2014): 35-50

Effect of prey availability on growth-rate trajectories of an aquatic predator, the viperine snake Natrix maura Aikaterini Filippakopoulou1, Xavier Santos2,*, Mónica Feriche3, Juan M. Pleguezuelos3, Gustavo A. Llorente1 Departament de Biologia Animal, Universitat de Barcelona, Barcelona, Spain.

CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Vairão, Portugal.

3 Departamento de Zoología, Universidad de Granada, Granada, Spain.

1 2

* Correspondence: CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, 4485-661 Vairão, Portugal. Phone: +351 252660400, Fax: +351 252661780, E-mail: xsantossantiro@gmail.com

Received: 17 January 2014; received in revised form: 29 April 2014; accepted: 3 May 2015.

The energy gained by an organism is used for maintenance, growth and reproduction. In habitats with limited resources, these processes compete for available energy and may induce intraspecific variation in body condition, growth trajectories and reproductive output. we tested the hypothesis that populations exposed to higher food availability are able to grow faster, and attain larger body sizes in the viperine snake (Natrix maura). we estimated snake age by counting growth lines in the skull’s ectopterygoid bone, and compared body size growth curves from three Iberian populations exposed to temporal variation of food resources availability. In the three localities, and in males and females, the growth curves followed a quadratic function that tended to an asymptotic value as growth slowed down. Growth curves showed slower growth rates and an early asymptote for males, in agreement with the reverse sexual dimorphism in body size of this species. we also detected interpopulational differences, with the Ebro Delta population exhibiting slower growth rates and smaller asymptotic body size in both sexes. This population inhabits rice fields with an artificial waterflow cycle, a condition that implies a shorter period of prey availability for snakes, compared to the other two populations, where prey is available for longer periods of time. Moreover, high proportion of snakes with tail breakage in this population indicated high predation pressure. These environmental conditions suggest that food availability and predation pressure may be concurrently acting to produce smaller N. maura at the Ebro Delta than at the other two populations.

Key words: energy allocation; life-history traits; Natrix maura; quadratic regression; skeletochronology; snake.

Efecto de la disponibilidad de presas en las trayectorias de crecimiento de un depredador acuático, la culebra viperina Natrix maura. Los organismos invierten su energía en mantenimiento, crecimiento y reproducción.

En hábitats con una disponibilidad de recursos limitada, estos procesos compiten por la energía disponible y pueden inducir variación intraespecífica en la condición corporal, trayectorias de crecimiento y rendimiento reproductivo. Hemos comprobado en la culebra viperina (Natrix maura) la hipótesis de que las poblaciones con una mayor disponibilidad de recursos son capaces de crecer más rápido y alcanzar tamaños corporales mayores. En este estudio estimamos la edad de los individuos contando las líneas de crecimiento en el hueso pterigoideo del cráneo, y comparamos las curvas de crecimiento corporal de tres poblaciones ibéricas expuestas a variación temporal en la disponibilidad de recursos alimentarios. En las tres localidades, y tanto en machos como en hembras, las curvas de crecimiento siguieron una función cuadrática con tendencia a valores asintóticos a medida que el crecimiento disminuía. Las curvas de crecimiento mostraron tasas menores y una asíntota más temprana en machos, de acuerdo con el dimorfismo sexual reverso en tamaño corporal en esta especie. Asimismo detectamos diferencias interpoblacionales, con la población del delta del Ebro mostrando tasas de crecimiento menores y un menor tamaño corporal asintótico en los dos sexos. Esta población ocupa arrozales con ciclos artificiales de disponibilidad de agua, una condición que implica un periodo más corto de disponibilidad de presas en comparación con las otras dos poblaciones, donde las presas están disDOI: http://dx.doi.org/10.11160/bah.14001/

Supplementary material available online

36

FILIPPAKOPOULOU ET AL.

ponibles durante periodos de tiempo más prolongados. Por otra parte, una mayor proporción de individuos con colas partidas sugiere una mayor presión de depredación. Estas condiciones ambientales sugieren que la disponibilidad de alimento y la presión de depredación pueden estar actuando simultáneamente produciendo N. maura de un tamaño menor en el Delta del Ebro que en las otras dos poblaciones.

Key words: capacidades cognitivas; navegación; orientación; Rumanía; señales visuales; Tulcea.

Organisms have the capacity to extract energy from their environment, process that energy, and allocate it to maintenance and production (CONGDON et al., 1982, 2001; MCNAB, 2002). Energy used for maintenance covers two targets: i) standard maintenance, i.e. the basal energetic cost of living, and ii) activity maintenance, i.e. the energy required for activities such as digestion and locomotion. The energy allocated to production supports growth and reproduction. For many organisms, most energy is used for maintenance and far less is used for production (DURANT et al., 2007). For example, nonavian reptiles spend 80% of their energy budget on maintenance and 20% on production (CONGDON et al., 1982).

Resources available in the environment are often limited, and tasks such as maintenance, growth, and reproduction may compete for energy to optimise their respective output values (LESSELLS, 1991; STEARNS, 1992). Consequently, the allocation of energy to one particular process could occur at the expense of others (STEARNS, 1976, 1989; SHINE, 1980). Foragers occasionally face periods in which food is scarce or even non-existent, and stress caused by a reduction in prey availability may constrain the rate of energy intake (REzNICK et al., 1990). In these situations, organisms may allocate less energy to growth and reproduction, and more to maintenance, in order to increase their chances of survival (FORSMAN & LINDELL, 1991).

Snakes are an adequate group for studying a variety of biological and ecological aspects related to how the partition of energy to different competing needs is affected by resource levels (FORSMAN & LINDELL, 1996; SHINE et al., 2002; BOBACK, 2003). Most female snakes are capital breeders, which accumulate body reserves for long periods before reproduction for fuelling vitellogenesis (BONNET et al., 1994; NAULLEAU & BONNET, 1996). They continue to grow after attaining reproductive status (ANDREwS, 1982), and therefore adult body size and reproductive output can interact and vary depending on the local conditions of prey availability (AUBRET & SHINE, 2007). How food availability drives some snake reproductive parameters (i.e. reproductive outputs) has been widely studied in snakes (reviewed in SHINE, 2003). In contrast, few studies have examined the effects of food availability on snakes’ growth trajectories, due to the inherent complexity of long-term monitoring studies. Snakes show a high degree of ontogenetic plasticity, and environmental factors impacting early life stages can modify later growth rates (MADSEN & SHINE, 1993; O’STEEN, 1998; AUBRET et al., 2004). In this context, we hypothesize that intraspecific differences in growth trajectories and / or reproductive output will appear among populations under different availability of food resources, ultimately affecting the maximum body size attained by snakes.

GROWTH-RATE TRAJECTORIES OF SNAKES

we examined this hypothesis within the viperine snake Natrix maura, an aquatic predator that feeds on a wide range of prey types (SANTOS, 2004) and whose diet is modulated by the availability of aquatic prey (SANTOS et al., 2000). In this species, seasonal variation in prey availability influenced the amount of energy stored in several body compartments, and affected reproductive output (SANTOS & LLORENTE, 2004; SANTOS et al., 2007). when prey were scarce, N. maura delayed its reproductive timing until females obtained sufficient reserves (SANTOS et al., 2005).

These results highlight how food availability may influence energy-demanding processes in this aquatic snake.

In this study, we examined how preyavailability regimes may affect intraspecific growth patterns and offspring size in N. maura. we hypothesized that populations under different prey-availability regimes differ in their growth-rate responses due to conflicts in energy allocation between energydemanding processes (e.g. growth and reproduction). Natrix maura shows strong sexual dimorphism in body size, as females are larger and achieve sexual maturity at larger sizes than males (SANTOS, 2004), a feature that allows grow-rate trajectories to be compared intersexually. To analyse inter-population and sexual differences in growth rates, we measured the growth trajectories of three N. maura populations inhabiting two natural habitats, a wetland and a river, and one artificial habitat with high food availability, a fish farm. we expect faster growth rates in the larger sex (females), and in populations that experience longer periods of prey availability irrespective of sex.

37

MATERIALS AND METHODS Study area Natrix maura is a medium-sized aquatic snake that inhabits western Mediterranean natural (ponds, rivers, marshes, streams) and artificial water bodies (SANTOS, 2004). we examined 168 N. maura specimens (in collections in the Animal Biology Departments at the Universities of Barcelona and Granada), from three Iberian populations with different environmental characteristics. Each locality was sampled to measure prey availability for viperine snakes, as described below.

The Ebro Delta (ca. 0º 45’ E, 40º 42’ N, 5 m above sea level) is a wetland partially covered by rice fields. Rice-crop cycles cause disturbances to aquatic species due to changes in the regime of water flow. Canals and rice fields overflow from April to October, when they dry up until the following April. we studied 93 individuals of N. maura captured in 1990 and 1991. The snake’s diet at this population was composed of the green frog Pelophylax perezi and two fish species Cyprinus carpio and Gambussia holbrooki (SANTOS et al., 2000). Prey availability was estimated by sampling 4-6 canals monthly, from April to November 1991, as this is the habitat most frequently used by N. maura for foraging (SANTOS & LLORENTE, 1998).

Samples were taken using a 2 m hand net (60 x 60 cm, 1.8 mm mesh). The net was positioned near the bottom of the canal, and moved unidirectionally along 10 meter transects, collecting fish and other prey types.

This method efficiently samples all vertebrates, except large fish (FASOLA, 1986), but

38

FILIPPAKOPOULOU ET AL.

these specimens / taxa are not consumed by the viperine snake (SANTOS & LLORENTE, 1998). Collected prey specimens were identified to the species level, measured (± 1 mm), and their dry weight mass calculated by the linear regressions of dry mass on body length (biomass; GONzáLEz-SOLÍS et al., 1996). we then calculated N. maura’s prey biomass per square meter of canal to obtain monthly variation in available biomass in the habitat.

The Matarranya River (ca. 0º 12’ E, 41º 13’ N, 508 m above sea level) has a typical Mediterranean water regime, with seasonal flow changes related to rainfall periods; the highest flows occur in spring and autumn, and the lowest in summer. we studied 30 female N. maura individuals collected between 1984 and 1986 (the absence of males precluded a sexual comparison at this population). The snake’s diet was composed of P. perezi, and four fish species, Barbus graellsii, Chondrostoma miegii, Squalius cephalus and Salaria fluviatilis (SANTOS et al., 2006).

Fish were sampled every two months from 1984 to 1986. Surveys were performed with standard electrofishing equipment (device of direct current, 4500 w generator, working voltage of 300-400 V, intensity of 1.5-2.0 A, and a 30 cm anode), efficient for estimating fish densities (BOHLIN et al., 1989).

Electrofishing was conducted three times in river sections ca. 100 m long previously confined with nets. Captured fish were identified to the species level, counted, weighed (± 0.1 g), measured (± 1 mm), and released at the localities they were caught. Abundance estimates were made using the zippin (1958) method and the CAPTURE software (white et al., 1978).

Riofrío (4º 10’ w, 37º 10’ N, 485 m above sea level) is a fish farm in the south of the Iberian Peninsula devoted to raising Oncorhynchus mykiss. we studied 45 N. maura collected between 1988 and 1990; their diet was exclusively composed by fish (J.M. Pleguezuelos, unpublished data). Data on number of fish per water volume (prey availability) and their average size were provided by fish farmers. we used this information to calculate fish wet mass per square meter of water.

No snakes were killed for this study.

Snout-vent length (SVL) of individuals at the time of collection was available for the Ebro Delta and the Matarranya River populations. In the Riofrío fish farm, snakes were killed by fish farmers to reduce predation upon fish, and we obtained body-size measures from preserved specimens. The procedure to estimate fresh body size of the snakes is explained below.

In most of its Iberian range, N. maura becomes active in March (JAéN & PéREzMELLADO, 1989; SANTOS & LLORENTE, 2001). Although N. maura may be occasionally active in sunny winter days (SANTOS & LLORENTE, 2001; MALKMUS, 2008), experimental studies demonstrated that digestion stops and prey are regurgitated when body temperature falls below 10ºC (HAILEY & DAVIES, 1987a). Thus, snakes are typically active in water temperatures above 13.017.8ºC in Iberia (HAILEY et al., 1982; JAéN & PéREz-MELLADO, 1989). At the Ebro Delta, field observations indicate that N. maura starts its activity when air temperature is ca.

12ºC (authors’ personal observations; SANTOS, 2004), thus, we assumed that snakes were not active below this temperature.

GROWTH-RATE TRAJECTORIES OF SNAKES

To determine the foraging period for each population, we collated temporal variation in prey availability and mean air temperatures, the latter obtained from the Agencia Estatal de Meteorología. As explained previously, food availability was measured with different methods at each population. However, our objective was not to compare the amount of food availability among the sites, but to know when prey were available at each study site. we assumed that foraging activity started in all three study sites when prey were available and air temperature was higher than 12ºC. Snake body size and age we measured the snout-vent length (SVL) of freshly caught individuals from the Ebro Delta and Matarranya River populations using a cord placed along the mid-dorsal line of the body. In general, preserved animals (in 75% ethanol) from the Riofrío population had shrunk. To compare SVL measurements from the three populations, we estimated the SVL of Riofrío at the time of collection following the procedures outlined by SANTOS et al. (2011). we estimated the snakes’ ages by skeletochronology (CASTANET et al., 1977). Previous studies in N. maura demonstrated that the ectopterygoid is a suitable flat bone to observe growth marks (HAILEY & DAVIES, 1987a).

Likewise, wAYE & GREGORY (1998) detected little variation in the number of layer counts between the caudal vertebrae and the ectopterygoid in Thamnophis spp. garter snakes from Canada; 20 out 37 (54%) of the animals examined by these authors had the same number of growth layers in both bones, and only four individuals (10.8%) showed more

39

layers in the ectopterygoid bone than in the caudal vertebrae (maximum difference was two layers). we removed the right ectopterygoid from 168 individuals of N. maura. To facilitate skeletochronology procedures, bones were photographed with an optic microscope (Leitz Dialux 20) at 40 X magnification.

Each photograph was analysed carefully, and growth marks counted following procedures described in PEABODY (1961), i.e. each dense line in the bone corresponded to an active osteogenesis period followed by low or lack of osteogenesis (no visible marks). To prevent inaccurate interpretations influenced by bone size (wAYE & GREGORY, 1998), we carried out a blind test: a code was assigned to each bone, and growth mark numbers were not assigned to specific bones until all readings were completed. Additionally, we counted the number of layers on caudal vertebrae of 10 randomly selected N. maura specimens, following procedures by wAYE & GREGORY (1998). Vertebrae were decalcified with 4% formaldehyde and 3% nitric acid during 1 h 45 min, and sections of 14 mm thickness were made with a cryomicrotome and stained with 0.05 Ehrlich's Haematoxilyn. The number of layers on caudal vertebrae and ectopterygoid bones were identical for each of the ten individuals examined (Fig. S1), supporting the reliability of our procedure for aging snakes.

Data analysis After checking that body sizes were evenly distributed throughout the entire age range, we verified whether SVL significantly differed between populations using Analysis of the Variance (ANOVA). Male and female

40

FILIPPAKOPOULOU ET AL.

Figure 1: Temporal variation in food availability (dotted line) and environmental temperature (dashed line) for the three populations studied. To establish the foraging period for each population (grey line), we assumed that foraging activity started when prey availability was different from zero and the environmental temperature was higher than 12ยบC (solid black line).

N. maura were analysed separately because of sexual dimorphism in body size. To estimate growth curves, we conducted quadratic and logistic regressions between the estimated age and SVL for both sexes in the three populations with STATISTICA 8.0 (STATSOFT, 2007) and MatLab 7.0 (MATHwORKS, 1996) softwares. Once we confirmed our data fitted a quadratic regression function, we performed intersexual and interpopulation comparisons for both sexes in growth trajectories.

Sexual and interpopulation differences in growth rates were tested by comparing line slopes using SMATR Software (FALSTER et al., 2006). This program adjusts comparative categories to a linear regression model and conducts two types of tests: the standardised

major axis test (SMA), which reports growthrate differences, and the wald test, which reports elevation differences that indicate different body sizes at birth. Finally, the maximum of each quadratic function was calculated to find the asymptotic growth point. This point indicates the age at which growth slows, and the maximum size reached by the study population.

RESULTS Estimates of food-availability Comparisons of temporal variation in air temperatures and food availability at each population (Fig. 1) suggested that the fora-

41

GROWTH-RATE TRAJECTORIES OF SNAKES

ging period estimates is six months for the Ebro Delta population, and slightly longer than seven months at the Matarranya River and the Riofrío fish farm. In the Ebro Delta, rice-field farmers regulate the water flow to keep the rice fields dry until the end of April, and consequently prey are not available for water snakes until this period (SANTOS et al., 2000). At the Riofrío fish farm, fish are available the entire year, and food availability varies due to fish cohorts replacement every three months. In summary, as food resources were available all year at Matarranya and Riofrío, foraging activity of viperine snakes in these localities is likely regulated by environmental temperature.

Age estimates and growth curves The estimated age of N. maura, calculated by counting the ectopterygoid growth marks ranged from 0 to 22 years (the oldest snake was a female from the Matarranya River, 595 mm SVL). The relationship between estimated age and SVL was adjusted in all

cases to quadratic and logistic distributions, with a goodness of fit ca. 80% (Table 1).

Because both adjustments had a similar coefficient of determination, we chose the quadratic regression, which allowed us to calculate the asymptotic curve more easily.

The equations of the quadratic regressions indicated that the growth of males from the Ebro Delta and Riofrío slowed down at the same estimated age (18.9 and 18.7 years respectively; Table 1), whereas the asymptotic point for Ebro Delta females was 19.7 years. This finding suggests that females continue growing for a longer period than males. Females from Matarranya and Riofrío apparently exhibited linear growth; this could be an artefact as some individuals reached the largest SVL measured in this study. Thus, to estimate the maximum size attained by females in the Matarranya and Riofrío populations, we assumed 20 years as the asymptotic point, based in the maximum age registered for females in the Ebro Delta and southeastern Iberia (HAILEY & DAVIES, 1987b).

Table 1: Quadratic and logistic goodness of fit (R2), and quadratic equation of the relationship between age and body size in Natrix maura males and females at the three study populations. Using the quadratic equation, we calculated the age at which growth slows downs (asymptotic point) as well as the maximum body size reached (snout-vent length, SVL). The asymptotic points for females from the Matarranya and Riofrío populations (in brackets) were estimated following the procedure detailed in the text.

R2 logistic model

R2 quadratic model

Quadratic equation

Age (years)

♀ Ebro Delta

0.8173

0.8165

SVL = 143.55 + 28.14 x – 0.74 x2

18.9

410.0

♀ Matarranya

0.8689

0.8738

SVL = 127.70 + 37.37 x – 0.95 x2

19.7

496.2

♂ Riofrío

0.8569

0.8527

SVL = 188.39 + 25.61 x – 0.11 x2

(20)

656.59

♀ Riofrío

0.8948

0.8923

SVL = 178.19 + 32.27 x – 0.86 x2

18.7

480.0

0.7782

0.7781

SVL = 177.55 + 33.44 x – 0.59 x

(20)

610.35

Group ♂ Ebro Delta

2

Max SVL (mm)

42

FILIPPAKOPOULOU ET AL.

At the Ebro Delta, females were larger than males of the same age (ANOVA, F1,91 = 10.9, P = 0.001). As stated, the asymptotic points of the same age differed by about one year, and at this age females had a much larger SVL than males (496 and 410 mm, respectively).

Predicted growth rates were 14.28 mm / year for males and 18.08 mm / year for females.

Consequently, the slopes of the regression lines differed significantly (SMA test, T = 7.5, P = 0.007; Fig. 2).

Ebro Delta females were smaller than those from Riofrío (ANOVA, F1,60 = 7.53, P = 0.007) and Matarranya (F1, 68 = 13.04, P = 0.0005), but females from Matarranya and Riofrío had similar body sizes (F1, 50 = 0.61, P = 0.4). we assumed that the asymptotic point of the females did not differ among the three populations (19.7 years), and at this age females from Riofrío and the Matarranya had a much larger SVL than those from the Ebro Delta (609, 650, and 496 mm, respectively; Fig. 3). The predicted growth rate for Riofrío females was 22.80 mm / year, that is 4.72 mm / year higher than for the Ebro Delta females. The slopes of the regression lines did

Figure 2: Relationship between age and body size (snout-vent length, SVL) for Natrix maura males (empty circles and dotted line) and females (closed circles and solid line) in the Ebro Delta.

Figure 3: Relationship between age and body size (snout-vent length, SVL) for Natrix maura females in the Ebro Delta (closed circle and dotted line), Matarranya River (triangles and dashed line) and Riofrío (empty circles and solid line).

not differ significantly in any of the three pairwise comparisons (Table 2, SMA test), perhaps because of the small sample sizes available for this test. However, we found significant differences in the elevation of the regression lines in Ebro Delta - Riofrío, and Ebro Delta Matarranya (Table 2, wald test), a finding consistent with the observed differences in annual growth rates.

Similarly, Riofrío males were larger than those from Ebro Delta (ANOVA, F1, 74 = 14.05, P = 0.0003). The asymptotic point did not differ between the two populations (see above), and at that this point, Riofrío males had a much larger SVL than those from the Ebro Delta (480 and 410 mm, respectively; Fig. 4). Predicted growth rate in Riofrío males was 17.48 mm / year, 3.20 mm / year higher than in the Ebro Delta males.

Although the slopes of the regression lines did not differ significantly (SMA test, T = 0.130, P = 0.71), their elevations did (wald test Stat = 124.9, P = 0.0001) (Fig. 4) in agreement with variation in annual growth rate.

GROWTH-RATE TRAJECTORIES OF SNAKES

43

Table 2: Interpopulation comparisons of slopes (SMA test) and asymptotes (wald test) calculated from the age versus body size quadratic equation in female Natrix maura in three populations within the Iberian Peninsula.

Compared groups Ebro Delta and Riofrío

Slope comparisons (SMA test)

Asymptote comparisons (wald Test)

T = 0.5, P = 0.4

Stat = 18.8, P = 0.003

Ebro Delta and Matarranya

T = 0.4, P = 0.5

Stat = 15.3, P = 0.02

Riofrío and Matarranya

T = 0.4, P = 0.5

Stat = 10.58, P = 0.44

Reproductive traits The hatchlings from the Ebro Delta were smaller (151.4 ± 2.2 mm, N = 28) than those from Riofrío (166.2 ± 4.4 mm, N = 17; Mann-whitney U test, z = 2.72, P = 0.007).

No data were available for body size of hatchlings from the Matarranya River.

DISCUSSION The use of growth marks of the ectopterygoid for age determination and their correlation with body size indicated sexual and interpopulation variation in growth trajectories in

Figure 4: Relationship between age and body size (snout-vent length, SVL) for Natrix maura males in the Ebro Delta (closed circles and dotted line) and Riofrío (empty circles and solid line).

N. maura. with respect to interpopulation variation, we acknowledged that snakes and food availability at each population were collected in different years, and the causal linkage among food availability and growth trajectories must be interpreted with caution.

The Mediterranean Basin is quite unpredictable year to year in climate and available food resources (BLONDEL et al., 2010), and annual variation in food resources could potentially modify snake’s growth trajectories. However, two of the snake populations, the Ebro Delta and Riofrío, use food resources strongly controlled by humans because rice fields always follow a regular and constant cycle at the Ebro Delta (GONzáLEz-SOLÍS & RUIz, 1996), and fish production in Riofrío is constant throughout the year (A. Domezain, personal communication). These facts provide compelling evidence that collecting snakes in different years presumably do not affect growth interpopulation variation in growth trajectories. A second shortcoming of our study is that snakes from populations where potential prey are more abundant, may consume significantly more prey than those from populations with fewer trophic resources. There are several evidences that the percentage of N. maura individuals with recent prey in stomach varied with prey availability (RUGIERO et al., 2000;

44

FILIPPAKOPOULOU ET AL.

SANTOS et al., 2000), and we also found interpopulation differences in the proportion snakes with recent prey (32.5% [N = 40] at Matarranya, SANTOS et al., 2006; 13.4% [N = 343] at the Ebro Delta, SANTOS et al., 2000; 29.9% [N = 97] at Riofrío, authors’ unpublished data). At the Ebro Delta for instance, the percentage of individuals with recent prey varied monthly in parallel to the increase of food availability after the rice field flooding, and raised in May to 21.8%, when availability was already high (SANTOS et al., 2000). Thereafter, the low availability of food at the Ebro Delta during part of the feeding period may obscure interpopulation differences in growth rates in N. maura;the differences exist, but may arise from different regimes of prey availability, from differences in the amount of prey availability, or from both factors. These shortcomings do not affect our finding of sexual variation at a single locality.

Sexual variation in growth trajectories The relationship between estimated age and SVL fits a quadratic regression model in the three populations. This model assumes that snakes experience a period of rapid growth during two thirds of their lifespans, slowing down in the last third of their lives.

In Matarranya and Riofrío however, the oldest females seemed to continue to grow and reach larger sizes, and this precluded calculation of asymptotic body size. This result was first reported by HAILEY & DAVIES (1987a) for female N. maura in the Jalón River (eastern Spain), and suggests that large, older females, do not stop growing. The maximum age recorded by the ectopterygoid growth marks from the Matarranya River

females, 22 years, evidences the long lifespan attained by some females. This is the oldest estimated age for N. maura, as the maximum age previously reported was 20 years for a female from the Jalón River (HAILEY & DAVIES, 1987b). The lack of an asymptotic female body size is not the consequence of unlimited growth of N. maura, but the result of some females reaching a very large size, a phenomenon that is likely in dimorphic snake species in which females grow larger than males (SHINE, 1980).

The comparison of the slopes of the regression lines during the active growing period shows that female growth rate was higher than that of the males. Moreover, sexual differences in growth trajectories indicate that the age at which growth slows down in males and females varies by one year, happening earlier in males. Age and body size of sexual maturity also vary between sexes: males mature earlier and at smaller body size (2-3 years old, SVL 220-250 mm) than females (4-6 years old, SVL 312-350 mm; DUGUY & SAINT GIRONS, 1966; HAILEY & DAVIES, 1987a,c; FERICHE & PLEGUEzUELOS, 1999; SANTOS & LLORENTE, 2001). Sexual dimorphism in these traits may be related to the fecundity selection theory applied to snakes, because females are larger than males in those species where larger body sizes have been selected to favour the increase in abdominal cavity for accommodating larger clutches or litters (SHINE, 1993).

Interpopulation variation in growth trajectories Interpopulation comparisons suggested that snakes in the Ebro Delta were younger and smaller than in the Matarranya River and Riofrío populations. Our results indicated slo-

GROWTH-RATE TRAJECTORIES OF SNAKES

wer growth trajectories in the Ebro Delta population, this fact contributing to the smaller body size attained by these snakes. The interpopulation comparisons also showed that the asymptotic SVL of the growth curves in males were smaller in the Ebro Delta than in Riofrío. Similar results were obtained when comparing the Ebro Delta versus the Matarranya and Riofrío females. Although the slopes of the regression lines did not show significant interpopulation differences, the asymptotic point and the estimated annual growth rates did. Moreover at the Ebro Delta, the high proportion of snakes with the tail broken suggests a high predation pressure (SANTOS et al., 2011). These environmental conditions suggest that food availability and predation pressure may be concurrently acting to produce smaller N. maura at the Ebro Delta than at the other two populations. what factors can account for these differences? Higher predation pressure at the Ebro Delta is caused by a high number of snake’s predators (SANTOS et al., 2011). Differences in annual grow rates might be caused for interpopulation differences in the length of the feeding season, inferred by combining environmental temperatures and food availability. The monthly percentage of snakes with recent prey at the Ebro Delta (the only locality where these data were available) confirmed that snakes scarcely fed when rice fields were dry, whereas did when fields flooded up (SANTOS et al., 2000). Although there are not monthly values of the percentage of snakes with recent prey for Matarranya River and Riofrío, the comparison of the average values for the three populations (13.4%, 32.5%, and 29.9%, for Ebro Delta, Matarranya and Riofrío, respectively) supports the reduced

45

feeding opportunities of N. maura at the Ebro Delta. According to life-history theory, energy-demanding activities (e.g. maintenance, growth and reproduction) depend on an organism’s feeding success (STEARNS, 1976).

Some snakes have flexible strategies for adjusting the relative amount of energy allocated to body growth and storage in response to food availability (FORSMAN & LINDELL, 1996). Our findings indicate that snakes at the Ebro Delta experience a shorter feeding season compared to the Matarranya River and Riofrío populations. The Ebro Delta is a wetland area with high productivity rates (FORéS & COMÍN, 1992); however, restrictions in prey availability in this habitat are related to the rice-field irrigation system, which begins in April and ends in early autumn after rice harvesting. The rice-field cycle limits prey availability for N. maura, as fields and canals dry up from October to April, and aquatic prey become unavailable.

Accordingly, snakes in the Ebro Delta have access to prey for 1-2 month less (on average) than snakes in the other two populations. On the contrary, we suggest that similarities in growth trajectories between the Matarranya and Riofrío snakes are primarily caused by a similar feeding season and presumably no limitation in food resources, as the Matarranya River has among the highest diversity and density of fish in Europe (DE SOSTOA, 2001) and Riofrío is a fish farm.

Interpopulation differences in the size of hatchlings we found that the size of N. maura hatchling at the Ebro Delta was smaller than at Riofrío. Variation in the length of the feeding season experienced by each population may

46

FILIPPAKOPOULOU ET AL.

affect food-intake rates, which in turn may influence variation in hatchling size. In support of this explanation, SEIGEL & FORD (2001) found that Thamnophis marcianus showed a marginal difference in neonate mass from females with access to higher prey availability.

Moreover, SPARKMAN et al.(2007) showed that larger or older females had larger offspring, a result that fit our Ebro Delta-Riofrío comparison. Reproduction is energetically demanding, and consequently we would expect a trade-off between growth and reproductive output, especially where food availability is limited. In snakes, prey availability can affect reproductive output by limiting the number of females reproducing per year (SHINE & MADSEN, 1997; PLEGUEzUELOS et al., 2007), litter or clutch size (LOURDAIS et al., 2002), or offspring or hatchling body size or mass (FORD & SEIGEL, 2011). Adult N. maura females reproduce every year throughout their range (SANTOS, 2004), and SANTOS et al. (2005) did not find any differences in clutch size (relative to female size) among the three populations studied here despite variation in the timing and duration of prey availability. Collectively, these findings suggest that clutch size (scaled for female size) is a fixed parameter within N. maura. Thus, our study found that N. maura’s reproductive plasticity is manifested through hatchling size, and varies according to female food intake rates, which in turn may be determined by the duration of the period of prey availability (GREGORY & LARSEN, 1993, 1996; SEIGEL & FORD, 2001). Interpopulation differences in clutch and/or offspring size is based on the idea that local selective pressures are driving reproductive traits to maximize fitness on a particular geographic area (FORD & SEIGEL, 2011). Most snakes are capital breeders and

tend to gather resources over a long period prior to expending them during the short reproduction period (BONNET et al., 1994; NAULLEAU & BONNET, 1996). Our study illustrates that intraspecific comparison among populations that experience different food regimes can exemplify the evolutionary strategies displayed by ectothermic organisms in energyallocation decisions.

Acknowledgement we thank Genaro de Gamboa for his valuable mathematical support, Hernando Diaz and Ana María Diaz for their statistical comments, and to the blind testers Núria Garriga, Borja Ruiz and Guillem Pascual. we also thank Alberto Domezaín and the staff of the Riofrío fish farm for facilitating fieldwork. Research was carried out under hunting permits by the Direcció General del Medi Natural, Catalan Government (no. 6539, 26.10.1990 and no.

537, 29.01.1991) in the Ebro Delta, and by the Instituto para la Conservación de la Naturaleza (ICONA, Spanish Government) in the Matarranya River. Xavier Santos was supported by a post-doctoral grant (SFRH⁄ BPD⁄73176/2010) from Fundação para a Ciência e a Tecnologia (FCT, Portugal).

REFERENCES ANDREwS, R.M. (1982). Patterns of growth in reptiles, In: C. Gans & F.H. Pough (eds.).

Biology of the Reptilia, vol. 13. Academic Press, New York, USA, pp. 273-320.

AUBRET, F. & SHINE, R. (2007). Rapid preyinduced shift in body size in an isolated snake population (Notechis scutatus, Elapidae). Austral Ecology 32: 889-899.

GROWTH-RATE TRAJECTORIES OF SNAKES

AUBRET, F.; SHINE, R. & BONNET, X. (2004).

Adaptive developmental plasticity in snakes. Nature 431: 261–262.

BLONDEL, J.; ARONSON, J.; BODIOU, J.-Y. & BOEUF, G. (2010). The Mediterranean Region: Biological Diversity in Space and Time, 2nd ed.

Oxford University Press, Oxford, UK. BOBACK, S. (2003). Body size evolution in snakes: evidence from island populations.

Copeia 2003: 81-94.

BOHLIN, T.; HAMRIN, S.; HGGBERGET, T.G.; RASMUSSEN, G. & SALTVEIT, S.V. (1989).

Electrofishing: theory and practice with special emphasis on salmonids.

Hydrobiologia 173: 9-43.

BONNET, X.; NAULLEAU, G. & MAUGET, R. (1994). The influence of body condition on 17-b estradiol levels in relation to vitellogenesis in female Vipera aspis Reptilia, Viperidae. General and Comparative Endocrinology 93: 424-437.

CASTANET, J.; MEUNIER, F. & DE RICQLèS, A. (1977). L’enregistrement de la croissance cyclique par le tissu osseux chez les vertébrés poikilotermes: données comparatives et essai de synthèse. Bulletin Biologique de la France et de la Belgique 111: 183-202.

CONGDON, J.D.; DUNHAM, A.E. & TINKEL, D.w. (1982). Energy budgets and life history of reptiles, In: C. Gans (ed.) Biology of Reptilia, vol. 13. Academic Press, New York, USA, pp. 233-271.

CONGDON, J.D.; DUNHAM, A.E.; HOPKINS, w.A.; ROwE, C.L. & HINTON, T.C. (2001). Resource allocation-based life histories: a conceptual basis for studies of ecological toxicology. Environmental Toxicology and Chemistry 20: 1698-1703.

DE SOSTOA, A. (2001). Las comunidades de peces de las cuencas mediterráneas: caracte-

47

rización y problemática, In I. Doadrio (ed.)

Atlas y Libro Rojo de los Peces Continentales de España. Dirección General de Conservación de la Naturaleza, Madrid, Spain, pp. 51-56.

DUGUY, R. & SAINT-GIRONS, H. (1966).

Cycle annuel d’activité et reproduction de la couleuvre viperine Natrix maura (L.), d’après les notes manuscrites de Rollinat et des observations personnelles. La Terre et la Vie 4: 423-457.

DURANT, S.E.; HOPKINS, w.A. & TALENT, L.G. (2007). Energy acquisition and allocation in an ectothermic predator exposed to a common environmental stressor.

Comparative Biochemistry and Physiology C 145: 442-448.

FALSTER, D.S., wARTON, D.I. & wRIGHT, I.J. (2006). SMATR: Standardised major axis tests and routines, ver 2.0. Available at http://www.bio.mq.edu.au/ecology/SMATR/.

Retrieved on 17 January 2014 FASOLA, M. (1986). Resource use of foraging herons in agricultural and nonagricultural habitats in Italy. Colonial Waterbirds 9: 139–148.

FERICHE, M. & PLEGUEzUELOS, J.M. (1999).

Características de la reproducción de la culebra viperina, Natrix maura (Linnaeus, 1758), en la Depresión de Granada (sureste ibérico). Revista Española de Herpetología 13: 37-48.

FORD, N.B. & SEIGEL, R.A. (2011). Offspring size variation in snakes, In R.D. Aldridge & D.M. Sever (eds.) Reproductive Biology and Phylogeny of Snakes. Series: Reproductive Biology and Phylogeny, vol. 9. Science Publisher, Enfield, New Hampshire, USA, pp. 573-586.

FORéS, E. & COMÍN, F.A. (1992). Ricefields, a limnological perspective. Limnetica 8: 101-109.

48

FILIPPAKOPOULOU ET AL.

FORSMAN, A. & LINDELL, L.E. (1991). Trade-off between growth and energy storage in male Vipera berus (L.) under different prey densities. Functional Ecology 5: 717-723.

FORSMAN, A. & LINDELL, L.E. (1996).

Resource dependent growth and body condition dynamics in juvenile snakes: an experiment. Oecologia 108: 669–675.

GONzáLEz-SOLÍS, J. & RUIz, X. (1996).

Succession and secondary production of gastropods in the Ebro Delta ricefields.

Hydrobiologia 337: 85-92.

GONzáLEz-SOLÍS, J.; BERNARDÍ, X. & RUIz, X. (1996). Seasonal variation of waterbird prey in the Ebro Delta rice fields. Colonial Waterbirds 19 (Special Publication 1): 135-142.

GREGORY, P.T. & LARSEN, K.w. (1993).

Geographic variation in reproductive characteristics among Canadian populations of the common garter snake (Thamnophis sirtalis). Copeia 1993: 946-958.

GREGORY, P.T. & LARSEN, K.w. (1996). Are there any meaningful correlates of geographic life-history variation in the garter snake Thamnophis sirtalis? Copeia 1996: 183-189.

HAILEY, A. & DAVIES, P.M.C. (1987a).

Growth, movement and population dynamics of Natrix maura in a drying river.

Herpetological Journal 1: 185-194.

HAILEY, A. & DAVIES, P.M.C. (1987b).

Digestion, specific dynamic action, and ecological energetics of Natrix maura.

Herpetological Journal 1: 159-166.

HAILEY, A. & DAVIES, P.M.C. (1987c).

Maturity, mating and age-specific reproductive effort of the snake Natrix maura.

Journal of Zoology 211: 573-587.

HAILEY, A.; DAVIES, P.M.C. & PULFORD, E. (1982). Lifestyle and thermal ecology of

natricine snakes. British Journal of Herpetology 6: 261-268.

JAéN, M.J. & PéREz-MELLADO, V. (1989).

Temperaturas corporales y ritmos de actividad en una población de Natrix maura (L.) del Sistema Central. Doñana Acta Vertebrata 16: 203-217.

LESSELLS, C. (1991). The evolution of life histories, In: J.R. Krebs & N.B. Davies (eds.) Behavioural Ecology. Blackwell, Oxford, UK, pp. 32-68.

LOURDAIS, O.; BONNET, X.; SHINE, R.; DENARDO, D.; NAULLEAU, G. & GUILLON, M. (2002). Capital-breeding and reproductive effort in a variable environment: a longitudinal study of a viviparous snake. Journal of Animal Ecology 71: 470-479.

MADSEN, T. & SHINE, R. (1993). Phenotypic plasticity in body sizes and sexual dimorphism in European grass snakes. Evolution 47: 321-325.

MALKMUS, R. (2008). winteraktive Schlangen in Portugal (Erganzende Bemerkungen).

Zeitschrift fur Feldherpetologie 15: 97-98.

MATHwORKS (1996). MATLAB. The Language of Technical computing. Version 7.

The Mathworks, Inc. Available at http:// www.mathworks.com. Retrieved on 17 January 2014.

MCNAB, B.K. (2002). The Physiological Ecology of Vertebrates: a View from Energetics. Cornell University Press, Ithaca, New York, USA. NAULLEAU, G. & BONNET, X. (1996). Body condition threshold for breeding in a viviparous snake. Oecologia 107: 301-306.

O’STEEN, S. (1998). Embryonic temperature influences juvenile temperature choice and growth rate in snapping turtles Chelydra serpentina.

Journal of Experimental Biology 201: 439-449.

GROWTH-RATE TRAJECTORIES OF SNAKES

PEABODY, F.E. (1961). Annual growth zones in vertebrates (living and fossil). Journal of Morphology 108: 11-62.

PLEGUEzUELOS, J.M.; SANTOS, X.; BRITO, J.C.; PARELLADA, X.; LLORENTE, G.A. & FAHD, S. (2007). Reproductive ecology of Vipera latastei in the Iberian Peninsula: implications for the conservation of a Mediterranean viper. Zoology 110: 9-19.

REzNICK, D.A.; BRYGA, H. & ENDLER, J.A. (1990). Experimentally induced life-history evolution in a natural population.

Nature 346: 357-359.

RUGIERO, L.; CAPULA, M.; PERSICHETTI, D.; LUISELLI, L. & ANGELICI, F.M. (2000).

Life-history and diet of two populations of Natrix maura (Reptilia, Colubridae) from contrasted habitats in Sardinia.

Miscelanea Zoologica 23: 41-51.

SANTOS, X. (2004). Culebra viperina. Natrix maura, In A. Salvador & A. Marco (eds.)

Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid, Spain. Available athttp://www.vertebradosibericos.org/.

Retrieved on 11/22/2013.

SANTOS, X. & LLORENTE G.A. (1998). Sexual and size-related differences in the diet of the snake Natrix maura from the Ebro Delta, Spain. Herpetological Journal 8: 161-165.

SANTOS, X. & LLORENTE, G.A. (2001).

Seasonal variation in reproductive traits of the oviparous water snake, Natrix maura, in the Ebro Delta of Northeastern Spain.

Journal of Herpetology 35: 653-660.

SANTOS, X. & LLORENTE, G.A. (2004). Lipid dynamics in the viperine snake, Natrix maura, from the Ebro Delta (NE Spain).

Oikos 105: 132-140.

SANTOS, X., GONzáLEz-SOLÍS, J. & LLORENTE,

49

G.A. (2000). Variation in the diet of the viperine snake Natrix maura in relation to prey availability. Ecography 23: 185-192.

SANTOS, X.; LLORENTE, G.A.; FERICHE, M.; PLEGUEzUELOS, J.M.; CASALS, F. & DE SOSTOA, A. (2005). Food availability induces geographic variation in reproductive timing of an aquatic oviparous snake (Natrix maura). Amphibia-Reptilia 26: 183-191.

SANTOS, X.; VILARDEBó, E.; CASALS, F.; LLORENTE, G.A.; VINYOLES, D. & DE SOSTOA, A. (2006). wide food availability favours intraspecific trophic segregation in predators: the case of a water snake in a Mediterranean river. Animal Biology 56: 299-309.

SANTOS, X.; ARENAS, C.; LLORENTE, G.A. & RUIz, X. (2007). Exploring the origin of egg protein in an oviparous water snake (Natrix maura). Comparative Biochemistry and Physiology A 147: 165-172.

SANTOS, X.; FERICHE, M.; LEóN, R.; FILIPPAKOPOULOU, A.; VIDAL-GARCÍA, M.; LLORENTE, G.A. & PLEGUEzUELOS, J.M. (2011). Tail breakage frequency as an indicator of predator risk for the aquatic snake Natrix maura. Amphibia-Reptilia 32: 375-383.

SEIGEL, R.A. & FORD, N.B. (2001).

Phenotypic plasticity in reproductive traits: geographical variation in plasticity in a viviparous snake. Functional Ecology 15: 36-42.

SHINE, R. (1980). Cost of reproduction in reptiles. Oecologia 46: 92-100.

SHINE, R. (1993). Australian Snakes. A Natural History. Reed Books, Chatswood, New South wales, Australia.

SHINE, R. (2003). Reproductive strategies in snakes. Proceedings of the Royal Society B: Biological Sciences 270: 995-1004.

50

FILIPPAKOPOULOU ET AL.

SHINE, R. & MADSEN, T. (1997). Prey abundance and predator reproduction: rats and pythons on a tropical Australian floodplain. Ecology 78: 1078-1086.

SHINE, R.; REED, R.N.; SHETTY, S. & COGGER, H.G. (2002). Relationship between sexual dimorphism and niche partitioning within a clade of sea-snakes (Laticaudinae). Oecologia 133: 45-53.

SPARKMAN, A.M.; ARNOLD, S.J. & BRONIKOwSKI, A.M. (2007). An empirical test of evolutionary theories for reproductive senescence and reproductive effort in the garter snake Thamnophis elegans.

Proceedings of the Royal Society B: Biological Sciences 274: 943-950.

STATSOFT (2007). STATISTICA (data analysis software system), version 8.0. StatSoft Inc. Available at http://www.statsoft.com.

Retrieved on 17 January 2014.

STEARNS, S.C. (1976). Life-history tactics: a review of the ideas. Quarterly Review of Biology 51: 3-47.

STEARNS, S.C. (1989). Trade off in life history evolution. Functional Ecology 3: 259-268.

STEARNS, S.C. (1992). The Evolution of Life Histories. Oxford University Press, New York, USA. wAYE, H.L. & GREGORY, P.T. (1998).

Determining the age of garter snakes (Thamnophis spp.) by means of skeletochronology. Canadian Journal of Zoology 76: 288-294. wHITE, G.C.; BURNHAM, K.P.; OTIS, D.L. & ANDERSON, D.R. (1978). Userâ&#x20AC;&#x2122;s Manual for Program CAPTURE. Utah State University Press, Logan, Utah, USA. zIPPIN, C. (1958). The removal method of population estimation. Journal of Wildlife Management 22: 82-90.

Basic and Applied Herpetology 28 (2014): 51-63

Diversidad de una comunidad de Anolis (Iguania: Dactyloidae) en la selva pluvial central, departamento del Chocó, Colombia Jhon Tailor Rengifo M.1,*, Fernando C. Herrera2, Francisco J. Purroy3 Universidad Tecnológica del Chocó, Facultad de Ciencias Básicas, Chocó, Colombia.

Universidad del Valle, Laboratorio de Herpetología, Cali, Valle del Cauca, Colombia.

3 Universidad de León, Departamento de Biodiversidad y Gestión Ambiental, León, España.

1 2

* Correspondence: Cra 22 Nº18b-10 B/Nicolas Medrano, Quibdó, Chocó, Colombia. Phone: +574 6726565, Fax: +574 6710172, E-mail: jhontailorrengifo@gmail.com

Received: 21 June 2012; received in revised form: 23 April 2014; accepted: 2 May 2014.

Se ha realizado la caracterización ecológica de una comunidad de Anolis en cinco localidades del departamento del Chocó, enclavados en una zona de bosque pluvial tropical. Los muestreos se realizaron siguiendo el método de Encuentros Visuales (VES) en tres coberturas vegetales. Se registraron 303 individuos empleando un esfuerzo de muestreo de 960 horas / persona, obteniendo un éxito de captura de 0,31 individuos / hora / persona. El género Anolis está representado por 10 especies, siendo las más abundantes Anolis maculiventris (54,1% del total de observaciones correspondientes al género), A. granuliceps (20,1%) y A. chloris (11,2%).

El resto de las especies presentaron abundancias relativamente bajas. Los estimadores de diversidad indicaron que se muestreó un porcentaje significativo de dicha comunidad. Los resultados revelaron diferencias significativas en la composición y estructura de la comunidad de Anolis en las diferentes coberturas vegetales, así como el intercambio y exclusividad de especies entre diferentes estratos.

Key words: Abundacia; Anolis; Chocó; Comunidad; Diversidad.

Diversity of a community of Anolis (Iguania: Dactyloidae) in the Central rainforest, department of Choco, Colombia. The ecological characterization of an Anolis community was done in five localities of the Chocó District, all of them located in a tropical rainforest region. Visual Encounter Surveys (VES) were performed in three vegetation strata. In total, 303 individuals were recorded using a sampling effort of 960 hours / person, with a capture rate of 0.31 individuals / hour / person. The genus Anolis in this region is represented by 10 species, being A. maculiventris (54.1%), A. granuliceps (20.1%) and A. chloris (11.2%) the more common ones. All other species were present in low abundances. Estimates of diversity indicated that a significant percentage of the community was sampled. The results also revealed significant differences in the community structure of Anolis along the different rainforest altitudinal layers, as well as processes of exchange and exclusivity in particular cases.

Key words: Abundance; Anolis; Chocó; Community; Diversity.

Las especies del género Anolis (Lacertilia: Dactyloidae) se distribuyen desde Estados Unidos hasta Brasil, desde el nivel del mar hasta los 2000 m de altitud (wILLIAMS, 1976; DUELLMAN, 1978; GUYER & SAVAGE, 1986; FROST & ETHERIDGE 1989; SAVAGE & GUYER, 1989). Este grupo incluye las especies DOI: http://dx.doi.org/10.11160/bah.12004/

más pequeñas y numerosas del infraorden Iguania, ocupando una amplia variedad de microhábitats (arbóreos, terrestres, y semiacuáticos) en todo el Neotrópico. Los anoles son un ejemplo clásico de radiación adaptativa (JACKMAN et al., 1997). Este grupo está presente en una gran variedad de hábitats, e

52

RENGIFO M. ET AL.

incluye alrededor de 400 especies (wILLIAMS, 1983; LOSOS et al., 1998), de las cuales 140 se encuentran en el Caribe (wILLIAMS, 1992; POwELL et al., 1996). De ellas 111 está distribuidas en las Antillas Mayores (Cuba, Hispaniola, Jamaica, y Puerto Rico), presentando un alto grado de endemismo y ocupando una gran diversidad de nichos ecológicos (11 especies simpátricas) (wILLIAMS, 1983; LOSOS, 1994). En regiones continentales este grupo exhibe una amplia diferenciación ecológica (IRSCHICK et al., 1997).

La evaluación de la biodiversidad en áreas tropicales con base en la elaboración de inventarios completos es especialmente difícil, siendo únicamente posible en áreas relativamente pequeñas, donde es posible realizar inventarios exhaustivos de la biota (DI CASTRI & YOUNES, 1990; HALFFTER et al., 2001). Una alternativa para ultrapasar estas limitaciones es la utilización de indicadores de biodiversidad. Este concepto se basa en la premisa de que en áreas grandes el número de especies de un grupo (el cual ha sido bien estudiado) se correlaciona positivamente con la riqueza de especies de otros grupos de los cuales se posee menos información (BECCALONI & GASTON, 1995; PRENDERGAST & EVERSHAM, 1997). El objetivo de este estudio es analizar la composición y estructura de la comunidad de Anolis en la zona central del departamento del Chocó, teniendo en cuenta la cobertura vegetal y los procesos de gestión aplicados a los bosques de la selva pluvial.

MATERIALES Y METODOS Área de estudio y muestreo Las zonas estudiadas se localizan en las llanuras aluviales, colinas bajas y piedemonte cer-

canos al valle del río Atrato (municipio de Quibdó, departamento del Chocó), donde se concentra la mayor pluviosidad del andén del Pacífico (Chocó Biogeográfico) y donde las formaciones selváticas se encuentran entre las más ricas del mundo (CUATRECASAS, 1958; FORERO & GENTRY, 1989). La zona de muestreo se localiza en las coordenadas geográficas 5º00’-6º45’N y 77º15’-76º30’O. El régimen de precipitación es de tipo bimodal-tetraestacional con un período de mayor concentración de lluvias entre abril y octubre y una época de menor concentración desde noviembre hasta marzo (POVEDA et al., 2004). La precipitación anual es de 8558 mm con un promedio mensual de 395,5 mm (RANGEL-CH & LOwY 1993; ESLAVA 1994). Las comunidades vegetales de esta zona aparecen detalladas en CUATRECASAS (1958) y SUáREz NAVARRO (1984). Se establecieron cinco localidades de muestreo (Tabla 1), y en cada una de ellas se estudiaron zonas con tres tipos de cobertura vegetal, diferentes grados de intervención antrópica y tipos de gestión. En total se realizaron 15 muestreos (tres por localidad) durante 15 meses, comprendidos entre 2008 y 2010.

Cada muestreo tuvo una duración de ocho días, con un esfuerzo de muestreo de ocho horas / persona, repartidas entre el día y la noche, donde se hicieron recorridos a lo largo de caminos abiertos y zonas interiores de cada uno de los sitios de muestreos. Las coberturas vegetales estudiadas fueron: 1) Bosque secundario con 30 a 60 años de regeneración (área I): conformada por grandes extensiones forestales que no han sido transformadas o alteradas por la actividad humana en los últimos 30 años y que conservan características de la selva pluvial original.

Generalmente estas áreas están bastante aleja-

53

DIVERSIDAD DE ANOLIS DEL CHOCÓ, COLOMBIA

Tabla 1: Características biofísicas de las localidades objeto de estudio. Para cada localidad se muestran las coordenadas geográficas, altitud, temperatura (Temp), humedad relativa y precipitación (Precip) media anual.

Localidades muestreadas

Coordenadas

Altitud (m) Temp (ºC) Humedad (%) Precip (mm)

Unión Panamericana “Salero”

5°22’N, 76°36’w

100

28

90

7600

Certegüi “Recta Larga”

5°41’N, 76°39’w

43

28

95

7000 10000

Lloró “CMUTCH”

5°30’N, 76°33’w

48

28

85

Atrato “Samurindó”

5°35’N, 76°39’w

30

28

91,8

Quibdó “Urbana y Suburbana”

5°43’N, 76°37’w

47

26,5

87

das de asentamientos humanos. Poseen un alto porcentaje de cobertura, árboles de gran porte con abundantes plantas epífitas, y un gran número de lianas, plantas de guía (bejucos) y bromelias. Se caracteriza por intensificación lumínica baja y alto grado de humedad.

2) Bosques secundarios tempranos (área II): Bosques que después de haber sido intervenidos por el hombre han recuperado su estructura natural a través de una sucesión de especies colonizadoras, en estado transicional temprano, con menos 15 años de recuperación. área muy homogénea, donde es común la vegetación de estratos arbustivo y subarbóreo, predominando especies de la familia de las melastomatáceas, y unos pocos árboles que superan los 20 m de altura. Presenta abundancia de hojarasca y bromelias, y poca presencia de luz solar y bejucos.

3) área de gestión (área III): áreas destinadas a establecimiento de cultivos, extracción de material vegetal para diferentes labores, ubicación de pastos para ganadería y áreas de extracción minera artesanal o mecanizada, generando en el último caso la pérdida de grandes extensiones de cobertura vegetal. En esta área predomina la vegetación arbustiva, helechos y árboles frutales.

8000 12000

Los muestreos para determinar la riqueza de especies y las abundancias relativas de las especies se realizaron mediante el método de Encuentros Visuales (Visual Encounter Survey, VES) (CRUMP & SCOTT, 1994), usando la metodología detallada en RENGIFO (2002) y PAéz et al. (2002). Esta metodología consiste en la inspección pormenorizada de toda el área de muestreo, incluyendo las diferentes coberturas vegetales (árboles, arbustos y vegetación herbácea), lugares abiertos (caminos, linderos, senderos y otros) y zonas de difícil acceso (bejuco, enredaderas y ramas altas de los árboles). Los individuos localizados eran capturados, y la información relativa al lugar de captura registrada (altura y sustrato de la percha, posición del animal, diámetro de la percha y datos ambientales del hábitat). Los animales se mantuvieron en bolsas de tela, fueron procesados (fotografiados, medidos y pesados) en el lugar de trabajo y posteriormente liberados. La determinación taxonómica se realizó in situ, con la ayuda de guías de campo y claves taxonómicas (PETERS & DONOSO-BARROS, 1970; RENJIFO & LUNDBERG 1999; PáEz et al., 2002). Las identificaciones dudosas fueron confirmadas posteriormente en el laboratorio de zoología

54

RENGIFO M. ET AL.

de la Universidad Tecnológica del Chocó y Universidad del Valle usando el material fotográfico obtenido durante el muestreo.

Análisis de datos La diversidad alfa se estimó mediante índices directos, e incluyó la riqueza de especies (número de especies por área), el índice de diversidad de Margalef (número de especies en relación al número total de individuos), la abundancia (número de individuos por especie) y la abundancia relativa (Pi, porcentaje de individuos por especie en relación al número total de individuos capturados).

Igualmente se calculó el éxito de captura, definida como el número de individuos capturados en una hora por persona.

Adicionalmente, en cada zona se estimaron los siguientes índices: índice de dominancia de Simpson (λ), índice de diversidad de Shannon-weaver (H’, BAEV & PENEV, 1995), e índice de equitatividad de Pielou (J’). Estos dos últimos asumen que todas las especies están representadas en las muestras y que todos los individuos fueron muestreados al azar (áLVAREz et al., 2004).

La diversidad beta, definida como el grado de recambio en la composición de especies entre áreas de muestreo, se analizó mediante el índice de Sorensen, usando el coeficiente de similitud cualitativo (S), que trabaja con las riquezas, y cuantitativo (Iscuant) que usa las abundancias (MAGURRAN, 1988).

Todos estos índices fueron calculados en el programa PAST, versión 1.15 (HAMMER et al., 2001).

Se utilizó el índice de complementariedad que mide el grado de recambio en la composición de especies entre diferentes hábitats, y

que relaciona el número de especies en el área A, con el número de especies en el área B y el número de especies comunes entre ambas áreas (COLwELL & CODDINGTON, 1994; MAGURRAN, 2004). Los valores obtenidos en el análisis de complementariedad varían desde cero, cuando ambos sitios tienen una composición de especies idéntica, hasta uno, cuando las especies de ambos sitios son com& pletamente distintas (COLwELL CODDINGTON, 1994).

Las diferencias en la composición y estructura de las áreas de muestreo fueron analizadas para cada tipo de cobertura vegetal usando el test de Kruskal-wallis. Estos cálculos se realizaron con el programa SPSS (VISAUTA-VINACUA & MARTORI I CAñAS, 1998).

Asimismo, se estimó la representatividad de los muestreos comparando el número acumulado de especies (captura) y el esfuerzo de muestreo mediante los estimadores Chao1 y ACE empleando el programa estadístico ESTIMATES versión 6.0 (Robert K. Colwell, University of Connecticut, Storrs, CT, USA).

Finalmente se realizaron curvas de rangoabundancia, que representan la abundancia, diversidad y equitatividad de las especies, teniendo en cuenta su identidad y secuencia (FEINSINGER, 2001) para comparar los ambientes estudiados. Para ello, se calculó el log(10) de la abundancia relativa sobre la abundancia total, y estos datos se ordenaron desde la especie más abundante a la más escasa (FEINSINGER, 2001).

RESULTADOS Se registraron 303 individuos empleando un esfuerzo de muestreo de 960 horas / persona (320 horas / persona en cada área) obte-

DIVERSIDAD DE ANOLIS DEL CHOCÓ, COLOMBIA

55

Figura 1: Curva de acumulación de especies de una comunidad de Anolis en la zona centro del departamento del Chocó, Colombia. área I: bosque secundario con 30 a 60 años, área II: bosque secundario en regeneración natural y área III: área de gestión.

Se muestra el índice de riqueza Sobs (Mau Tau) (i.e. número de especies esperadas en el conjunto de muestras, teniendo en cuenta los datos empíricos) con su intervalo de confianza al 95% (COLwELL et al. 2004) y los estimadores de riqueza Chao1 (CHAO, 1987) y ACE (Abundance-base Coverage Estimator, COLwELL & CODDINGTON, 1994).

niendo un éxito de captura de 0,31 individuos / hora / persona (Fig. 1). El género Anolis está representado por 10 especies (Tabla 2), de las cuales las más abundantes fueron A. maculiventris con el 54,1% (N = 164) de las observaciones totales, A. granuliceps con el 20,1% (N = 61) y A. chloris con el 11,2% (N = 34). Las restantes especies presentaron abundancias relativamente bajas (Tabla 2, Fig. 2). Las 10 especies de Anolis

encontradas en la zona estudiada comprenden el 37.0% de las especies del género registradas para la región del Chocó según RENGIFO (2011), el 32,2 y 14,0% para la región biogeográfica del Chocó y Colombia respectivamente, según CASTAñO et al.

(2004) así como el 2,5% de la riqueza mundial de Anolis (wILLIAMS, 1983; LOSOS et al., 1998). Los estimadores de riqueza Chao1 y ACE indicaron que los muestreos fueron

56

RENGIFO M. ET AL.

Tabla 2: Abundancia total de las especies del género Anolis en cada una de las tres áreas de estudio con diferentes grados de intervención, así como abundancia total y relativa (%) en el conjunto de áreas muestreadas.

Especie A. maculiventris

Abundancia total área II área III

%

Código

área I

Total

A

21

36

107

164

54,1

A. granuliceps

B

2

28

31

61

20,1

A. malkini

C

1

1

2

4

1,3

A. chloris

D

1

3

30

34

11,2

A. latifrons

E

1

3

0

4

1,3

A. lyra

F

3

0

2

5

1,7

A. biporcatus

G

1

0

1

2

0,7

A. anchicayae

H

13

1

0

14

4,6

A. chocorum

I

6

5

0

11

3,6

A. notopholis

J

4

0

0

4

1,3

representativos en los tres tipos de coberturas vegetales. En el área I (bosque secundario con 30 a 60 años de regeneración), los estimadores predijeron la aparición de tres a cuatro nuevas especies (Chao1 = 13 (76%) y ACE = 14 (71%)). En el área II (bosque en regeneración actual), los estimadores predicen la aparición de una especie (Chao1 = 8 (87,5%) y ACE = 8 (87,5%)). Finalmente, los estimadores de riqueza en el área de gestión (área III) no predicen la aparición de nuevas especies.

Variable

En cuanto a la composición de las especies por áreas de muestreo, el área con mayor riqueza de especies fue el área I con 10 especies, incluyendo una de ellas exclusiva (A. notopholis), seguida del área II con siete especies, ninguna exclusiva, y el área III con seis especies (Tabla 2).

En cuanto a la diversidad de la comunidad de Anolis, la zona de bosque secundario fue la que presentó mayor valor en el índice de equidad de Shannon-weaver (H’ = 1,73; Tabla 3). Además, presenta un valor de índi-

área I

área II

área III

Esfuerzo de muestreo (horas / persona)

320

320

320

éxito de captura

0,16

0,24

0,54

53

77

173

Número total de individuos (abundancia) Índice de Shannon (H’)

1739

1267

1042

Índice de Pielou (J’)

0,75

0,65

0,58

Índice de Simpson (l)

0,76

0,64

0,97

Índice de Margalef (Mg)

2267

1381

555

Tabla 3: Resultados generales de los muestreos realizados sobre la comunidad de Anolis en cada una de las áreas analizadas con diferentes grados de intervención para el conjunto del área de estudio.

DIVERSIDAD DE ANOLIS DEL CHOCÓ, COLOMBIA

57

Figura 2: Abundancia de las diferentes especies de Anolis observadas en las diferentes áreas de muestreo estudiadas.

ce de dominancia de Simpson de 0,75, indicando que existen especies con una abundancia significativa, concretamente A. maculiventris (N = 21) y A. anchicayae (N = 13) con el 61% de los individuos registrados en esta área (Tabla 3, Fig. 3).

La curva de rango-abundancia muestra una distribución no uniforme de las especies en cada una de las coberturas vegetales estudiadas. Al comparar estas áreas se encontraron diferencias significativas (Kruskal-wallis, H = 79,82, gl = 2, P < 0,0001) entre las diferentes coberturas vegetales en términos de composición y estructura, siendo A. maculiventris, A. anchicayae y A. chocorum más comunes en el área de bosque (área I), y A. maculiventris y A. granuliceps en el área de bosque secundario actual. Finalmente, estas dos especies fueron junto a A. chloris las más representativas en las áreas de gestión (Fig. 3).

El análisis de similitud y complementariedad mostró la existencia de dos grupos de afinidad teniendo en cuenta el número de especies

compartidas. El primer grupo estaba conformado por las áreas I y II con un 70% de similitud entre las áreas, presentando siete especies en común. El área III es la más diferenciada, mostrando una similitud del 55% con las áreas I y II. En términos de abundancia de especies, se encontró que las áreas II y III presentaron la mayor similitud (Iscuant = 0,54), seguido de las áreas I y II (Iscuant = 0,49). Las áreas menos parecidas, en términos de abundancia de especies, fueron las áreas I y III con Iscuant = 0,24. El análisis de complementariedad de estas coberturas indicó que el área de bosque secundario actual y el área de gestión presentaron el mayor índice de recambio (0,55), mientras que las áreas con una composición de especies más similar fueron el bosque (área I) y el área de gestión (área III), con una complementariedad de 0,40.

DISCUSIóN Las curvas de acumulación de especies con sus respectivos estimadores (Chao1 e

58

RENGIFO M. ET AL.

ACE) e intervalos de confianza al 95% predicen la aparición de pocas nuevas especies en los microhábitats presentes en las tres áreas muestreadas, presentado una estabilización en el área de gestión (área III) y una alta representatividad en el bosque secundario actual (área II). Estos resultados sugieren que los muestreos realizados fueron suficientes para registrar la totalidad o un porcentaje significativo de la comunidad de Anolis en dicha área. Asimismo, el comportamiento de las curvas de acumulación de especies sugiere que el esfuerzo de muestreo aplicado es suficiente para caracterizar la comunidad de Anolis en los bosques tropicales de la zona centro del departamento del Chocó. Estos resultados contradicen las conclusiones de RENGIFO et al. (2002), MURILLO (2004) y GARCÍA & MOSQUERA (2005), que sostienen que únicamente los estudios prolongados permiten caracterizar con éxito la diversidad.

La elevada abundancia de A. maculiventris y A. granuliceps se debe a la gran variedad de hábitats presentes en la zona de estudio.

Asimismo, la preferencia de estas dos especies por microhábitats en las partes bajas del sustrato altitudinal hace que sean observadas y registradas más fácilmente. Por otro lado, estas dos especies presentaron una preferencia relativa por las áreas de gestión (área III), sugiriendo que se trata de especies muy plásticas en términos de uso del hábitat, ya que se pueden registrar desde bosques bien conservados hasta áreas altamente perturbadas, siendo muy tolerantes a las alteraciones antrópicas producidas en los bosques tropicales (RÍOS et al., 2011). Otros trabajos (RENGIFO, 2002; RENTERÍA, 2006; RÍOS & HURTADO, 2007) sugieren que A. maculiventris es la especie con mayor frecuencia de ocurrencia

en zonas de bosque pluvial tropical, principalmente en estratos bajos, ayudado por su coloración poco conspicua o críptica.

En la comunidad del género Anolis registrada en el bosque pluvial tropical de la zona centro del departamento del Chocó se reportan cuatro especies (A. chloris, A. chocorum, A. granuliceps y A. peraccae) cuya distribución, según CASTAñO et al. (2004), está exclusivamente confinada a esta región. La riqueza del género Anolis en esta zona es probablemente el resultado de la confluencia de dos grupos diferentes en la matriz vegetal de la selva del Chocó biogeográfico (CASTAñO et al., 2004): la sección alfa (sensu wILLIAMS, 1976), cuyo centro de dispersión se consideró en Sudamérica, y la sección beta, con origen en el arco de las Antillas y Centroamérica. Otro aspecto que influye en la riqueza de este género es su tamaño corporal moderado, soliendo habitar zonas de suelo, ramas, arbustos y troncos, con una excelente oferta de alimento y variedad de microhábitats, si bien prefieren zonas sombreadas y márgenes de bosques (S.C. Ayala & F. Castro-H., datos no publicados).

La heterogeneidad de la composición vegetal de esta región juega, por lo tanto, un papel importante al proporcionar una gran variedad de microhábitats para la comunidad de Anolis, catalogados como los reptiles más diversos y adaptables que constituyen la fauna de vertebrados terrestres de los bosques tropicales (PLEGUEzUELOS & FERICHE, 2004), siendo la cobertura vegetal constituida por el bosque la que ofreció las mejores condiciones para albergar la mayor riqueza de especies. La comparación de la composición y estructura de la comunidad de Anolis en diferentes coberturas vegetales sugiere que los bosques proporcionan más refugios, recursos

DIVERSIDAD DE ANOLIS DEL CHOCÓ, COLOMBIA

59

Figura 3: Curvas de rango-abundancias (Log(pi)) de la comunidad de Anolis en tres coberturas vegetales en la selva pluvial tropical en la zona centro del Chocó, Colombia. Las letras en mayúscula representan las especies de Anolis detectadas en este estudio (la correspondencia de cada letra con la especie de Anolis aparece detallada en la Tabla 1.

alimenticios y zonas adecuadas para la reproducción. Además, nuestro estudio mostró una alta complementariedad entre las áreas I y II, debido probablemente a la cercanía física entre ambas, mientras que la zona de gestión (área III) fue la más diferenciada, probablemente debido a los procesos extractivos que presenta. Los grupos de similitud mostrados son debidos, probablemente, al hecho de que las áreas comparten algunas características, favoreciendo la convergencia de ciertas especies en sitios particulares, siendo la presencia de arbustos y árboles con troncos desnudos un factor importante. El segundo grupo de afinidad está caracterizado por ser una zona en regeneración que alberga especies que no requieren condiciones específicas de un bosque bien conservado, pero sí una vegetación de soporte, con vegetación heterogénea. Además, la relativa cercanía de dos áreas diferentes (áreas I y II) permite compartir un número de especies que pueden extenderse hasta llegar a usar las dos zonas.

Por otro lado, el área de gestión, debido al

alto grado de perturbación a la que se encuentra sometida por causa de acciones antrópicas, ha visto modificada gran parte de su cobertura vegetal, obligando así a la desaparición y migración de algunas especies con requerimientos particulares.

De las especies registradas en este estudio, solamente A. granuliceps ha sido evaluada por la Unión Internacional para la Conservación de la Naturaleza (CASTRO & MAYER, 2013) y catalogada con el estatus de preocupación menor (LC). Algunos de los riesgos potenciales que pueden afectar a las poblaciones de este grupo, dado que ocupan áreas con gran cobertura vegetal y usan hábitats específicos, son la tala de árboles, la contaminación ambiental y el cambio climático.

Agradecimiento Se agradece a la Fundación Carolina España, Universidad de León, Grupos de Investigación en Herpetología y zoología de la Universidad Tecnologica del Chocó, y a las

60

RENGIFO M. ET AL.

comunidades negras asentadas en cada uno de los puntos de muestreo.

REFERENCIAS áLVAREz, M.; CóRDOBA, S.; ESCOBAR, F.; FAGUA, G.; GAST, F.; MENDOzA, H.; OSPINA, M.; UMAñA, A.M. & VILLAREAL, H. (2004). Manual de Métodos para el Desarrollo de Inventarios de Biodiversidad.

Programa de Inventarios de Biodiversidad, Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, Colombia.

BAEV, P.V. & PENEV, L.D. (1995). BIODIV: Program for Calculating Biological Diversity Parameters, Similarity and Niche Overlap, and Cluster Analysis: Version 5.1.

Pensoft, Sofia, Bulgaria - Moscú, Rusia.

BECCALONI, G.w. & GASTON, K.J. (1995).

Predicting the species richness of Neotropical forest butterflies: Ithomiinae (Lepidoptera: Nymphalidae) as indicators. Biological Conservation 71: 77-86.

C ASTAñO -M, O.V.; C áRDENAS -A, G.; HERNáNDEz-R, E.J. & CASTRO-H, F. (2004). Reptiles en el Chocó Biogeográfico, In J.O. Rangel-Ch (ed) Colombia, Diversidad Biótica IV. El Chocó Biogeográfico / Costa Pacífica.

Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá, Colombia, pp 277-324.

CASTRO, F. & MAYER, G.C. (2013). Anolis granuliceps, In The IUCN Red List of Threatened Species. Version 2014.3.

International Union for Conservation of Nature, Gland, Switzerland. Disponible en http://www.iucnredlist.org/. Consultado el 31/12/2014.

CHAO, A. (1987). Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43: 783-791.

COLwELL, R.K. & CODDINGTON, J.A. (1994). Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society B 345: 101-118.

COLwELL, R.K.; MAO, C.X. & CHANG, J. (2004). Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85: 2717-2727.

CRUMP, M. & SCOTT, N. (1994). Visual Encounter Surveys, In R.M. Heyer, Y.R. Donnelly, L. McDiarmid, A. Hayek, & M. Foster (eds.) Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press, washington, DC, USA, pp. 84-92.

CUATRECASAS, J. (1958). Aspectos de la vegetación natural de Colombia. Revista de la Academia Colombiana de Ciencias 10: 221-268.

DI CASTRI, F. & YOUNES, T. (1990). Ecosystem Function of Biological Diversity. Biology International, Special Issue 22. IUSB, Paris, Francia.

DUELLMAN, w.E. (1978). The biology of an Equatorial herpetofauna in Amazonian Ecuador. Miscellaneous Publications of the University of Kansas Museum of Natural History 65: 1-352.

ESLAVA, J.A. (1994). Climatología del Pacífico Colombiano. Serie: Colección Eratóstenes, vol. 1. Academia Colombiana de Ciencias Geofísicas, Santa Fé de Bogotá DC, Colombia.

FEISINGER, P. (2001). Designing Field Studies for Biodiversity Conservation. Island Press,

DIVERSIDAD DE ANOLIS DEL CHOCÓ, COLOMBIA

washington, DC, USA. FORERO, E. & GENTRY, A.H. (1989). Lista Anotada de las Plantas del Departamento del Chocó, Colombia. Instituto de Ciencias Naturales, Museo de Historia Natural, Universidad Nacional de Colombia, Bogotá, Colombia.

FROST, D.R. & ETHERIDGE, R. (1989). A phylogenetic analysis and taxonomy of Iguanian lizards (Reptilia:Squamata).

Miscellaneous Publications of the University of Kansas Museum of Natural History 81: 1-65.

G ARCÍA , U. & M OSQUERA , F. (2005).

Caracterización Taxonómica de la Comunidad de Lagartos (SquamataLacertilia) en el Sotobosque de la Cuenca del Rio Cabi, Chocó. Tesis de Grado, Universidad Tecnológica del Chocó “Diego Luís Córdoba”, Quibdó, Colombia.

G UYER , C. & S AVAGE , J.M. (1986).

Cladistic relationships among Anoles (Sauria: Iguanidae). Systematic Zoology 35: 509-531.

HALFFTER, G.; MORENO, C.E. & PINEDA, E.O. (2001). Manual para la Evaluación de la Biodiversidad en Reservas de la Biosfera. Serie: Manuales y Tesis, vol. 2.

Sociedad Entomológica Aragonesa, zaragoza, España.

HAMMER, Ø.; HARPER, D.A.T. & RYAN, P.D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 4.

IRSCHICK, D.J.; VITT, L.J.; z ANI, P.A. & LOSOS, J.B. (1997). A comparison of evolutionary radiations in mainland and Caribbean Anolis lizards. Ecology 78: 2191-2203.

61

JACKMAN, T.; LOSOS, J.B.; LARSON, A. & DE QUEIROz, K. (1997). Phylogenetic studies of convergent adaptive radiations in Caribbean Anolis lizards, In T.J. Givnish & K.J. Sytsma (eds.) Molecular Evolution and Adaptive Radiation.

Cambridge University Press, Cambridge, UK, pp. 535-557.

LOSOS, J.B.; JACKMAN, T.R.; LARSON, A.; DE Q UEIROz , K. & RODRÍGUEz SCHETTINO, L. (1998). Historical contingency and determinism in replicated adaptive radiations of island lizards.

Science 279: 2115-2118.

LOSOS, J.B. (1994). Integrative approaches to evolutionary ecology: Anolis lizard as model systems. Annual Review of Ecology and Systematics 25: 467-493.

MAGURRAN, A.E. (1988). Ecological Diversity and its Measurement. Princeton University Press, Princeton, NJ, USA. MAGURRAN, A.E. (2004). Measuring Biological Diversity. Blackwell Publishing, Oxford, UK. MURILLO, F.J. (2004). Contribución al Conocimiento de la Ofidiofauna de Cuatro Comunidades de la Cuenca Hidrográfica del Rió Cabí Chocó, Colombia. Trabajo de Grado, Universidad Tecnológica del Chocó “Diego Luís Córdoba”, Quibdó, Colombia.

PáEz, V.P.; BOCK, B.C.; ORTEGA, A.M.; E STRADA , J.J.; D AzA , J.M. & GUTIéRREz-C, P.D. (2002). Guía de Campo de Algunas Especies de Anfibios y Reptiles de Antioquia. Editorial Multimpresos, Medellín, Colombia.

PETERS, J.A. & DONOSO-BARROS, R. (1970).

Catalogue of the Neotropical Squamata.

Part II. Lizards and Amphisbaenia. United

62

RENGIFO M. ET AL.

States Natural History Museum Bulletin 297: 1-293.

PLEGUEzUELOS, J. & FERICHE. M. (2004).

Anfibios y Reptiles. Diputación de Granada, Granada, España.

POVEDA, M.C.; ROJAS, C.A.; RUEDAS, A. & RANGEL, J.O. (2004). El Chocó biogeografico: Ambiente físico, In C.H. Rangel (ed.)

Colombia Diversidad Biótica IV. El Chocó Biogeografico/Costa Pacífica. Instituto de Ciencias Naturales, Bogotá DC, Colombia, pp. 1-21.

POwELL, R.; HENDERSON, R.w.; ADLER, K. & DUNDEE, H.A. (1996). An annotated checklist of west Indian amphibians and reptiles, In R. Powell & R.w. Henderson (eds.) Contributions to West Indian Herpetology: A Tribute to Albert Schwartz.

Society for the Study of Amphibians and Reptiles, Ithaca, NY, USA. pp 51–93.

P RENDERGAST, J.R. & EVERSHAM , B.C. (1997). Species richness covariance in higher taxa: empirical tests of biodiversity indicator concept. Ecography 20: 210-216.

RANGEL-CH, J.O. & LOwY. P. (1993). Tipos de vegetación y rasgos fitogeográficos en la Región Pacífica de Colombia, In P. Leyva (ed.) Colombia Pacífico Tomo I. Publicaciones FEN, Instituto de Ciencias Naturales, Santa Fé de Bogotá, Colombia. pp. 184-198.

RENGIFO, J.T. (2002). Composición y Estructura de la Comunidad de Reptiles Presente en Dos Zonas del Bosque Pluvial Tropical en el Departamento del Chocó. Trabajo de Grado, Universidad Tecnológica del Chocó Diego Luis Córdoba, Quibdó, Colombia.

RENGIFO, J.T. (2011). Reptiles del departamento del Chocó, Colombia. Revista Biodiversidad Neotropical 11: 38-47.

RENGIFO-MOSQUERA, J.T.; ASPRILLA, J.; JIMéNEz, O.A.; RENJIFO, J.M. & CASTRO, A.A. (2002). Ecología y estructura taxonómica de la comunidad de reptiles presentes la granja de la universidad Tecnológica del Chocó, Municipio de Lloró-Chocó.

Revista Institucional Universidad Tecnológica del Chocó Diego Luis Córdoba 8: 46-52.

RENJIFO, J.M. & LUNDBERG, M. (1999).

Anfibios y Reptiles de Urrá: Guía de Campo. Colonias de Medellín, Medellín, Colombia.

RENTERÍA, M.L. (2006). Caracterización Taxonómica de la Comunidad de Reptiles Presentes en la Estación Ambiental Tutunendo (EAT), Quibdó-Chocó. Trabajo de Grado, Universidad Tecnológica del Chocó Diego Luis Córdoba, Quibdó, Colombia.

RÍOS, E.E. & HURTADO, C.F. (2007).

Contribución al Conocimiento de la Ecología de las Comunidades de Lagartos Presentes en Dos Zonas de Bosque en el Chocó Biogeográfico Colombiano. Trabajo de Grado, Universidad Tecnológica del Chocó Diego Luis Córdoba, Quibdó, Colombia.

RÍOS, E.E.; HURTADO P., C.F.; RENGIFO M., J.T. & CASTRO HERRERA, F. (2011).

Lagartos en comunidades naturales de dos localidades en la región del Chocó de Colombia. Herpetotropicos 5: 85-92.

SAVAGE, J.M. & GUYER, C. (1989). Infrageneric classification and species composition of the Anole genera, Anolis, Ctnonotus, Dactyloa, Norops and Semiurus (Sauria:Iguanidae).

Amphibia-Reptilia 10: 105-116.

SUáREz NAVARRO, A.E.; HURTADO-PEñA, G.; CARVAJAL-LEMUS, F.J.; RODRÍGUEzBAUQUERO, JE. & RODRÍGUEz-SOTO, R. (1984). Mapa de Bosques de Colombia:

DIVERSIDAD DE ANOLIS DEL CHOCÓ, COLOMBIA

Memoria explicativa. Instituto Geográfico "Agustín Codazzi" - Instituto Nacional de Desarrollo de los Recursos Naturales y del Ambiente - Corporación Nacional de Investigación y Fomento Forestal, Bogotá, Colombia.

VISAUTA VINACUA, B. & MARTORI I CAñAS, J.C. (1998), Análisis Estadístico con SPSS para Windows. Estadística Multivariante.

McGraw Hill, Barcelona, España. wILLIAMS, E.E. (1976). west Indian anoles: A taxonomic and evolutionary summary.

63

I. Introduction and a species list. Breviora 440: 1-21. wILLIAMS, E.E. (1983). Ecomorphs, Faunas, Island Size, and Diverse End Points in Island Radiations of Anolis, In R.B. Huey, E.R. Pianka & T.w. Schoener (eds.)

Lizard Ecology: Studies of a Model Organism. Harvard University Press, Cambridge, MA, USA. 326-370 pp. wILLIAMS, E.E. (1992). The Anolis Handlist.

Museum of Comparative zoology, Harvard University, Cambridge, MA, USA.

64

Basic and Applied Herpetology 28 (2014): 65-77

Una nueva especie de Liolaemus del grupo de L. nigromaculatus (Iguania: Liolaemidae) para la Región de Atacama, Chile Yery Marambio-Alfaro1, Jaime Troncoso-Palacios2,* 1 2

Programa Doctorado en Ciencias Aplicadas, Mención en Sistemas Marinos Costeros, Universidad de Antofagasta, Antofagasta, Chile.

Programa de Fisiología y Biofísica, Facultad de Medicina, Universidad de Chile, Santiago, Chile.

* Correspondence: Facultad de Medicina, Universidad de Chile, Casilla 70005, Santiago, Chile. E-mail: jtroncosopalacios@gmail.com

Recibido: 21 Agosto 2013; revisión recibida: 6 Mayo 2014; aceptado: 6 Mayo 2014.

Aquí describimos una nueva especie de Liolaemus (Iguania: Liolaemidae) del desierto costero de Atacama en las cercanías de Barranquilla, Chile. Esta nueva especie pertenece al grupo L. nigromaculatus y se distingue de las otras especies de este grupo y del género Liolaemus, por el llamativo patrón de coloración del macho, que presenta la cabeza y el dorso de color negro y los muslos y cola de color azul celeste, así como otras características de folidosis que permiten su diagnóstico. Con esta nueva especie, el grupo L. nigromaculatus asciende a 13 especies.

Key words: Atacama; Chile; Liolaemus nigrocoeruleus sp. nov.; L. nigromaculatus; L. platei.

A new species of Liolaemus of the L. nigromaculatus group (Iguania: Liolaemidae) from Atacama Region, Chile.

Here, we describe a new species of Liolaemus (Iguania: Liolaemidae) from the coastal desert of Atacama in the vicinity of Barranquilla, Chile. This new species belongs to the L. nigromaculatus group and can be distinguished from the other species of the group and the remaining species of the genus Liolaemus, by the striking color pattern of the male, with black head and dorsum, and light blue thighs and tail, as well as other scalation features that allow its diagnosis. with this new species, the L. nigromaculatus group increases to 13 species.

Key words: Atacama; Chile; Liolaemus nigrocoeruleus sp. nov.; L. nigromaculatus; L. platei.

El género Liolaemus contiene en la actualidad 242 especies (UETz & HOšEK, 2014), distribuidas en la parte sur de Sudamérica, desde las montañas de la zona central del Perú hasta Tierra del Fuego (ETHERIDGE & ESPINOzA, 2000; ESQUERRé et al., 2013). El género ha sido subdividido en dos subgéneros: Liolaemus (sensu stricto) y Eulaemus (LAURENT, 1985), cada uno subdividido a su vez en varios grupos (LOBO et al., 2010; FONTANELLA et al., 2012).

Las especies relacionadas con Liolaemus platei werner, 1898 presentan una historia taxonómica compleja. Tradicionalmente se han asignado al grupo de L. nigromaculatus (wiegmann, 1835) del subgénero Liolaemus, aunque lamenDOI: http://dx.doi.org/10.11160/bah.13011/

tablemente ningún estudio filogenético realizado hasta la fecha sobre el grupo de L. nigromaculatus ha incorporado comparaciones genéticas. ORTIz (1981) realizó el primer estudio cladístico de este grupo y propuso la división del grupo L. nigromaculatus en dos subgrupos (sin denominación). Posteriormente, LOBO (2001) consideró este grupo como parafilético y propuso tres grupos independientes: copiapensis, hellmichi y nigromaculatus. Sin embargo, en un nuevo análisis filogenético, LOBO (2005) propuso que las especies del grupo nigromaculatus conforman un sólo grupo monofilético.

PINCHEIRA-DONOSO & NúñEz (2005) denominaron a este conjunto de especies “complejo nigromaculatus”, indicando que éste está com-

66

MARAMBIO-ALFARO & TRONCOSO-PALACIOS

puesto por dos grupos diferenciables por varios caracteres de folidosis: grupo nigromaculatus y grupo platei. Sin embargo, esta propuesta no fue aceptada por LOBO et al. (2010), quienes rechazaron la existencia del grupo de L. platei, ya que PINCHEIRA-DONOSO & NúñEz (2005) no presentaron datos para sustentar su propuesta y las relaciones filogenéticas presentadas estaban basadas en un método desactualizado (análisis fenético).

Además, la identidad misma de L. nigromaculatus fue hasta hace poco motivo de gran controversia. Sólo recientemente TRONCOSOPALACIOS & GARÍN (2013) identificaron a esta especie nominal y tras revisar todas las especies del grupo nigromaculatus (con la excepción de L. ater) aceptaron provisionalmente la hipótesis de PINCHEIRA-DONOSO & NúñEz (2005), dado que el grupo platei y el grupo nigromaculatus muestran caracteres morfológicos diferentes que permiten su separación en dos grupos morfológicamente distintos, denominando al segundo de estos grupos como “nigromaculatus group, sensu stricto” (TRONCOSO-PALACIOS & GARÍN, 2013:44). Además, esta hipótesis se ha corroborado en un estudio filogenético basado en evidencias moleculares (TRONCOSOPALACIOS et al., en preparación). Sin embargo, dado que hasta la fecha no se ha publicado un estudio más concluyente al respecto, la propuesta más actualizada por el momento es la disponible en LOBO et al. (2010).

De acuerdo con LOBO et al. (2010) el grupo de L. nigromaculatus está conformado actualmente por: L. atacamensis Müller & Hellmich, 1933, L. ater Müller & Hellmich, 1933, L. bisignatus (Philippi, 1860), L. donosoi Ortiz, 1975, L. hellmichi Donoso-Barros, 1975, L. kuhlmanni Müller & Hellmich,

1933, L. melaniceps Pincheira-Donoso & Núñez, 2005, L. nigromaculatus, L. platei, L. pseudolemniscatus Lamborot & Ortiz, 1990, L. sieversi Donoso-Barros, 1954, L. silvai Ortiz, 1989, L. velosoi Ortiz, 1987 y L. zapallarensis Müller & Hellmich, 1933.

Posteriormente, TRONCOSO-PALACIOS & GARÍN (2013) demostraron que L. bisignatus es un sinónimo de L. nigromaculatus y TRONCOSO-PALACIOS (2013) concluyó que L. donosoi es un sinónimo de L. constanzae Donoso-Barros, 1961 (especie del grupo nigroviridis). Por lo tanto, el grupo se compone, hasta este estudio, de doce especies.

Por otra parte, la región desértica de Atacama en Chile presenta un 42% de reptiles endémicos (TRONCOSO-PALACIOS & MARAMBIO-ALFARO, 2011), pero el grado de conocimiento de la biodiversidad regional es uno de los más bajos de Chile (SIMONETTI et al., 1995). Durante una campaña de terreno en las cercanías de localidad costera de Barranquilla, Región de Atacama (Chile), se colectaron especímenes cuyas características difieren notablemente de todas las otras especies conocidas. Esta nueva especie se asemeja morfológicamente a L. platei. En este estudio se describe a esta nueva especie y se proveen los caracteres que permiten su diagnóstico.

MATERIALES Y MéTODOS Los caracteres para la descripción se tomaron de ETHERIDGE (1995), ORTIz (1981) y LOBO (2001, 2005). Las mediciones se hicieron con un calibre digital vernier (± 0,02 mm de precisión). La variación de las medidas se indica como promedio ± desviación estándar.

La observación de las escamas se realizó con lupas de distinto aumento. Las medidas y los

67

NUEVA ESPECIE DE LIOLAEMUS DE ATACAMA

datos de folidosis se tomaron en el lado derecho, salvo cuando se indica lo contrario. Los especímenes se colectaron usando un lazo o a mano y fueron sacrificados con Lidocaína 2% según el método descrito por NúñEz et al.

(2003). Dos de los especímenes colectados (SSUC Re 531 y 532) fueron fijados en formaldehído al 10% y preservados en etanol 70%, los restantes fueron fijados y preservados en etanol 95%. Todos los ejemplares se depositaron en la Colección de Flora y Fauna Profesor Patricio Sánchez Reyes de la Pontificia Universidad Católica de Chile (SSUC). La lista de los especímenes examinados se detalla en el Apéndice. a

b

Figura 1: Liolaemus nigrocoeruleus sp. nov.

(Holotipo SSUC Re 0527, longitud hocico-cloaca = 56,1 mm.). (a) Vista dorsal. (b) Vista ventral.

Para comparar los conteos de escamas ventrales se usó la prueba U de Mannwhitney. Se consideró un valor de probabilidad significativa de P< 0,05. Los datos de L. ater se tomaron a partir de fotografías digitales de especímenes tipo proporcionadas por Frank Tillack (Museum für Naturkunde, Berlín, Alemania).

RESULTADOS Liolaemus nigrocoeruleus sp. nov.

Holotipo: SSUC Re 0527 (Fig. 1). Macho adulto. Colectado a siete kilómetros al NE de Barranquilla (27º27’35’’S – 70º50’43’’w, Fig. 2), en una loma sin nombre, a 200 m sobre el nivel del mar. Provincia de Copiapó, Región de Atacama, Chile. Colectado por J. TroncosoPalacios y Y. Marambio-Alfaro en mayo de 2012.

Paratipos: SSUC Re 0528 a 0532, 0552 a 0554. Dos machos, tres juveniles y tres hembras. Colectados a siete kilómetros al NE de Barranquilla (27º27’35’’S – 70º50’43’’w, Fig. 2), en una loma sin nombre, a 200 m sobre el nivel del mar. Provincia de Copiapó, Región de Atacama, Chile. Colectados por J. Troncoso-Palacios y Y. Marambio-Alfaro en mayo de 2012. SSUC Re 0533 y 0534. Un macho y un juvenil. Colectados a nueve kilómetros al NE de Barranquilla (27º27’00’’S – 70º49’41’’w), en una loma sin nombre, a 180 m sobre el nivel del mar. Provincia de Copiapó, Región de Atacama, Chile.

Colectados por J. Troncoso-Palacios y Y. Marambio-Alfaro en mayo de 2012.

Etimología: El epíteto nigrocoeruleus hace referencia al diseño de coloración negro y azulado que presenta el macho de Liolaemus nigrocoeruleus sp. nov.

68

MARAMBIO-ALFARO & TRONCOSO-PALACIOS

Figura 2: Mapa de distribución de Liolaemus nigrocoeruleus sp. nov. y las especies morfológicamente relacionadas. Triangulo = L. hellmichi. Estrella = L. nigrocoeruleus. Diamante = L. platei. Cuadrado = L. velosoi.

Algunas localidades para L. platei fueron tomadas de los apéndices de material examinado de otras publicaciones: Carén y Chañar Blanco (NúñEz et al., 2001); Morrillos, El Teniente, Andacollo y Totoralillo (PINCHEIRA-DONOSO & NúñEz, 2005). Los límites regionales y los nombres de las regiones están indicados.

Diagnosis Liolaemus nigrocoeruleus sp. nov. pertenece al grupo L. nigromaculatus, dentro del cual puede asociarse, de acuerdo a su morfología, con L. hellmichi, L. platei y L. velosoi. Liolaemus nigrocoeruleus sp. nov. se diferencia de L. atacamensis, L. ater, L. kuhlmanni, L. melaniceps, L. nigromaculatus, L. sieversi, L. silvai y L. zapallarensis, porque estas especies presentan siem-

pre la escama nasal separada de la rostral (siempre en contacto en L. nigrocoeruleus sp. nov.).

Liolaemus nigrocoeruleus sp. nov. se diferencia de L. hellmichi, L. platei y L. velosoi (Fig. 3), en que estas especies presentan abundantes gránulos entre las escamas de los flancos (escasos en L. nigrocoeruleus). Las escamas temporales están débilmente aquilladas en L. hellmichi y L. velosoi pero fuertemente aquilladas en L. nigrocoeruleus (Fig. 4). En L. velosoi las escamas temporales se disponen de forma yuxtapuesta o subimbricada, mientras que en L. nigrocoeruleus están dispuestas de forma imbricada. Liolaemus nigrocoeruleus presenta un mayor número de escamas ventrales (85,1 ± 4,8) que L. hellmichi (81,2 ± 1,3) (Mann–whitney U = 15,0; 16 g.l.; P = 0,04), que L. platei (77,1 ± 3,7) (U = 9,0; 21 g.l.; P< 0,01) y que L. velosoi (76,4 ± 2,2) (U = 9,0; 36 g.l.; P< 0.01). Liolaemus hellmichi, L. platei y L. velosoi presentan escamas dorsales terminadas en una punta menos aguzada que la de L. nigrocoeruleus (Fig. 4). La garganta de los machos de L. hellmichi, L. platei y L. velosoi presenta un diseño distinto al de L. nigrocoeruleus (Tabla 1). El color y diseño del dorso de los machos de L. hellmichi, L. platei y L. velosoi es totalmente diferente al del macho de L. nigrocoeruleus (Tabla 1). Liolaemus hellmichi, L. platei y L. velosoi presentan un dicromatismo sexual poco acentuado, mientras que L. nigrocoeruleus presenta un dicromatismo sexual mucho más evidente, expresado en un color y diseño totalmente diferente entre machos y hembras (Fig. 3). Liolaemus nigrocoeruleus sp. nov. se diferencia de L. pseudolemniscatus en que este último carece de mancha antehumeral, presente en la hembra de L. nigrocoeruleus. Además, los machos de L. pseudolemniscatus no presentan melanismo en el dorso ni la cola azul celeste.

NUEVA ESPECIE DE LIOLAEMUS DE ATACAMA

69

a

b

c

d

Figura 3: Algunas de las especies usadas en este estudio. (a) Liolaemus hellmichi (topotipos: macho MzUC 25945 y hembra MzUC 25950). (b) L. nigrocoeruleus (paratipos: macho SSUC Re 533 y hembra SSUC Re 532). (c) L. platei (topotipos: macho SSUC Re 420 y hembra SSUC Re 526). (d) L. velosoi (especímenes de Copiapó: macho MzUC 32704 y hembra MzUC 32706).

Descripción del holotipo Macho adulto. Longitud hocico-cloaca: 56,1 mm. Diámetro horizontal del ojo: 3,6 mm. Longitud del subocular: 4,4 mm.

Longitud de la cuarta supralabial: 2,0 mm.

Longitud de la cabeza (medido desde el borde

posterior de la apertura del oído hasta la punta del hocico): 15,4 mm. Alto de la cabeza (medido a nivel del meato auditivo): 6,2 mm. Ancho de la cabeza (medido entre ambos meatos auditivos): 10,1 mm. Ancho del cuello: 9,6 mm.

Distancia oído-ojo: 5,1 mm. Distancia internarinas: 1,9 mm. Longitud axila ingle: 21,5 mm.

70

MARAMBIO-ALFARO & TRONCOSO-PALACIOS

a

b

c

d

Figura 4: Caracteres comparativos. (a) Escamas temporales imbricadas y aquilladas en Liolaemus nigrocoeruleus sp. nov. (SSUC Re 531). (b) Escamas temporales yuxtapuestas-subimbricadas y ligeramente aquilladas o lisas en L. velosoi (MzUC 36624). (c) Escamas dorsales en L. nigrocoeruleus (SSUC Re 0527). (d) Escamas dorsales en L. platei (SSUC Re 420).

Ancho del cuerpo (medido en la parte media del tronco): 14,2 mm. Longitud del muslo: 10,1 mm. Longitud de la tibia: 9,9 mm.

Longitud del húmero: 7,2 mm. Longitud del antebrazo: 6,3 mm. Longitud de la mano: 7,5 mm. Longitud de la cola (no autotomizada): 67,4 mm. Ancho de la cloaca: 6,3 mm.

Longitud del pie derecho: 17,3 mm. Distancia interorbital: 2,4 mm. Ancho del oído: 1,3 mm.

Alto del oído: 1,4 mm.

Interparietal pentagonal más pequeña que los parietales y rodeada por ocho escamas.

Siete escamas entre el interparietal y rostral.

Circum orbital incompleto. Tres escamas supraoculares en cada lado. Seis escamas superciliares. Frontal dividido en dos escamas. Dos escamas entre la nasal y canthal. Cuatro escamas entre la subocular y la nasal. Nasal en contacto con la rostral y rodeada por seis escamas.

Dos lorilabiales en contacto con la subocular.

Cinco escamas supralabiales, la cuarta se curva hacia arriba y contacta con el subocular. Cinco escamas infralabiales. Mental pentagonal, en contacto con cuatro escamas. Cuatro pares de

71

NUEVA ESPECIE DE LIOLAEMUS DE ATACAMA

Tabla 1: Caracteres de folidosis y diseño de coloración para Liolaemus nigrocoeruleus sp. nov. y las especies actualmente consideradas dentro del grupo L. nigromaculatus que presentan la característica de tener la escama nasal en contacto con la rostral (datos referentes únicamente a los especímenes adultos).

Parámetro Superficie de las escamas temporales

Disposición de las escamas temporales

Gránulos en los flancos Forma de las escamas dorsales Dicromatismo sexual

Color de fondo en el macho Diseño de la garganta en el macho

Escamas alrededor del medio del cuerpo Dorsales

Ventrales

L. hellmichi (4♂♂, 7♀♀)

L. nigrocoeruleus sp. nov. (4♂♂, 3♀♀)

L. platei (13♂, 3♀♀)

L. pseudolemniscatus (2♂♂, 2♀♀)

Ligeramente aquilladas

Aquilladas

Aquilladas

Ligeramente aquilla- Lisas (algunas ligeradas (algunas lisas) mente aquilladas)

Subimbricadas a imbricadas

Imbricadas

Imbricadas

Imbricadas

L. velosoi (20♂♂, 11♀♀)

Subimbricadas o yuxtapuestas

Abundantes

Escasos

Abundantes

Ausentes

Abundantes

Lanceoladas

Lanceoladas

Lanceoladas

Lanceoladas

Lanceoladas

Leve

Marcado

Leve

Marcado

Leve

Café amarillento Negro y celeste hacia Café amarillento la parte posterior

Gris

Café grisáceo

Líneas finas

Melánica o con líneas gruesas

Inmaculada o con líneas finas

Manchada

Inmaculada o con líneas finas

42-45

44-48

42-52

42-48

38-47

39-44

40-45

38-47

40-44

37-44

79-83

78-93

73-88

75-83

72-82

escudos postmentales; el segundo par está separado por una escama. Escama auricular no diferenciada. Dos escamas agrandadas y proyectadas en el borde anterior del oído. Escamas temporales aquilladas y dispuestas de forma imbricada. Pliegue horizontal en forma de “Y” al costado del cuello. Ocho escamas temporales entre el nivel de las superciliares y la comisura de la boca, fuertemente aquilladas, dispuestas de forma imbricada. Escamas alrededor del cuerpo: 44. Escamas dorsales: 43.

Escamas dorsales lanceoladas, aquilladas y con mucrón, sin gránulos acompañantes y dispuestas de forma imbricada. Escamas dorsales ligeramente más grandes que las ventrales. Escasos gránulos entre las escamas de los flancos.

Número de ventrales: 78. Escamas ventrales redondeadas, lisas y dispuestas de forma imbri-

cada o subimbricada, sin gránulos. Tres poros precloacales. Escamas suprafemorales lanceoladas, aquilladas, dispuestas de forma imbricada.

Escamas infrafemorales redondeadas, lisas, dispuesta de forma subimbricada. Ocho escamas proyectadas en el borde posterior ventral del muslo. Escamas dorsales del antebrazo lanceoladas, aquilladas y dispuesta de forma imbricada. Escamas ventrales del antebrazo redondeadas, lisas y dispuesta de forma imbricada.

Lamelas del cuarto dedo de la mano derecha: 20. Lamelas del cuarto dedo del pie derecho: 28. Escamas dorsales del primer tercio de la cola romboidales, fuertemente aquilladas y con mucrón, se disponen de forma imbricada.

Las escamas ventrales del primer tercio de la cola son romboidales, lisas, dispuestas de forma imbricada.

72

MARAMBIO-ALFARO & TRONCOSO-PALACIOS

Color del holotipo en vida: Parte dorsal de la cabeza, dorso, flancos y extremidades anteriores de color negro brillante. La subocular es blanca, con dos líneas negras verticales.

Hacia la base de la cola aparecen escamas celestes que se hacen más abundantes hacia la parte posterior, dándole a la cola una coloración dorsal celeste. Extremidades posteriores de color negro brillante en la parte dorsal anterior y de color celeste en la parte dorsal posterior. Garganta melánica. Vientre melánico, excepto en la zona media. Pecho, zona media del abdomen, cara ventral de las extremidades y cola de color gris.

Variación Datos basados en cuatro machos (incluido el holotipo), tres hembras y cuatro juveniles.

Longitud de la cabeza en machos entre 15,1 y 15,7 mm (media ± DE = 15,4 ± 0,3 mm), ancho de la cabeza en machos entre 9,7 y 10,3 mm (10,1 ± 0,3 mm), altura de la cabeza en machos entre 6,2 y 6,7 mm (6,5 ± 0,2 mm), ancho del cuello en machos entre 8,9 y 9,6 mm (9,3 ± 0,3 mm), longitud hocico-cloaca en machos entre 50,6 y 56,1 mm (53,0± 2,3 mm) y longitud de la cola en machos (considerando dos machos y autotomizada en el resto) entre 67,4 y 86,1 mm (77,1 ± 9,4 mm), longitud de la cabeza en las hembras de 10,5 a 12,5 mm (11,7 ± 1,1 mm), ancho de la cabeza en las hembras entre 7,4 y 9,6 mm (8,7 ± 1,1 mm), alto de la cabeza en las hembras entre 4,6 y 5,4 mm (5,1 ± 0,4 mm), ancho del cuello en las hembras entre 6,2 y 8,3 mm (7,4 ± 1,0 mm), longitud hocico-cloaca en las hembras entre 42,6 y 50,9 mm (45,6 ± 4,6 mm), 56,9 mm de longitud de la cola en la hembra SSUC Re 532 y autotomizada en el resto.

La variación folidótica es: cinco escamas supralabiales. Tres o cuatro supraoculares.

Frontal no dividida, dividida en una escama anterior y otra posterior, o dividida en una anterior y dos posteriores. Interparietal de menor tamaño que las parietales y rodeada por 6-8 escamas. Nasal rodeada de seis escamas.

Cinco infralabiales. Cuatro escamas en contacto con la mental. Una o dos escamas de mayor tamaño en el margen anterior del oído. Escama auricular no diferenciada o ancha y restringida al tercio superior del meato. Pliegue horizontal en forma de «Y» entre el hombro y el oído.

Entre 44 y 48 escamas alrededor del cuerpo en su parte media (46,6 ± 1,5). De 40 a 45 escamas dorsales (42,7 ± 2,4), de 78 a 93 escamas ventrales (85,1 ± 4,8). Machos con tres poros precloacales. Hembras sin poros precloacales.

Escamas del dorso lanceoladas, imbricadas, con quillas y mucrón. Escamas dorsales más grandes que las ventrales.

En general, los machos presentan el patrón de coloración descrito para el holotipo, aunque en algunos especímenes el hocico es de color café muy oscuro, la garganta puede presentar un diseño de líneas oscuras o ser melánica. Flancos de color negro intenso. El vientre es melánico o gris con manchas oscuras dispersas. Las hembras presentan un color de fondo pardo oscuro. La cabeza presenta pequeñas manchas oscuras dispersas. Línea supraocular y subocular amarillenta. Banda temporal formada por manchas oscuras, las cuales se hacen más difusas hacia la extremidad posterior. Manchas para-vertebrales de color café oscuro, que tienden a conectarse con la línea vertebral. Cola con diseño dorsal formado por manchas oscuras paralelas.

Extremidades de color café con manchas

73

NUEVA ESPECIE DE LIOLAEMUS DE ATACAMA

oscuras. Las extremidades posteriores y la cola presentan escasas escamas de color azul celeste. Garganta de color gris con finas líneas oscuras. Vientre de color gris.

El diseño de los juveniles se corresponde con el de las hembras.

Distribución, hábitat e historia natural Solamente conocida en las lomas costeras al sur de Barranquilla. Actualmente sólo se ha colectado en dos puntos (distanciados por unos 2 km), aunque probablemente la especie esté presente en todo el conjunto de lomas. El hábitat de L. nigrocoeruleus consiste en lomas costeras de pendiente suave, con una elevación máxima de 350 m y mínima de 140 m, con presencia de abundantes afloramientos rocosos. Estas lomas cubren un área aproximada de 50 km2 y están rodeadas por desierto. Cinco kilómetros hacia el norte de las lomas, la zona desértica es interrumpida por la cuenca del río Copiapó. La vegetación está conformada principalmente por arbustos (Atriplex sp, Heliotropium floridum y Tetragonia macrocarpa) y herbáceas perennes (Cristaria sp., Encelia canescens y Polyachyrus poeppigii). Las cactáceas están representadas por algunos ejemplares de Eulychnia breviflora, Copiapoa marginata y escasos ejemplares de Eriosyce sp.

Liolaemus nigrocoeruleus es una especie diurna de hábitos saxícolas. Se han observado especímenes entre las 12:00 y las 18:00 horas.

Es una especie poco abundante, siendo su captura una tarea difícil. Fue encontrada junto a L. nigromaculatus. El lagarto Callopistes maculatus Gravenhorst, 1838 fue registrado en el lugar y probablemente constituye un depredador.

DISCUSIóN La región de Atacama en Chile ha arrojado importantes descubrimientos herpetológicos en los últimos años. NúñEz et al.

(2003) describieron Liolaemus manueli en la localidad de Diego de Almagro y más tarde NúñEz et al. (2012) reportaron una población aislada de L. manueli a unos 110 km al suroeste de la distribución original. Este último hallazgo se realizó en la localidad de Caserón (29º23’S; 70º42’O), a unos 40 km al nordeste de donde se realizó el descubrimiento de L. nigrocoeruleus. Llama la atención que esta zona desértica de la Región de Atacama concentre varios descubrimientos herpetológicos importantes en poco tiempo, probablemente debido a las escasas prospecciones realizadas en esta zona, mayoritariamente debido al mal estado de los caminos y a los escasos asentamientos humanos existentes en esta zona.

El diseño de coloración del macho de L. nigrocoeruleus resulta extremadamente llamativo. Ninguna otra especie del grupo L. nigromaculatus presenta un diseño con dos colores distribuidos uno en la parte dorsal superior y otro en la parte dorsal inferior. De hecho, al menos en las especies chilenas de Liolaemus, solo se observa un patrón similar en L. tenuis (Duméril & Bibron, 1837). En esta especie el macho presenta la parte dorsal superior del cuerpo de color verde y la parte dorsal inferior del cuerpo de color azul celeste (PINCHEIRA -D ONOSO & N úñEz , 2005).

Sin embargo, esta especie no tiene relación con L. nigrocoeruleus, y actualmente se considera miembro del grupo pictus (LOBO et al., 2010).

74

MARAMBIO-ALFARO & TRONCOSO-PALACIOS

Por otra parte, las relaciones filogenéticas del grupo de L. nigromaculatus son aún motivo de controversia. En este trabajo hemos usado la propuesta más actualizada (LOBO et al., 2010) pese a las diferencias morfológicas entre las especies atribuidas a este grupo, las cuales se reflejan en los resultados preliminares de un estudio filogenético en preparación (Troncoso-Palacios et al., en preparación), en el cual el grupo L. nigromaculatus y el grupo L. platei son recobrados como independientes, de manera similar a la propuesta de PINCHEIRA-DONOSO & NúñEz (2005).

Por otro lado, las especies relacionadas morfológicamente con L. platei todavía presentan ciertos aspectos no resueltos. wIEGMANN (1835) describió a Tropidurus oxicephalus (= L. oxicephalus) sin proporcionar datos sobre la localidad de colecta.

TRONCOSO-PALACIOS & GARÍN (2013) revisaron fotografías digitales de alta resolución del holotipo y proponen que es imposible determinar si éste corresponde a la especie actualmente conocida como L. platei o a L. velosoi, dado el mal estado de conservación del holotipo, que ambas especies son similares y que el espécimen podría haber sido colectado en áreas donde ambas especies habitan. Además, PHILIPPI (1860) describió a Proctotretus pallidus (= L. pallidus) para la localidad de Paposo, Región de Antofagasta (Chile). De acuerdo a ORTIz & NúñEz (1986) los especímenes tipo están perdidos. Aunque la ilustración de PHILIPPI (1860) recuerda a L. platei, es necesario realizar un muestreo en la zona para determinar si es posible confirmar la presencia de la especie y designar un neotipo.

La especie descrita en este estudio, L. nigrocoeruleus, se distribuye en los alrededores de

Barranquilla, Región de Atacama, Chile.

De acuerdo con R AMÍREz DE A RELLANO et al. (2008), en esta región el 24,5% de las especies de vertebrados presentes no se encuentran en áreas protegidas, y respecto a los reptiles, seis especies endémicas de la región no se encuentran en ninguna área protegida. En la misma situación se encuentra L. nigrocoeruleus. Esperamos que este artículo contribuya a avanzar en el conocimiento de las especies del grupo nigromaculatus, uno de los grupos de reptiles más importantes de la Región de Atacama.

Agradecimiento J. Troncoso-Palacios agradece a M. Penna su apoyo. Agradecemos a P. zavala por permitir el acceso a la Colección de Flora y Fauna Profesor Patricio Sánchez Reyes de la Pontificia Universidad Católica de Chile (SSUC), J. Artigas y J.C. Ortiz por autorizar acceso a la Colección del Museo de zoología de la Universidad de Concepción (MzUC), y a F. Troncoso por consentir el acceso a la Colección del Museo Regional de Concepción (MRC). A F. Tillack (Museum für Naturkunde, Berlín) por enviarnos fotografías digitales de especímenes tipo de Liolaemus ater. A D. Hiriart, T. Marambio y F. Ferri por su ayuda en el terreno. A M.C. Contreras por su ayuda en la identificación de flora. A la editora A. Perera Leg y a dos revisores anónimos por sus correcciones y comentarios.

Agradecemos al Servicio Agrícola y Ganadero (SAG) por las autorizaciones de captura bajo los permisos Nº1637 del 2011 y Nº2411 del 2012.

NUEVA ESPECIE DE LIOLAEMUS DE ATACAMA

REFERENCIAS ESQUERRé, D.; NúñEz, H. & SCOLARO, J.A. (2013). Liolaemus carlosgarini and Liolaemus riodamas (Squamata: Liolaemidae), two new species of lizards lacking precloacal pores, from Andean areas of central Chile.

Zootaxa 3619: 428-452.

ETHERIDGE, R. (1995). Redescription of Ctenoblepharys adspersa Tschudi, 1845, and the taxonomy of Liolaeminae (Reptilia: Squamata: Tropiduridae).

American Museum Novitates 3142: 1-34.

ETHERIDGE, R. & ESPINOzA, R.E. (2000).

Taxonomy of the Liolaeminae (Squamata: Iguania: Tropiduridae) and a semi-annotated bibliography. Smithsonian Herpetological Information Service 126: 1-64.

FONTANELLA, F.M.; OLAVE, M; AVILA, L.J.; SITES, J.w., JR. & MORANDO, M. (2012).

Molecular dating and diversification of the South American lizard genus Liolaemus (subgenus Eulaemus) based on nuclear and mitochondrial DNA sequences. Zoological Journal of the Linnean Society 164: 825-835.

LAURENT, R.F. (1985). Segunda contribución al conocimiento de la estructura taxonómica del género Liolaemus wiegmann (Iguanidae). Cuadernos de Herpetología 1(6): 1-37.

LOBO, F. (2001). A phylogenetic analysis of lizards of the Liolaemus chiliensis group (Iguania: Tropiduridae). Herpetological Journal 11: 137-150.

LOBO, F. (2005). Las relaciones filogenéticas dentro grupo chiliensis (Iguania: Liolaemidae: Liolaemus): sumando nuevos caracteres y taxones. Acta Zoológica Lilloana 49: 67-89.

75

LOBO, F.; ESPINOzA, R.E. & QUINTEROS, S. (2010). A critical review and systematic discussion of recent classification proposals for liolaemid lizards. Zootaxa 2549: 1-30.

NúñEz, H.; SCHULTE, J.A., II & GARÍN, C. (2001). Liolaemus josephorum, nueva especie de lagartija para el norte de Chile.

Boletín del Museo Nacional de Historia Natural, Chile 50: 91-107.

NúñEz, H.; NAVARRO, J.; GARÍN, C.; PINCHEIRA-DONOSO, D. & MERIGGIO, V. (2003). Phrynosaura manueli y Phrynosaura torresi, nuevas especies de lagartijas para el norte de Chile (Squamata: Sauria). Boletín del Museo Nacional de Historia Natural, Chile 52: 67-88.

NúñEz, H.; TORRES-MURA, J.C. & YáñEz, J. (2012). Nuevas localidades para lagartijas chilenas del Norte Grande. Boletín del Museo Nacional de Historia Natural, Chile 61: 177-183.

ORTIz, J.C. (1981). Estudio multivariado de las especies de Liolaemus del grupo nigromaculatus (Squamata, Iguanidae). Anales del Museo de Historia Natural de Valparaíso 14: 247-265.

ORTIz, J.C. & NúñEz, H. (1986). Catálogo crítico de los tipos de reptiles conservados en el Museo Nacional de Historia Natural, Santiago, Chile. Publicación Ocasional del Museo Nacional de Historia Natural, Chile 43: 3-23.

PHILIPPI, R.A. (1860). Reisedurch die Wüste Atacama, auf Befehl der chilenischen Regierungim Sommer 1853-1854. Eduard Anton, Halle, Alemania.

PINCHEIRA-DONOSO, D. & NúñEz, H. (2005).

Las especies chilenas del género Liolaemus wiegmann, 1834 (Iguania: Tropiduridae: Liolaeminae) Taxonomía, sistemática y evolución. Publicación Ocasional del Museo Nacional de Historia Natural, Chile 59: 7-486.

76

MARAMBIO-ALFARO & TRONCOSO-PALACIOS

RAMÍREz DE ARELLANO, P.I; TOGNELLI, M.F.; GARIN, C. & MARQUET, P.A. (2008).

Vacíos de conservación y sitios prioritarios para la conservación de los vertebrados nativos de la región de Atacama, In F.A. Squeo, G. Arancio & J.R. Gutiérrez (eds.)

Libro Rojo de la Flora Nativa y de los Sitios Prioritarios para su Conservación: Región de Atacama. Ediciones Universidad de La Serena, La Serena, Chile, pp. 251-266.

SIMONETTI, J.A.; ARROYO, M.T.K.; SPOTORNO, A.E. & LOzADA, E. (1995).

Diversidad Biológica de Chile. Comisión Nacional de Ciencia y Tecnología, Santiago, Chile.

TRONCOSO-PALACIOS J. (2013). Revisión del estatus taxonómico de Liolaemus donosoi Ortiz, 1975 (Iguania: Liolaemidae).

Boletín del Museo Nacional de Historia Natural, Chile 62: 119-127.

TRONCOSO-PALACIOS, J. & GARÍN, C.F. (2013). On the identity of Liolaemus nigromaculatus wiegmann, 1834 (Iguania, Liolaemidae) and correction of its type locality. ZooKeys 294: 37-56.

TRONCOSO-PALACIOS, J. & MARAMBIOALFARO, Y. (2011). Lista comentada de los reptiles de la Región de Atacama. Boletín del Museo Regional de Atacama 2: 62-76.

UETz, P. & HOšEK, J. (2014). The Reptile Database. Disponible en http://www. reptile-database.org/. Consultada el 03/05/2014. wIEGMANN, A.F.A. (1835). Beiträgezur zoologie, gesammeltaufeiner Reiseum die Erde, von F.J.F. Meyen. Siebente Abhandlung. Amphibien. Nova Acta Physico-Medica Academiae Caesareae Leopoldino-Carolinae Naturae Curiosorum 17: 183-268.

APéNDICE: ESPECÍMENES EXAMINADOS Los acrónimos son: MNHN-CL (Museo Nacional de Historia Natural, Chile), MRC (Museo Regional de Concepción), MzUC (Museo de zoología de la Universidad de Concepción) y SSUC (Colección de Flora y Fauna Patricio Sánchez Reyes, Pontificia Universidad Católica de Chile).

Liolaemus atacamensis. SSUC Re 469: 20 Km al norte de Vallenar; F. Ferri col. 2010.

SSUC Re 470–71: El Trapiche, Coquimbo; J. Troncoso-Palacios, Y. Marambio & D. Hiriart cols. Mayo 2012. SSUC Re 454, 464–68: Lomas de Buitre, Freirina, Atacama; J. Troncoso-Palacios, Y. Marambio & D. Hiriart cols. Mayo 2012. SSUC Re 455–61: Playa Humedal Pachingo, entre Tongoy y Puerto Aldea, Coquimbo; C. Garín col. 10/12/2009.

MzUC 30193, 30196: Punta Teatinos, sector de dunas costeras; J.C. Ortiz col. 14/09/1982.

Liolaemus hellmichi. MzUC 25942–52: Cerro Moreno; J.C. Ortiz col. 02/04/2001.

Liolaemus kuhlmanni. MzUC 28829, 28838–41: Papudo; J. Simonetti & J.C. Ortiz col. 09/09/1977. SSUC Re 282–84: Dunas de Ritoque; F. Ferri col. 13/11/2010.

SSUC Re 285–97: Caleta de La Ligua; F. Ferri col. 26/11/2010. SSUC Re 473: Dunas de Concón; J. Troncoso-Palacios & F. Urra cols. 04/01/2011.

Liolaemus melaniceps. MNHN-CL 3601–03: Isla Chungungo; J.C. Torres-Mura col. Enero 2002.

Liolaemus nigrocoeruleus. SSUC Re 527–32, 552–54: Siete kilómetros al NE de Barranquilla, en una loma sin nombre, Provincia de Copiapó, Región de Atacama, Chile; J. Troncoso-Palacios & Y. MarambioAlfaro cols. Mayo 2012. SSUC Re 533–34:

NUEVA ESPECIE DE LIOLAEMUS DE ATACAMA

Nueve kilómetros al NE de Barranquilla, en una loma sin nombre, Provincia de Copiapó, Región de Atacama, Chile; J. Troncoso-Palacios & Y. Marambio-Alfaro cols. Mayo 2012.

Liolaemus nigromaculatus. MRC 051, 053: Caldera; J. Moreno col. Mayo 1982. MRC 162, 273, 276, 282–83: Caldera; J. Moreno col. 1983. MRC 087–94: Copiapó; C. Valdovinos col. 15/09/1984. MRC 514: Copiapó. Noviembre 1996. MNHN-CL 1477: Atacama; R.A. Philippi col. MNHNCL 2237–38: 20 km de Caldera entre Copiapó y Caldera; H. Núñez col.

30/09/1991. MNHN-CL 2249–55: Travesía, Copiapó; H. Núñez col. 28/09/1999. MzUC 14820: Sector algarrobal (entre Vallenar y Copiapó); J. Moreno col. 21/08/1984. SSUC Re 478: 20 km al sur este de Puerto Viejo; J. Troncoso-Palacios & Y. Marambio cols. Mayo 2012. SSUC Re 306–15, 474-75: Caldera; F. Ferri col. Noviembre 2011. SSUC Re 476–77: Caldera, Atacama; Y. Marambio col. Mayo 2012. SSUC Re 007: Llanos de Challe; G. Lobos, A. Channier & J. González cols. 2002.

SSUC Re 453, 462–63: 50 km al norte de Vallenar; J. Troncoso-Palacios col.

05/06/2011.

Liolaemus platei. MzUC 2152–53: Combarbalá; I. Peña col. Noviembre 1961.

SSUC Re 029: Llanos de Challe; G. Lobos, A. Charrier & J. González cols. 2002. SSUC Re 317–20, 335–36, 380: Caldera; F. Ferri col. SSUC Re 321: Illapel; F. Ferri col. SSUC Re 420: Coquimbo; J. Troncoso-Palacios & Y. Marambio cols. 12/12/2011. SSUC Re 526, 555: Coquimbo; J. Troncoso-Palacios & Y. Marambio cols. Mayo 2012. MRC 058, 063: Chañaral; J. Moreno col. 28/07/1982.

77

Liolaemus pseudolemniscatus. SSUC Re 030, 031: Cerro Provincia, Región Metropolitana; J. Troncoso-Palacios col. 2010. SSUC Re 390: 20 km al sur de las Chinchillas; F. Ferri col.

17/03/2012. SSUC Re 391–93: 20 km de la costa, Salida de Cachagua, Región de Valparaíso; F. Ferri col. 18/03/2012. SSUC Re 535–536: Cerro Provincia, Región Metropolitana; J. Troncoso-Palacios & L. Negrete col. Agosto 2011.

Liolaemus sieversi. MzUC 8914, 12096–98, 12100, 12119–23, 12126, 12128: Isla Los Locos; R. Donoso-Barros col.

15/02/1954.

Liolaemus silvai. MzUC 30184: Carrizalillo; J.C. Ortiz col. Febrero 1983.

Liolaemus velosoi. MzUC 36612–14, 3661820, 36624: Estación Paipote; J.C. Ortiz col.

16/02/1978. MzUC 32695, 32699, 32702, 32704, 32706: Copiapó; R. Moreno col. Febrero 2000. MRC 054: Copiapó; Sin datos del colector, 16/06/1982. MRC 055: Copiapó; Sin datos del colector, 20/04/1982. MRC 061, 062, 066: Copiapó; Sin datos del colector, 19/07/1982.

SSUC Re 322–26: Tierra Amarilla; J. TroncosoPalacios & F. Ferri cols. 23/11/2011. SSUC Re 330: Diego de Almagro; F. Ferri & J. TroncosoPalacios cols. 09/12/2011. SSUC Re 327–29, 331–34, 419: Diego de Almagro; F. Ferri & J. Troncoso-Palacios cols. 12/12/2011.

Liolaemus zapallarensis. MzUC 29118, 29122–23: Las Tacas, Región de Coquimbo; J.C. Ortiz col. 15/10/1976. MzUC 29127: Las Tacas, Lagunillas, sector rocoso de la playa; J.C. Ortiz & J. Simonetti cols.

10/09/1977. SSUC Re 472: Totoralillo, Región de Coquimbo. J. Troncoso-Palacios & Y. Marambio cols. 12/12/2011.

78

Basic and Applied Herpetology 28(2014): 79-86

Blood differential count and effect of haemoparasites in wild populations of Pyrenean lizard Iberolacerta aurelioi (Arribas, 1994) Albert Martinez-Silvestre1,*, Oscar Arribas2 1 2

CRARC (Catalonia Reptile and Amphibian Rehabilitation Centre), Masquefa, Barcelona, Spain.

C/ Francesc Cambó, Barcelona, Spain.

* Correspondence: CRARC (Catalonia Reptile and Amphibian Rehabilitation Centre), Santa Clara s/n, 08783 Masquefa, Barcelona, Spain.

Phone: +34 937726396, E-mail: crarc@amasquefa.com

Received: 16 October 2012; received in revised form: 15 November 2012; accepted: 18 November 2012.

Differential cell count in four wild populations of Iberolacerta aurelioi (the smallest and most endangered lizard species found in the Pyrenees) has been studied. Iberolacerta aurelioi has cytological values similar to those described for other lacertid species. Moreover, the survey has detected the presence of haemoparasites genus Haemogregarina in this species. Haemoparasites are very abundant in the population of Mont-Roig, being almost insignificant in Pica d’Estats. The presence of haemoparasites is significantly related to erythroblast occurrence. Results suggest that haemoparasitism in this species stimulates high rates of blood cell regeneration.

Key words: Haemogregarina; haemoparasites; Iberolacerta aurelioi; leukocyte differential count.

Recuento diferencial y efecto de los hemoparásitos en la sangre de poblaciones silvestres de lagartija pirenaica Iberolacerta aurelioi (Arribas, 1994). Se ha estudiado el recuento sanguíneo diferencial en cuatro poblaciones de Iberolacerta aurelioi (el lacértido endémico más amenazado y de menor tamaño de los Pirineos).

Iberolacerta aurelioi tiene valores citológicos similares a los descritos para otras especies de lacértidos.

Asimismo, el análisis de frotis sanguíneos ha permitido detectar la presencia de hemoparásitos del género Haemogregarina. Estos hemoparásitos son abundantes en una de las poblaciones estudiadas (Mont-Roig) y son minoritarios en otra (Pica d’Estats). La presencia de hemoparásitos está significativamente relacionada con la aparición de eritroblastos. Los resultados sugieren que el hemoparasitismo en esta especie estimula unas altas tasas de regeneración celular sanguínea.

Key words: Haemogregarina; hemoparásitos; Iberolacerta aurelioi; recuento diferencial leucocitario.

The Pyrenean’s Rock lizard Iberolacerta aurelioi (Arribas, 1994) is endemic to the easternmost part of Central Pyrenees, where it only inhabits three mountain massifs: MontRoig, Pica d’Estats and the nucleus of Coma Pedrosa, distributed across Catalonia (northeast Spain), Andorra and the Ariège (south France). This species, discovered in the field in 1991 and described in 1994, is a small lizard (males up to 57.6 mm with average DOI: http://dx.doi.org/10.11160/bah.12007/

52.05 mm, females up to 62.21 mm with average 54.32 mm) with a body mass between 6 and 8 g. It inhabits alpine belts, usually between 2100 and 2940 m, being more abundant from 2300 to 2500 m. It lives on rocks, boulders and screes, usually in glacial cirques, in sheltered, well insolated and moderately sloped localities (ARRIBAS, 2007).

Due to the harsh climate of the areas where it is present, the species has a short annual

80

MARTÍNEZ-SILVESTRE & ARRIBAS

period of activity (four or five months, from mid-May to late September or early October; ARRIBAS, 2009).

Iberolacerta aurelioi is an endangered species, nominally protected in Spain, France and Andorra. Apart from climatic change, which is forcing this species higher up the mountain beyond its survival range, conservation problems involve any activity that implies change in the habitat of separated micropopulations. In the short term, any action involving the modification and disappearance of fragile high alpine habitats should be avoided: ski resorts, mountain refuges that attract mass tourism to inhabited areas or flooding due to hydroelectric dams, among others (ARRIBAS, 2004, 2007).

Some of the most important tools to learn about the physiological adaptations of reptiles to special environmental conditions (e.g. high mountain or insularity, among others) are haematology and blood cytology (MARTÍNEz SILVESTRE, 2011). Both are also very important aspects of the diagnostic evaluation of endangered saurians of the Lacertidae family (HERNANDEz-DIVERS et al., 2003; MARTÍNEz SILVESTRE et al., 2007; SACCHI et al., 2011).

The objective of this study is to describe basic

haematological values for I. aurelioi. Reference intervals are useful for physiological evaluation and detection of pathological alterations in wild lizards, which might be ultimately relevant for conservation purposes. Although some studies exist on haematological and biochemical values in other lacertid lizards such as the giant Canary lizards (Gallotia simonyi, G. bravoana and G. intermedia; MARTÍNEz SILVESTRE et al., 2004, MARTÍNEz-SILVESTRE et al., 2005), or Mediterranean lizards (SEVINç & UGURTAS, 2008), there are not, as far as we know, comparative haematological and cytological reference values for Pyrenean lacertid lizards. In addition, we will investigate the presence of haemoparasites. This study constitutes the first description of these parameters in the rare, endangered and high-mountain dwelling lizard I. aurelioi.

MATERIALS AND METHODS A total of 17 specimens were captured during the reproductive period (from midJune to mid-July) of 2006 in four localities (see Table 1 for more details) and sexed using described morphological characteristics (ARRIBAS, 2009).

Table 1: Localities, number of specimens, coordinates and altitude of the Iberolacerta aurelioi samples analysed. N, number of samples analysed (M: males, F: females, Sub: subadults).

Locality

Country

Locality Code

N (M / F / Sub)

Coordinates

Altitude (m)

Port de Rat (Coma Pedrosa Massif ) Estany d’Estats (Pica d’Estats Massif, Lleida) Salòria Massif (Lleida) Calberante (Mont-Roig Massif, Lleida)

Andorra

AND P

Spain

CAP

Spain

MR

42º 37’ 23.46’’ N 1º 28’ 34.84’’ E 43º 39’ 11.50’’ N 1º 22’ 55.6’’ E 42º 30’ 52.27’’ N 1º 23’ 5.75’’ E 42º 41’ 33.64’’ N 1º 10’ 18.01’’ E

2387

Spain

5 (2 / 3 / 0) 5 (0 / 5 / 0) 4 (2 / 1 / 1) 3 (2 / 1 / 0)

2400 2450 2361

81

BLOOD AND PARASITES IN IBEROLACERTA AURELIOI

All animals were apparently clinically healthy at the time of sampling. Blood samples were collected in the field, with blood extraction in situ and immediate release of the specimens.

Blood smears were prepared using blood obtained from the ventral coccygeal vein, using disposable syringes and 23 gauge needles. Due to the little size of the lizards, only 0.1 ml was taken for cytological assessment.

Differential leucocyte counts were made from blood smears using 1000x magnification lens. A total of 100 leucocytes per slide were examined. The air-dried smears were studied by conventional light microscopy and stained with a commercial wright’s stain (Quick Panoptic®, Química Clínica Aplicada S.A., Amposta, Spain) for differential leucocyte counts and description of erythrocytes, thrombocytes, leucocytes and hemoparasites. Leucocytes were categorized as: heterophils, eosinophils, basophils, azurophils, lymphocytes and monocytes. Presence of cytological disorders (mitosis and parasitologic assessment) was also performed. Blood parasites were detected, and 20 of them were measured using an optical microscope.

Multivariate statistical analysis (correspondence analysis) was performed with the software NCSS 2001 (NCCS LLC, UTAH, USA; HINTzE, 2001). Correspondence analy-

sis (CA) is a very useful exploratory technique for graphically displaying a two-way table by calculating coordinates representing both its rows and columns using Chi-square (thus, nonparametric) distances (GREENACRE, 1993; HINTzE, 2001). Rows in the original matrix were the different samples, and columns were the number (counts) of heterophils, eosinophils, basophils, azurophils, monocytes, lymphocytes, erythrocytes, erythroblasts, mitoses and haemoparasites observed. Comparison between cell counts by sex and localities and correlations between cell types were done using nonparametric approaches (Mann-whitney significance test and Spearman correlation test, respectively; SOKAL & ROHLF, 1969).

RESULTS According to our data, sex had no relation to special blood parameters (Mann-whitney U-test, P > 0.05 in all variables). The haematological differential reference values for the 17 specimens of I. aurelioi analysed are presented in Table 2. Presence of immature forms of erythrocytes (erythroblasts) was detected in 45% of the animals sampled, and mitoses were observed in 11.8% of counted erythrocytes.

Parasites measured between 2.9 to 3.6 mm of

Table 2: Descriptive statistics of the cyto-hematologic reference values and erythrocytes parasitized per microscopic field of the 17 wild-caught I. aurelioi included in this study.

Heterophils Eosinophils Basophils Azurophils Monocytes Lymphocytes Mean Std. Dev(sd) Max Min

40 11,24 56 15

6 7,84 24 0

0 1,33 4 0

9 9,91 28 0

6 6,35 20 0

35 13,48 70 15

Parasitized erythrocytes (%) 5 15,8 7 1

82

MARTĂ?NEZ-SILVESTRE & ARRIBAS

Figure 1: Haemogregarina spp. parasitizing erythrocytes in the lizard I. aurelioi, inducing a displacement in nucleus position and a change in cell shape.

width and 15.3 to 14.6 mm of length (Fig. 1).

These protozoa affected 5% (average) of the cells and had an intracellular location. Affected erythrocytes had the nucleus marginalized and increased cell size, being the parasites identified as belonging to the group of haemogregarines. Cytological identification of the species was concordant with genus Haemogregarina, family Haemogregarinidae (TELFORD, 2009) according to their disposition, aspect, shape and morphology. However, definitive identification via molecular testing or other methods was not performed. Haemoparasites were detected in 50% of the animals analysed, but percentages varied depending on the micropopulation of origin of the host as follows: Pica d'Estats Massif (20%), Andorra (40%), Saloria (50%), and Mont-Roig (100%).

Correspondence analysis was run to explore the relationships among the most determinant factors in the observed inter-sample variability (Fig. 2). In our study the first two axes

represented graphically accounted for 51.23% of the total variability. Relationships among the haematological parameters can be extracted from the axis structure. In detail; the first axis (eigenvalue, E = 0.12) explains 26.8% of total variability, with a high contribution (loadings with higher absolute value) of basophils (-1.65) and mitosis (-1.037), both in the negative part of the bivariate space. The second axis (E = 0.11) explains 24.43% of the total variability, and the most contributing variables were basophils (-1.800) in the negative part and mitosis (1.059) plus haemoparasites (1.009) in the positive part of the bivariate space (Fig. 2).

Several blood parameters appear in the analysis, which are more or less grouped and seem to be correlated among them (monocytes,

Figure 2: Representation of the haematological parameters (triangles) of the I. aurelioi samples studied (circles). Locality codes are provided for each sample (see Table 1 for more details). The oval shows the location of the number of mitoses and the presence of haemoparasites in the CA multivariate space.

BLOOD AND PARASITES IN IBEROLACERTA AURELIOI

lymphocytes, heterophils, azurophils and erythroblasts) with no specific clinical application, but two parameters appear surprisingly related and individualized in the graph: the number of mitoses and the presence of haemoparasites. Although the relationship of these two parameters seems to be accidental, as their pairwise relationship is not significant (Spearman Rank correlation, rs = 0.18, P > 0.05), we find a significant correlation (one tailed test) between the presence of haemoparasites and erythroblasts (rs = 0.44, P < 0.05) and also between the number of mitoses and the number of erythroblasts (rs = 0.6, P < 0.01), both reflected in Fig. 2.

DISCUSSION Our study reveals a significant correlation between the presence of haemoparasites and erythroblasts. Such correlation may be due to the effect of parasitism in the stimulation of blood regeneration, as described in other reptiles (MARTÍNEz-SILVESTRE et al., 2011).

Moreover, correlation between the number of mitoses and the number of erythroblasts might be related to the high mountain environments. In fact, high blood regeneration to compensate lower oxygen pressure is a physiological adaptation to altitude described in several animal groups (MANI, 1968; RIVOLIER et al., 1985). On the other side, the correspondence analysis showed the existence of two cell types that are independent from the others and between them: eosinophils and basophils. This is a usual situation, since there is great variability in these cell types, as seen in other lacertilian reptiles such as Gallotia lizards (MARTÍNEz SILVESTRE et al., 2004). Although eosinophils and basophils increase is associated with para-

83

sitism, this is not the case here. This fact is observed in other studies where the presence of haemoparasites is not related to variations of these kinds of cells, either in tortoises (LAwRENCE & HAwKEY, 1985) or crocodilians (GLASSMAN et al., 1979). As consequence, it should be inferred that haemoprotozoa may not trigger the same immune reaction as other kinds of parasites do.

In the representation of samples based on their haematological parameters, Mont-Roig samples are fairly similar among them, whereas Andorra, Pica d’Estats and Capifonts are more heterogeneous. It is possible that the high degree of parasitization and other possibly linked phenomena such as the large number of mitoses, made the three MontRoig samples appear so close in the analysis.

The joint representation of samples and haematological parameters showed that the Mont-Roig samples are notable particularly in terms of number of mitoses, haemoparasites and erythroblasts. The remaining samples are fairly well correlated with the abovementioned parameters that appear more or less grouped together (monocytes, lymphocytes, heterophils, azurophils and erythroblasts) with values that we can consider as the usual for the species, at the light of our data. These results are not coincident with the ones observed in other Lacertidae studies such as the ones carried out on the giant lizards from Canary Islands (Spain) (genus Gallotia) (MARTÍNEz SILVESTRE et al., 2004). In this genus, higher values of heterophils (33%), basophils (10%) and azurophils (12%) were observed, whereas eosinophils (1.5%), monocytes (1.5%) and lymphocytes (14%) had higher values in I. aurelioi (Table 1).

These differences may be indicative of

84

MARTÍNEZ-SILVESTRE & ARRIBAS

physiological adaptations to different environmental conditions (SACCHI et al., 2011).

Interestingly, mitoses in this species show a relatively higher occurrence in I. aurelioi when compared to other species (SALAKIJ et al., 2002; MARTÍNEz SILVESTRE et al., 2004; STRIK et al., 2007).

Mitosis and regeneration resulting from haematological parasitosis could be related to heterophilia or eosinophilia, since they are also usually associated with parasitosis in reptiles (JACOBSON, 2007). However, in our case, the presence of haemoparasites is not related with eosinophilia in any of our sampled populations. This is in agreement with other studies carried out with haemoparasites in crocodilians (GLASMANN et al., 1979) and tortoises (LAwRENCE et al., 1985). In our study, monocytosis was neither associated with haemoparasitism, contrary to the results obtained in the lizard Ameiva ameiva parasitized with the protozoan Plasmodium (BONADIMAN et al., 2010). Moreover, animals with higher number of erythroblasts also show erythrocytes in mitosis, which although not rare, is neither very common in reptiles.

Finally, the presence of haemoparasites seems to be an important factor in the observed results.

The biological cycle of the parasite causes the destruction of the infected erythrocytes, leading to blood regeneration. This relationship has been shown in several studies (MARTÍNEzSILVESTRE et al., 2011). Erythrocyte regeneration is characterized by a high frequency of young cells in peripheral blood (also confirmed in this study) and an activation of cell regeneration processes in a frequency higher than usual.

The presence of mitoses is not rare in peripheral blood, but, although not significant, such a high number of mitoses as observed in these lizards is

infrequent. In our analysis, the correlation is almost significative and probably it would be with a larger sample size.

Populations of this lizard are not as dense as in other known lacertid species, which may be important from an epidemiological viewpoint.

Maximum densities for the species of 175 and 145 individuals per hectare (ind / ha) were estimated in two successive years in Andorra (Ordino-Arcalís) in particularly favourable sites (ARRIBAS, 2009). During the collection of samples for this study (end of June and early July 2006), densities of 20.8 ind / ha in MontRoig massif, 25.8 ind / ha in Pica d’Estats and 10.27 ind / ha in Salòria (Capifonts) were observed (ARRIBAS, 2006). Theoretically, the more crowded lizards live, the more possibilities have parasites to infest new hosts. In our case, low lizard densities combined with the isolation of the populations in different mountain massifs might have helped to avoid high infestation levels and explain differences among micropopulations. In other words, orography of the habitat of I. aurelioi could represent a true barrier for parasitaemia levels become homogeneously epidemic. we can conclude that parasitized animals have higher erythrocyte regeneration, and hence parasites are probably directly involved in this situation. The most important question to answer is whether the lizards are able to co-evolve and reach equilibrium with the parasite or whether these parasites represent a threat to the conservation of I. aurelioi in the affected mountain micropopulations.

Acknowledgement Blood samples were obtained under permission code SF/102 (2005) from the

BLOOD AND PARASITES IN IBEROLACERTA AURELIOI

Departament de Medi Ambient i Habitatge (Generalitat de Catalunya, Spain). we thank Joaquim Soler for the literature support, and the Departament de Medi Ambient i Habitatge (Generalitat de Catalunya, Spain) and the High Pyrenees Natural Park for providing research permits, funding the study and organising the conservation studies of Iberolacerta aurelioi for the last seventeen years since its discovery.

REFERENCES ARRIBAS, O. (2004). Lacerta aurelioi Arribas, 1994. Lagartija pallaresa, In J.M. Pleguezuelos, R. Márquez & M. Lizana (eds.) Atlas y Libro Rojo de los Anfibios y Reptiles de España, 3rd ed. Dirección General de Conservación de la Naturaleza, Asociación Herpetológica Española, Madrid, Spain, pp. 218-219.

ARRIBAS, O. (2006). Estat de la sargantana pallaresa (Iberolacerta aurelioi) al Parc Natural de L’Alt Pirineu. Anuari Naturalista del Parc Natural de L’Alt Pirineu 1: 54-55.

ARRIBAS, O. (2007). Istòria Naturau e Evolucion dera Cernalha Aranesa, Iberolacerta aranica. Conselh Generau d’Aran, Huesca, Spain.

ARRIBAS, O. (2009). Lagartija pallaresa – Iberolacerta aurelioi, In A. Salvador & A. Marco (eds.) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid, Spain.

Available at: http://www.vertebradosibericos.org/. Retrieved on: 10/10/2012.

BONADIMAN, S.F.; MIRANDA, F.J.; RIBEIRO, M.L.S.; RABELO, G.; LAINSON, R.; SILVA, E.O. & DAMATTA, R.A. (2010).

Hematological parameters of Ameiva amei-

85

va (Reptilia: Teiidae) naturally infected with hemogregarine: Confirmation of monocytosis. Veterinary Parasitology 171: 146-159.

GREENACRE, M.J. (1993). Correspondence Analysis in Practice. Academic Press, San Diego, California, USA. GLASSMAN, A.; HOLBROK, T.w. & BENNETT, C.E. (1979). Correlation of leech infestation and eosinophilia in Alligators.

Journal of Parasitology 65: 323-324.

HERNANDEz-DIVERS, S.; LAFORTUNE, M.; MARTÍNEz-SILVESTRE, A. & PETHER, J. (2003). Assessment and conservation of the giant gomeran lizard (Gallotia bravoana). Veterinary Record 152: 395-399.

HINTzE, J. (2001). NCSS and PASS. Number Cruncher Statistical Systems. Kaysville, Utah, USA. Available at: http://www.NCSS.com.

Retrieved on: 10/10/2012.

JACOBSON, E.R. (2007). Parasites and parasitic diseases of reptiles, In E.R Jacobson (ed.) Infectious Diseases and Pathology of Reptiles: Color Atlas and Text. CRC Press, Boca Raton, Florida, USA, pp. 571-666.

LAwRENCE, K. & HAwKEY, C.M. (1985).

Haemogregarine infection in long term captive Mediterranean tortoises.

Veterinary Record 117: 129-130.

MANI, M.S. (1968). Ecology and Biogeography of High Altitude Insects. Series Entomologica, vol. 4. Dr. w. Junk N.V. Publishers, The Hague, the Netherlands.

MARTÍNEz SILVESTRE, A. (2011). Hematología y Bioquímica Sanguínea en Tres Especies de Lagartos Gigantes de las Islas Canarias (Género Gallotia). Ph.D. dissertation. Universitat Autònoma de Barcelona, Bellaterra, Spain.

MARTÍNEz SILVESTRE, A.; RODRÍGUEz DOMÍNGUEz, M.A.; MATEO, J.A.; PASTOR, J.; MARCO, I.; LAVIN, S. & CUENCA, R. (2004).

86

MARTÍNEZ-SILVESTRE & ARRIBAS

Comparative haematology and blood chemistry of endangered lizards (Gallotia species) in the Canary Islands. Veterinary Record 155: 266-269.

MARTÍNEz-SILVESTRE, A.; MARCO, I.; RODRÍGUEz-DOMÍNGUEz, M.A.; LAVIN, S. & CUENCA, R. (2005). Morphology, cytochemical staining and ultrastructural characteristics of the blood cells of the giant lizard of El Hierro (Gallotia simonyi).

Research in Veterinary Science 78: 127-134.

MARTÍNEz-SILVESTRE, A.; SOLER MASSANA, J.; MATEO MIRAS, J.A.; RODRÍGUEzDOMÍNGUEz, M.A., LAVÍN, S. & CUENCA, R. (2007). Application of hematology on conservation of giant lizards (Genus Gallotia) in the Canary Islands, In Université Cadi Ayyad. Faculté des Sciences, Semlalia. UFR «Biodiversité & Gestion de Patrimoine Naturel». First Mediterranean Herpetological Congress. 16-20 April - 2007. Université Cadi Ayyad, Marrakesh, Morocco, pp. 59-60.

MARTÍNEz-SILVESTRE, A.; LAVÍN, S. & CUENCA, R. (2011). Hematología y citología sanguínea en reptiles. Clínica Veterinaria de Pequeños Animales 31: 131-141.

RIVOLIER, J.; CERRETELLI, P.; FORAY, J. & SEGANTINI, P. (1985). High Altitude Deterioration. Karger Ed., Basel, Switzerland.

SACCHI, R.; SCALI, S.; CAVIRANI, V.; PUPIN, F.; PELLITTERI-ROSA, D. & zUFFI, M.A.L. (2011). Leukocyte differential counts and morphology from twelve European lizards.

Italian Journal of Zoology 78: 418-426.

SALAKIJ, CH.; SALAKIJ, J.; APIBAL, S.; NARKKONG, N.A.; CHANHOME, L. & ROCHANAPAT, N. (2002). Hematology, morphology, cytochemical staining, and ultrastructural characteristics of blood cells in King cobras (Ophiophagus hannah).

Veterinary Clinical Pathology 31: 116-126.

SEVINç, M. & UGURTAS, I.H. (2008).

Comparative erythrocyte size and morphology of some lacertid lizards from Turkey.

Pakistan Journal of Zoology 40: 59-60.

SOKAL, R.R. & ROHLF, J. (1969). Biometry.

The Principles and Practices of Statistics in Biological Research. w.H. Freeman and Co, New York, USA. STRIK, N.L.; ALLEMAN, A.R. & HARR, K.E. (2007). Circulating inflammatory cells, In E.R. Jacobson (ed.) Infectious Diseases and Pathology of Reptiles: Color Atlas and Text. CRC Press, Boca Raton, Florida, USA, pp. 167-218.

TELFORD, S.R. (2009). Hemoparasites of the Reptilia. Color Atlas and Text. CRC Press, Taylor & Francis Group, Boca Raton, Florida, USA.

Basic and Applied Herpetology 28 (2014): 87-97

Teeth number variation and cranial morphology within Vipera aspis group Marco A.L. Zuffi Museum of Natural History and Territory, University of Pisa, Italy.

Correspondence: Museum of Natural History and Territory, University of Pisa, via Roma 79, I-56011 Calci (Pisa), Italy. Phone: +39 0502212967, Fax: +39 0502212975; E-mail: marcoz@museo.unipi.it

Received: 18 March 2012; received in revised form: 23 November 2012; accepted: 1 February 2013.

The huge morphological variability of asp viper (Vipera aspis) snakes has been longly addressed and studied to solve systematic and phylogeographic questions, with emphasis mainly to external morphology, distributive patterns and genome analyses. Teeth number and skull size variation are presently considered in order to contribute to the definition of the morphological puzzle that characterise the asp viper, comparing these structures among age classes and subspecies. The results indicated that, on the whole, 1) teeth number did not vary between sexes, 2) right palatine, total palatine and right dental teeth number varied among taxa and 3) skull length was markedly dimorphic. These differences apparently are congruent to taxonomic position and published phylogeographic patterns.

Key words: Anatomical features; teeth count; Vipera aspis subspecies; western Europe.

Variación en el número de dientes y morfología craniana del grupo Vipera aspis. La gran variabilidad morfológica de la víbora aspid (Vipera aspis) ha sido investigada extensamente en el pasado para resolver problemas de sistemática y filogeografía, con especial énfasis en la morfología externa, patrones de distribución y análisis genéticos. Este estudio analiza la variación existente en el número de dientes y el tamaño del cráneo entre sexos y subespecies con el objetivo de contribuir a la resolución del rompecabezas morfológico existente en esta especie. Los resultados indican que, de modo general, 1) el número de dientes no varía entre sexos, 2) el número de dientes del palatino derecho, el número total de dientes palatinos y el número de dientes en la parte derecha del cráneo varía entre taxones, 3) la longitud del cráneo es marcadamente dimórfica. Nuestros resultados están en concordancia con la posición taxonómica y los patrones filogeográficos estudiados en esta especie.

Key words: número de dientes; oeste de Europa; rasgos anatómicos; subespecies de Vipera aspis.

Snake skulls represent unique features among vertebrate taxa, showing an impressive variability in both shape and size. Skull shape, more than size, has been used to describe taxonomic ranks, contributing to the systematics of the group (KRAMER, 1980; GLOYD & CONANT, 1990; LEE & SCANLON, 2002). However, bones allometries are furthermore suitable for this purpose. Static and dynamic relationship of skull bones, movement of articulations or number of mobile and fixed bones among DOI: http://dx.doi.org/10.11160/bah.12002/

extant and extinct species have contributed to actual phylogeny (LEE & SCANLON, 2002). At this respect, for example, the presence of a markedly reduced, mobile, maxilla with elongated fangs discriminate the Viperidae family from all the other serpents.

Skulls, on the other hand, have been studied for analysis of the kinematic of prey swallowing or when inspecting relationships between trophic resources and mouth opening in unrelated taxa (ROSS et al., 2010).

88

ZUFFI

Furthermore, skull morphology and kinematics have been informative of adaptive functions in Lepidosauria (METzGER, 2002).

Despite its determinant value in phylogeny and systematics (CUNDALL, 1981; LEE & SCANLON, 2002), analytical data on snake skull morphology are relatively scarce: frequently snake skulls are simply figured, presented as drawings or pictures (BOULENGER, 1913; KRAMER, 1980; BOUGHNER et al., 2007; see also a general overview on http://en.wikipedia.org/wiki/Snake_skeleton), being rarely described in detail except when describing a species or when comparing different or related species (SCHäTTI, 1988; GLOYD & CONANT, 1990; LEE & SCANLON, 2002). Skull morphology is considered a conservative and little variable anatomical character that shows appreciable differences usually between distinct, unrelated genera and, less frequently, in closely related species (JOGER et al., 1997). In general, bones constituting dorsal, lateral and ventral skull parts (i.e. parietal, basisphenoid) may differ in size and shape (i.e. interspecific differences, GENTILLI et al., 2009), or may display relative allometric development (i.e. shorter premaxillary bones and longer maxillary bone) during ontogenesis (zUFFI et al., 2011) or between sexes (VINCENT et al., 2004). More specifically, the distal skull portion (i.e. the neurocranium) is the less variable structure of the head (SCHäTTI, 1988; GENTILLI et al., 2009), while the proximal portion (i.e. the splancnocranium), on the contrary, is more susceptible to shape variability, due to functional demands related to dietary habits, as some studies demonstrate in several taxa (e.g. bats: VAN CAKENBERGHE et al., 2002; lizards: METzGER & HERREL, 2005; snakes:

VINCENT et al., 2004). Integrative approaches including shape analysis or other characters such as scale patterns might provide insights of sexual dimorphism, taxonomic characteristics or functional structures (KALIONTzOPOULOU et al., 2007; GENTILLI et al., 2009; ADAMS & NISTRI, 2010).

Moreover, the inspection of skull anatomical and kinematic features could reveal hidden or unexpected phenomena (e.g. jaw closing inlever, HERREL et al., 2010). In the Viperidae, and especially in the European vipers, one of the most studied groups of snakes in the world, information on head skeletal features is still scarce (KRAMER, 1980; GENTILLI et al., 2009). while on one side, a wide and rich literature does exist on the evolution, function and structure of fangs (see KARDONG, 1982; GREENE & FOGDEN, 2000; JACKSON, 2003, among others), on the other side other teeth have received almost none or very little attention. Despite the fact that they do not show either particular adaptive meaning or special morphological differentiation, number of teeth could be relevant for systematic and taxonomic purposes.

The asp viper, Vipera aspis (L., 1758), is divided into four subspecies morphologically distinct, with allopatric distribution (Fig. 1; zUFFI & BONNET, 1998; zUFFI, 2002; GOLAY et al., 2008), whose anatomical characteristics are not well studied (KRAMER, 1980; zUFFI 2002), resulting in a partially unresolved taxonomy (URSENBACHER et al., 2006; GOLAY et al., 2008; BARBANERA et al., 2009; MASSETI & zUFFI, 2011).

This paper aims at describing the range variation in the number of non maxillary teeth among Vipera aspis subspecies and of some other Vipera species in order to:

TEETH AND SKULL IN VIPERA ASPIS

89

Figure 1: Vipera aspis ssp distribution.

1) verify sexual dimorphism variation in skull size and 2) assess any geographical pattern in teeth numbers, as a contribution to the overall knowledge of V. aspis.

MATERIALS AND METHODS Teeth count and cranial morphology Skulls of the “Enrica Calabresi” historical collection at the zoological Museum “La Specola”, University of Florence were examined.

These specimens were described and three of them were also figured by Calabresi (see table IV in CALABRESI, 1924). Unfortunately in her paper, Calabresi (1924) was not able to discriminate to variation in teeth number and position, despite she reported variability for this parameter. For this study, I considered 55 specimens (Vipera aspis aspis N = 6; V. a. francisciredi N = 24; V. a. hugyi N = 22; V. berus berus N = 3; Appendix 1). Other skulls with incomplete information on sex or locality were discarded. For purely descriptive purposes, drawings of dorsal and ventral views of complete skulls are presented in Fig. 2. Teeth number was established considering the niche of each tooth along left (L) and right

(R) palatines, L and R pterygoids, and L and R dentals (Fig. 3). I also considered the total number of teeth pairing left and right niches of each bone, and the total number of teeth of palatine plus pterygoid bones. Count was performed under stereomicroscope at 6x magnification. Since some crania were incomplete, teeth niches counting was not possible in all cases, showing variation in sample size. I also

Figure 2: Dorsal (above) and ventral (below) view of V. aspis subspecies skulls. (A) V. a. aspis ♂, Monte Rosa, Piedmont, Nw Italy, MzUF C315; (B) V. a. francisciredi ♂, Udine, Friuli Venezia Giulia, NE Italy, MzUF C395; (C) V. a. hugyi ♀, Mongiana, Calabria, S Italy, MzUF C287 (taken from the Calabresi collection, zoology Museum, University of Florence; original drawings of the author).

90

ZUFFI

Figure 3: Ventral view of V. a. aspis skull (Calabresi collection, catalogue number C315, MzUF). Main dentary bones are shown with arrows.

measured overall length of Calabresiâ&#x20AC;&#x2122;s skulls and of additional 16 skulls preserved in the Natural History Museum, University of Pisa, including three V. a. aspis; five V. a. francisciredi; two V. a. hugyi; one V. a. zinnikeri; one V. ammodytes; one V. berus; and three V. a. francisciredi x hugyi hybrids (see Appendix 1 for more details). Overall length was measured as the distance from the midline of frontals to the rear margin of the basioccipital bone (Fig. 4).

For all available localities I also retrieved geographic coordinates (longitude and latitude), to perform further analyses on geographical variation.

ne teeth (z = 1.403, P = 0.039 and z = 1.677, P = 0.0007 respectively) and in the L pterygoid teeth (z = 1.494, P = 0.023). Parametric tests were used in the case of normally distributed variables, while the rest of the variables were analysed using non parametric statistics.

The analyses that considered all variables together were carried out with non parametric tests. Non parametric bivariate correlations (Spearman r) were performed on all teeth variables (L and R palatines, L and R pterygoids, L and R dentals, total number of palatine teeth, total number of pterygoid teeth and total number of dental teeth; Table 1) and head length in order to test for any correlation. Kruskal-wallis test was run on the total number of teeth per bone, with subspecies as factor. I performed a Hierarchical cluster analysis, with Agglomerative approach (each observation starts in its own cluster, and pairs of clusters are merged as one moves up the hierarchy) with Average Linkage (between groups) in order to classify any homogeneous group (taxa and area); furthermore, with free R statistical package (R DEVELOPMENT CORE TEAM, 2011), I run a Mantel test statistic based on Pearson's product-moment correlation [Call: mantel (xdis = MM.dist, ydis = MD.dist), where

Statistical analyses Data were checked for normality (Kolmogorov-Smirnov test). Total number of palatine teeth, total number of pterygoid teeth, total number of dental teeth and total number (palatine + pterygoid) of teeth were normally distributed. All these parameters were also homogeneous (Levene test, all P > 0.05).

Distribution was not normal in L and R palati-

Figure 4: Dorsal view of V. a. francisciredi skull, showing skull length measurement (Calabresi collection, catalogue number C399, MzUF).

91

TEETH AND SKULL IN VIPERA ASPIS

Table 1: Average value, standard deviation and sample size (in parenthesis) of the number of teeth for each V. aspis subspecies and sex. L = left; R = right.

Palatine L Males V. a. aspis V. a. francisciredi V. a,. hugyi V. a. berus Females V. a. aspis V. a. francisciredi V. a. hugyi V. a. berus

R

Pterygoid Total

L

R

Dental Total

L

R

Total

4 ± 0.01 (3) 4 ± 0.02 (2) 8 ± 0.03 (2) 3 ± 0.8 (11) 2.8 ± 0.7 (11) 5.9 ± 1.4 (10) 2.7 ± 0.7 (10) 2.9 ± 0.4 (8) 5.7 ± 1.1 (6) 4 (1) 4 (1) 8 (1)

12.7 ± 0.6 (3) 12 ± 1.4 (2) 24.5 ± 2.1 (2) 10.8 ± 2.6 (11) 10.6 ± 2.4 (12) 21.3 ± 5 (11) 11.8 ± 1.5 (10) 12.1 ± 1.2 (9) 24.6 ± 2.6 (7) 12 (1) 11 (1) 23 (1)

15.7 ± 0.6 (3) 14.5 ± 0.7 (2) 30 ± 0.02 (2) 13.7 ± 1.8 (9) 14.4 ± 0.9 (8) 28.5 ± 1.4 (6) 15.3 ± 1.1 (9) 15.1 ± 0.9 (11) 30.4 ± 2 (8) 16 (1) 16 (1) 32 (1)

3 (1) 4 ± 0.1 (2) 7 (1) 2.6 ± 0.5 (7) 2.6 ± 0.5 (9) 5.1 ± 0.9 (7) 2.6 ± 0.8 (7) 2.8 ± 0.9 (8) 5.1 ± 1.6 (7) 4 (1) 5 (1) 9 (1)

11 (1) 11.5 ± 0.7 (2) 23 (1) 10.6 ± 1.4 (9) 10.6 ± 1.7 (9) 21.1 ± 2.8 (9) 11.6 ± 0.8 (7) 11.1 ± 1.4 (8) 22.7 ± 2 (7) 13 (1) 13 (1) 26 (1)

-14.5 ± 2.1 (2) -14.7 ± 2 (8) 13.7 ± 1.1 (8) 28.5 ± 2.7 (8) 14.8 ± 1.8 (5) 15 ± 0.6 (7) 30.2 ± 1.7 (4) 15 (1) 14 (1) 29 (1)

MM is the morphometric matrix (average data of teeth number), as Euclidean distance, and MD is the geographic matrix (distance in kilometres between pairs of localities)].

Probability was set at a = 0.05, and statistical analyses were performed with SPSS 13.0 release 2005 for windows (SPSS Inc., Chicago, Illinois, USA) and R, version 2.15.2 (©R Foundation for Statistical Computing, Vienna, Austria).

RESULTS Descriptive statistics regarding the number of teeth per bony section for each subspecies are detailed in Table 1.

Spearman correlation was positively significant between all pairs of splacnocranium teeth, while only total pterygoid teeth and total palatine+total pterygoid teeth correlated to right dental teeth (N = 35, r = 0.408, P = 0.015 and N = 32, r = 0.361, P = 0.042 respectively); head length correlated only slightly with L palatine teeth (N = 46, r = -0.290, P = 0.05) and negatively with palatine+pterygoid teeth (N = 40, r = -0.341,

P = 0.032). All other correlations were not significant. Kruskal-wallis test was significant only with taxon effect on L palatine (z = 13.156, d.f. = 3, P = 0.004), R palatine (z = 19.005, d.f. = 3, P < 0.0001), and R dental teeth (z = 9.815, d.f. = 3, P = 0.02).

Relationship between number of teeth and skull length (preserved skulls), compared between sexes, age classes and taxa, showed that sexual dimorphism is absent at teeth level, that palatine teeth number varied among taxa and that there was a marked sexual difference in skull length.

Hierarchical cluster showed a first cluster of southern asp vipers (V. a. hugyi), and a second large cluster with two subclusters: central and northeastern asp vipers (V. a. francisciredi) plus northwestern asp vipers (V. a. aspis-V. a. atra) (Fig. 5). Regarding the spatial correlation between geographic distance and the number of teeth of each taxa, the Mantel test did not find correlation between the average teeth number and the geographic distance (Mantel statistic r = -0.155, P = 0.964, based on 999 permutations, after standardization).

92

ZUFFI

DISCUSSION CALABRESI (1924) experimented the modern idea of comparing external and internal anatomy in order to solve taxonomical matters, and in addition to scalation and colour analyses, she extracted skulls from specimens preserved in liquid. She found differences among northern and northeastern Italy plus central Italy vs. northwestern Italy asp vipers (now V. a. francisciredi vs V. a. aspis respectively, as forma I vs. forma II), but especially she found a clear differentiation between these two subspecies and the one in the southern part of Italy V.a. hugyi (forma III) (CALABRESI, 1924: pp. 118119). KRAMER (1980) had difficulties in separating V. a. atra (now V. a. aspis) from V. a. hugyi, even if he used potentially suitable ratios derived from osteological measures (KRAMER, 1980: pp. 5-6). As declared

(KRAMER, 1980: p. 5, table and description of V. a. atra distribution), specimens from northeastern (V. a. aspis) and southern Apennines (V. a. hugyi) were considered together, therefore introducing a strong bias in his analyses and preventing any firm conclusion.

On the contrary, GENTILLI et al. (2009), using dorsal and ventral skull shapes, showed that the highest divergence was between V. a. aspis vs V. a. francisciredi-V. a. hugyi, and a secondary, less marked, divergence between V. a. francisciredi and V. a. hugyi. Sexual differences were not considered (CALABRESI, 1924; KRAMER, 1980) or were found negligible (GENTILLI et al., 2009).

In all these papers, however, relatively low or no attention at all was paid to teeth. Teeth in snakes have frequently been used in anatomical studies (see for instance HANDRIGAN & RICHMAN, 2011) as a tool that discriminates, throughout the evolution of snakes, between

Figure 5: Hierarchical cluster analysis on teeth number and taxa in Vipera aspis.

93

TEETH AND SKULL IN VIPERA ASPIS

venomous and harmless snakes (KARDONG, 1982). The use of snakes’ teeth in palaeontology is quite rare (but see SzYNDLAR, 1991) despite it has been proved to be extremely useful (GONG et al., 2010). However, recently, differential teeth morphology in a very specialized species has been described being associated with different dietary habits (JACKSON & FRITTS, 2004). Vipera aspis subspecies have a similar trophic spectrum, and no sexual differences have been reported in the diet across all the distribution area (see LUISELLI & AGRIMI, 1991; SAVIOzzI & zUFFI, 1997). This suggests that differences observed in this study in teeth number are due to selective pressures other than diet.

Interestingly, different teeth number (e.g. palatine and dental teeth) was related to taxonomic assignment (Hierarchical Cluster Analysis, Fig. 4) and not to the geographic distribution itself. In fact, the Mantel test did not support any spatial correlation between geographic distance and the number of teeth.

These results support previous papers (POzIO, 1980; zUFFI, 2002; BARBANERA et al., 2009; GENTILLI et al., 2009) confirming differences in the number of teeth at taxonomical level. The role and meaning of all these dentary features should be carefully investigated in future studies to understand what selective forces are responsible for these differences, and to properly address the asp viper systematic position (see zUFFI, 2002).

Acknowledgement Annamaria Nistri (La Specola Museum, University of Florence) allowed access to the Enrica Calabresi skull collection. Roberto Sacchi (University of Pavia) helped in run-

ning Mantel test with R package. Suggestions and criticisms of two anonymous reviewers and those of Ana Perera highly improved a previous version of this ms.

REFERENCES ADAMS, D.C. & NISTRI, A. (2010).

Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae).

BMC Evolutionary Biology 10: 216.

BARBANERA, F.; zUFFI, M.A.L.; GUERRINI, M.; GENTILLI, A.; TOFANELLI, S.; FASOLA, M. & DINI, F. (2009). Phylogeography of the Italian asp viper (Vipera aspis) as inferred from mitochondrial and microsatellite DNA data. Molecular Phylogenetics and Evolution 52: 103-114.

BOUGHNER, J.C.; BUCHTOVA, M.; FU, K., DIEwERT, V., HALLGRÍMSSON, B. & RICHMAN, J.M. (2007). Embryonic development of Python sebae – I: Staging criteria and macroscopic skeletal morphogenesis of the head and limbs. Zoology 110: 212-230.

BOULENGER, G.A. (1913). The snakes of Europe. 2nd ed. Methuen & Co., Ltd., London, UK. CALABRESI, E. (1924). Ricerche sulle variazioni della Vipera aspis Auct. in Italia.

Bollettino dell’Istituto di Zoologia della Regia Università di Roma 2: 78-127.

CUNDALL, D. (1981). Cranial osteology of the Colubrid snake genus Opheodrys.

Copeia 1981: 353-371.

GENTILLI, A.; CARDINI, A.; FONTANETO, D. & zUFFI, M.A.L. (2009). The phylogenetic signal in cranial morphology of Vipera aspis: a contribution from geometric morphometrics. The Herpetological Journal 19: 69-77.

94

ZUFFI

GLOYD, H.K. & CONANT, R. (1990). Snakes of the Agkistrodon complex: a monographic review. SSAR, St. Louis, Missouri, USA. GOLAY, P.; MONNEY, J.-C.; CONELLI, A.; DURAND, T.; THIERY, G.; zUFFI, M.A.L. & URSENBACHER, S. (2008). Systematics of the Swiss asp vipers: some implications for the European Vipera aspis (Linnaeus, 1758) complex (Serpentes: Viperidae) – A tribute to Eugen Kramer. AmphibiaReptilia 29: 71-83.

GONG, E.; MARTIN, L.M.; BURNHAM, D.A. & FALK, A.R. (2010). The birdlike raptor Sinornithosaurus was venomous.

Proceedings of the National Academy of Sciences 107: 766-768.

GREENE, H.w. & FOGDEN, M. (2000).

Snakes: the Evolution of Mystery in Nature.

University of California Press, Los Angeles, California, USA. HANDRIGAN G.R. & RICHMAN J.M. (2011).

Unicuspid and bicuspid tooth crown formation in Squamates. Journal of Experimental Zoology B 316: 598-608.

H ERREL , A.; M OORE , J.A.; B REDEwEG , E.M. & NELSON, N.J. (2010). Sexual dimorphism, body size, bite force and male mating success in tuatara.

Biological Journal of the Linnean Society 100: 287-292.

KALIONTzOPOULOU, A.; CARRETERO, M.A. & LLORENTE, G.A. (2007). Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis lizards. Journal of Morphology 268: 152-165.

KARDONG, K.V. (1982). The evolution of the venom apparatus in snakes from colubrids to viperids and elapids. Memórias do Instituto Butantan 46: 105-118.

KRAMER, E. (1980). zum skelett der Aspisviper, Vipera aspis (Linnaeus, 1758).

Revue Suisse de Zoologie 87: 3-16.

JACKSON, K. (2003). The evolution of venom‐delivery systems in snakes.

Zoological Journal of the Linnean Society 137: 337-354.

JACKSON, K. & FRITTS, T.H. (2004).

Dentitional specialisations for durophagy in the Common wolf snake, Lycodon aulicus capucinus. Amphibia-Reptilia 25: 247254.

Joger, U.; Lenk, P.; Baran, I.; Böhme, w.; ziegler, T.; Heidrich, P. & wink, M. (1997). The phylogenetic position of Vipera barani and V. nikolskii within the Vipera berus complex, In w. Böhme, w. Bischoff & T. ziegler (eds.) Herpetologia Bonnensis.

Societas Europaea Herpetologica, Bonn, Germany, pp. 185-194.

LEE, M.S.Y. & SCANLON, J.D. (2002). Snake phylogeny based on osteology, soft anatomy and ecology. Biological Reviews 77: 333-401.

LUISELLI, L. & AGRIMI, U. (1991).

Composition and variation of the diet of Vipera aspis francisciredi in relation to age and reproductive stage. Amphibia–Reptilia 12: 137-144.

MASSETI, M. & zUFFI, M.A.L. (2011). On the origin of the asp viper Vipera aspis hugyi Schinz, 1833, on the island of Montecristo, Northern Tyrrhenian Sea (Tuscan archipelago, Italy). Herpetological Bulletin 117: 1-9.

METzGER, K. (2002). Cranial kinesis in Lepidosaurs: skulls in motion, In P. Aerts, K. D’Août, A. Herrel & R. Van Damme (eds.) Topics in Functional and Ecological Vertebrate Morphology. Shaker Publishing, Maastricht, Netherlands, pp. 15-46.

TEETH AND SKULL IN VIPERA ASPIS

METzGER, K. & HERREL, A. (2005).

Correlations between lizard cranial shape and diet: a quantitative, phylogenetically informed analysis. Biological Journal of the Linnean Society 86: 433-466.

POzIO, E. (1980). Contributo alla sistematica di Vipera aspis (L.) mediante analisi elettroforetica delle proteine contenute nel veleno. Natura 71: 28-34.

R DEVELOPMENT CORE TEAM (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.

ROSS, C.F.; BADEN, A.L.; GEORGI, J.; HERREL, A.; METzGER, K.A.; REED, D.A., SCHAERLAEKEN, V. & wOLFF, M.S. (2010). Chewing variation in lepidosaurs and primates. Journal of Experimental Biology 213: 572-584.

SAVIOzzI, P. & zUFFI, M.A.L. (1997). An integrated approach to the study of the diet of Vipera aspis. Herpetological Review 28: 23-24.

SCHäTTI, B. (1988). Systematik und Evolution der Schlangengattung Hierophis Fitzinger 1843 (Reptilia, Serpentes). Ph.D. Dissertation, University of zurich, zurich, Switzerland.

SzYNDLAR, z. (1991). A review of Neogene and Quaternary snakes of central and eastern Europe. Part 11: Natricinae, Elapidae, Viperidae. Estudios geologicos 47: 237-266.

URSENBACHER, S., CONELLI, A., GOLAY, P., MONNEY, J.-C., zUFFI, M.A.L., THIERRY, G., DURAND, T. & FUMAGALLI, L. (2006).

Phylogeography of the asp viper (Vipera

95

aspis) inferred from mitochondrial DNA sequence data: evidence for multiple Mediterranean refuges.

Molecular Phylogenetics and Evolution 38: 546-552.

VAN CAKENBERGHE, V.; HERREL, A. & AGUIRRE, L.F. (2002). Evolutionary relationships between cranial shape and diet in bats (Mammalia: Chiroptera), In P. Aerts, K. D’Août, A. Herrel & R. Van Damme (eds.) Topics in Functional and Ecological Vertebrate Morphology. Shaker Publishing, Maastricht, Netherlands, pp. 205-236.

VINCENT, S.E.; HERREL, A. & IRSCHICK, D.J. (2004). Ontogeny of intersexual head shape and prey selection in the pitviper Agkistrodon piscivorus. Biological Journal of the Linnean Society 81: 151-159. zUFFI, M.A.L. (2002). A critique of the systematic position of the asp viper subspecies Vipera aspis aspis (Linnaeus, 1758), Vipera aspis atra Meisner, 1820, Vipera aspis francisciredi Laurenti, 1768, Vipera aspis hugyi Schinz, 1833 and Vipera aspis zinnikeri Kramer, 1958. AmphibiaReptilia 23: 191-213. zUFFI, M.A.L. & BONNET, X. (1999). Italian subspecies of the asp viper, Vipera aspis: patterns of variability and distribution.

Italian Journal of Zoology 66: 87-95. zUFFI, M.A.L.; SACCHI, R.; PUPIN, F. & CENCETTI, T. (2011). Sexual size and shape dimorphism in the Moorish gecko (Tarentola mauritanica, Gekkota, Phyllodactylidae). North-Western Journal of Zoology 7: 189-197.

96

ZUFFI

Appendix 1: Specimens examined in this study. No = museum catalog number. Hybrids determined as in GENTILLI et al. (2009).

No

Taxon

Sex

Locality

Museum

T65 F37 1188 741 741/3 170 170 688 1169 1187 1168 1186 701 1170 1171 1172 C490 C132 C87 C315 C315 C626 C96

V. a. aspis V. a. aspis V. a. aspis V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. hugyi V. a. hugyi V. a. zinnikeri V. ammodytes V. berus hybrid franc x hugyi hybrid franc x hugyi hybrid franc x hugyi V. a. aspis V. a. aspis V. a. aspis V. a. aspis V. a. aspis V. a. aspis V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. francisciredi

male female male male male male female male male female male female female male male male male female juvenile male female male male female female male male male male male female male female female juvenile male male male female female female female male

Chizè, Deux Sevres, Nw France Chizè, Deux Sevres, Nw France Gressoney La Trinitè, Nw Italy Arnino, Pisa, C Italy Arnino, Pisa, C Italy Torretta, Pavia, N Italy Torretta, Pavia, N Italy S.Quirino, Lucca, C Italy Torre del Loto, Taranto, S Italy Montecristo Is., C Italy Albeva, Catalonia, Spain Krk Is., Croatia Verona surroundings, N Italy S. Anastasia, Naples, S Italy Clanio valley, Avellino, S Italy Clanio valley, Avellino, S Italy Riva Valdobbia, Novara, Nw Italy Alpi d'Ossola, Novara, Nw Italy Calasca, Novara, Nw Italy Mount Rosa, Nw Italy Mount Rosa, Nw Italy Lanzo valleys, Turin, Nw Italy Sestaione, Pistoia, C Italy Poggio Riparghera, Florence, C Italy Vallombrosa, Florence, C Italy Radda Chianti, Florence, C Italy S. Croce Avellana, Florence, C Italy Treviso, NE Italy Udine, NE Italy Udine, NE Italy Udine, NE Italy Sestaione, C Italy Udine , NE Italy Udine, NE Italy Udine, NE Italy Cergnago, Pavia, Nw Italy Cergnago, Pavia, Nw Italy Cergnago, Pavia, Nw Italy Cergnago, Pavia, Nw Italy Cergnago, Pavia, Nw Italy Cergnago, Pavia, Nw Italy Alpi Apuane, C Italy Bagni di Lucca, Lucca, C Italy

Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Pisa Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence

C697 C699 C583 C139 C399 C399 C399 C96 C399 C399 C399 C312 C312 C312 C312 C312 C312 C60 C95

TEETH AND SKULL IN VIPERA ASPIS

97

Appendix 1 (cont.)

No

Taxon

Sex

Locality

Museum

C95

V. a. francisciredi V. a. francisciredi V. a. francisciredi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. a. hugyi V. berus V. berus V. berus

female male female male female male male juvenile male male male male male male female female female female female male juvenile male male female female male juvenile female

Bagni di Lucca, Lucca, C Italy S Rossore, Pisa, C Italy S Rossore, Pisa, C Italy Neto, Crotone, S Italy Neto, Crotone, S Italy Simmeri, Catanzaro, S Italy Simmeri, Catanzaro, S Italy Simmeri, Catanzaro, S Italy Serra S. Bruno, Catanzaro, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Serra S. Bruno, Vibo Valenzia, S Italy Mongiana, Vibo Valenzia, S Italy Palermo, Sicily Catania, Sicily Montecristo Is., C Italy Montecristo Is., C Italy Montecristo Is., C Italy Montecristo Is., C Italy Morbegno, Sondrio, N Italy Is. Ariano, Ferrara, NE Italy Is. Ariano, Ferrara, NE Italy

Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence Florence

C573 C573 C580 C580 C580 C620 C620 C620 C620 C620 C541 C620 C541 C620 C620 C287 C640 C317 C199 C199 C199 C199 C414 C530 C530

98

Basic and Applied Herpetology 28 (2014): 99-111

Atlas of the distribution of reptiles in the Parc National du Banc d’Arguin, Mauritania Andack Saad Sow1, Fernando Martínez-Freiría2, Pierre-André Crochet3, Philippe Geniez4, Ivan Ineich5, Hamidou Dieng6, Soumia Fahd1, José Carlos Brito2,* Département de Biologie, Faculté des Sciences de Tétouan, Université Abdelmalek Essaâdi, Tétouan, Morocco.

CIBIO/InBio, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Vairão, Portugal.

3 CNRS-UMR 5175, Centre d’Ecologie Fonctionnelle et Evolutive, Montpellier, France.

4 EPHE-UMR 5175, Centre d’Ecologie Fonctionnelle et Evolutive, Montpellier, France.

5 Muséum national d’Histoire naturelle, Département Systématique et Evolution (Reptiles), UMR CNRS 7205 (OSEB), Paris, France.

6 Faculté des Sciences et Techniques, Université des Sciences, de Technologie et de Médecine de Nouakchott, Nouakchott. R.I. Mauritanie.

1 2

* Correspondence: Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661 Vairão, Portugal. Phone: +351 252660416, Fax: +351 252661780, E-mail: jcbrito@cibio.up.pt

Received: 17 December 2012; received in revised form: 19 April 2013; accepted: 19 April 2013.

This study provides the first atlas of the distribution of reptiles in the Parc National du Banc d’Arguin, Mauritania.

The area is a UNESCO world Heritage Site and a Nature Reserve. Unpublished fieldwork observations collected between 2008 and 2011 were combined with published records and museum data in a Geographical Information System to produce maps with the distribution of individual species and species richness. The taxonomic list of reptiles includes 21 species grouped in eight families. Three species (Stenodactylus mauritanicus, Mesalina pasteuri and Psammophis sibilans) were detected for the first time in the area. Reptiles form distinct groups according to their distribution patterns and preliminary habitat selection trends: 1) species selecting bare areas present throughout the park; 2) species selecting rocky habitats present mostly in the northern areas; and 3) species selecting sandy habitats present mostly in the southern areas. A total of eight areas were identified as of high species richness (N > 8 species), usually presenting species typical of rocky or dune habitats and also species present in open bare areas.

Key words: Africa; biodiversity; GIS; protected area; Sahara desert.

Atlas de distribución de los reptiles del Parque Nacional Banc d’Arguin, Mauritania. El presente estudio constituye el primer atlas de distribución de reptiles en el Parque Nacional Banc d’Arguin, Mauritania. El área es una Reserva Natural y está declarada Patrimonio de la Humidad por la UNESCO. Combinamos en un Sistema de Información Geográfica observaciones no publicadas obtenidas durante campañas de campo entre 2008 y 2011 con registros publicados y datos procedentes de museos para elaborar mapas de distribución de cada especie así como de la riqueza de especies. La lista taxonómica de reptiles incluye 21 especies agrupadas en ocho familias. Tres especies (Stenodactylus mauritanicus, Mesalina pasteuri y Psammophis sibilans) se detectaron por primera vez en el área. Los reptiles forman grupos distintos de acuerdo a sus patrones de distribución y a las tendencias preliminares de selección del hábitat: 1) especies que seleccionan áreas yermas distribuidas a lo largo del Parque, 2) especies que seleccionan hábitats rocosos presentes mayoritariamente en la zona norte, y 3) especies que seleccionan áreas arenosas presentes mayoritariamente en la zona sur. Se identificaron un total de ocho áreas de elevada riqueza específica (N > 8 especies) que habitualmente presentan especies típicas de hábitats rocosos y dunares, pero también especies presentes en áreas abiertas y sin vegetación.

Key words: áfrica; área protegida; biodiversidad; desierto del Sáhara; SIG. DOI: http://dx.doi.org/10.11160/bah.12011/

100

SOW ET AL.

Global biodiversity is being lost at an accelerated rate (BUTCHART et al., 2010), as a consequence of human induced factors such as habitat loss and fragmentation, biological invasions and climate change (BROOKS et al., 2002; GARCIA et al., 2012). Knowledge on the distribution patterns of species and the identification of areas holding high richness are necessary steps for developing coherent conservation policies (MYERS et al., 2000; HOBOHM, 2003; HOLE et al., 2011).

Biogeographic transition zones constitute attractive areas for long-term conservation of biodiversity. As they assemble communities of species at the border of their requirements, they allow conserving evolutionary processes (SPECTOR, 2002; CARVALHO et al., 2011) and meeting goals of representativeness and complementarity in protected-areas systems (ARAúJO, 2002; KATI et al., 2004).

Mauritania is located along the transition zone between the Palearctic and AfroTropical biogeographical regions and combines species of Saharan-Sindian and Sahelian affinities (DEKEYSER & VILLIERS, 1956; LE BERRE, 1989). within Mauritania, the coastal Parc National du Banc d’Arguin (PNBA) was declared as a UNESCO world Heritage Site and as a Nature Reserve to mainly protect natural resources, having exceptionally high importance as breeding, staging and wintering area for birds (MAHé, 1985).

However, a varied community of reptiles should be present in the PNBA due to its character of transition zone and its proximity to the Ocean (MONOD, 1988).

Knowledge on reptile species of PNBA is limited but it has been progressively increasing. Until the late 1980s, eight species of reptiles were known (LE BERRE, 1989), and

that number was increased to 19 species with the inventories made during the project “Environment et littoral mauritanien” (INEICH, 1997). Posterior works have allowed detailing distributional patterns for particular species (PADIAL et al., 2002; BRITO, 2003; CROCHET et al., 2003). Specifically, morphological analyses of the Acanthodactylus scutellatus group defined preliminary ranges of individual species and identified specimens with intermediate morphological traits between A. dumerili and A. senegalensis, suggesting the occurrence of interspecific gene flow.

The major aims of this work are to provide an updated taxonomic list of the reptiles present in the PNBA, to map their distributions, and to identify areas of species richness.

MATERIALS AND METHODS Study area The PNBA covers an area of about 120 000 km (latitudes 19°21’ to 21°51’ N and longitudes 16°00’ to 16°45’ w) and is located along the coastal Atlantic region of Mauritania, west Africa (Fig. 1). The PNBA comprises both terrestrial (48% of its area) and marine portions (52%) and there are eight islands and islets, the largest of which is Tidra, with a maximum length and width of 30 km and 10 km, respectively. The continental part includes also the small Cap Blanc Satellite Reserve, especially dedicated to the protection of monk seal (Monachus monachus) colonies. The PNBA is located in the Sahara terrestrial ecosystem, at the southern limit of the Palearctic realm. The area is mostly flat (maximum altitude 61 m) and there are two main rock outcrops located in the northern (Kerekchet et Teintâne) and 2

REPTILES OF THE PARC NATIONAL DU BANC D’ARGUIN

central (Dlô Amotai) areas. The climate is arid and hot, with annual precipitation and annual average temperature ranging between 17 and 50 mm and 21.8 and 25.2ºC, respectively (HIJMANS et al., 2005). The most representative land-cover categories are bare areas (40.1%), consolidated bare areas (hardpans, gravels, bare rock, stones, boulders; 37.9%) and non-consolidated bare areas (sandy desert; 21.5%) (BICHERON et al., 2008). The northern region is mostly dominated by consolidated bare areas associated with the alluvial floodplain of oued Chibkha, which is mostly dry and covered with sparsely distributed Acacia trees that often follow the former river. The southern region is dominated by non-consolidated bare areas associated to the huge sand seas of erg Azefal and Agneitir. Relict mangrove stands are found in coastal areas around Mamghar and in islands that testify past humidity conditions in the region (GASSE, 2000).

Field work and data analysis Field work was performed during a total of 31 days between 2008 and 2011. A total of 3200 km were covered by vehicle within the PNBA and two visits were made to Tidra Island (Fig. 1). Visual encounter surveys were performed by four persons in 2008/2009 and seven persons in 2010/2011. Sampling sites were selected in order to cover the environmental variability of the PNBA as well as particular topographic features, such as the Cap Figure 1: Limits of the Parc National du Banc d’Arguin, distribution of all reptile observations, tracks of sampling routes between 2008-2011, main land-cover types (BICHERON et al., 2008) and localities mentioned in text.

101

Blanc. Sampling sites were surveyed by foot for no longer than 1 hour (sampling effort ranging from 0.07 person/hour/day in 2008/2009 to 0.14 in 2010/2011) and night sampling was performed opportunistically around camping sites. Ad hoc observations (road-kills and live specimens) collected by the authors and National Park staff were also recorded. Captured specimens were photographed, a tissue sample was collected, and the geographic coordinates of the locality recorded with a Global Positioning System (GPS).

A georeferenced database of fieldwork observations was created and complemented with published data (MOCQUARD, 1895; PELLEGRIN, 1910; ANGEL, 1938; VILLIERS, 1954; VALVERDE, 1957; SALVADOR, 1982; LE BERRE, 1989; INEICH, 1997; PADIAL et al.,

102

SOW ET AL.

2002; BRITO, 2003; CROCHET et al., 2003; GENIEz et al., 2004; PLEGUEzUELOS et al., 2004; PADIAL, 2006). Geographic coordinates of bibliographic references were collected from topographical maps of Mauritania (Institut Géographique National; 1:200,000). Specimens from PNBA available at the collection of the Muséum national d’Histoire naturelle de Paris (INEICH, 1997) were also included in the database.

The distribution of individual species and species richness were projected on the coordinate system wGS 1984 UTM zone 28N, using the Geographical Information System ArcGIS 10.0 (ESRI, Redlands, California, USA). Species maps represent fieldwork and

published observations over 2 x 2 km UTM grid cells (1685 cells in total) while the species richness map represents number of species observed over 10 x 10 km UTM grid cells (92 cells in total). Observations of each species detected in more than 10 localities were intersected with land-cover categories (BICHERON et al., 2008) to quantify preliminary patterns of habitat selection.

RESULTS The published and fieldwork data comprised 461 records (389 unpublished observations and 72 published observations) from 21 reptile species, grouped in eight families

Table 1: Taxonomic list of reptiles present in the Parc National du Banc d’Arguin. N: number of observations, UTM: number of 2 x 2 km UTM squares in which species was detected, % area: percentage of area occupied, Bare / CBA / NCBA: percentage of observations in bare, consolidated bare and non-consolidated bare areas, respectively.

Family

Species

Phyllodactylidae Tarentola annularis (Geoffroy Saint-Hilaire, 1809) Tarentola chazaliae (Mocquard, 1895) Tarentola ephippiata O’Shaughnessy, 1875 Stenodactylus mauritanicus Guichenot, 1850 Gekkonidae Stenodactylus petrii Anderson, 1896 Stenodactylus sthenodactylus (Lichtenstein, 1823) Tropiocolotes tripolitanus Peters, 1880 Trapelus boehmei wagner, Melville & Schmitz, 2011 Agamidae Acanthodactylus aureus Günther, 1903 Lacertidae Acanthodactylus boskianus (Daudin, 1802) A. dumerili / senegalensis (Daudin, 1802) / Chabanaud, 1918 Acanthodactylus longipes Boulenger, 1921 Mesalina pasteuri (Bons, 1960) Chalcides sphenopsiformis (Duméril, 1856) Scincidae Scincus albifasciatus Boulenger, 1890 Varanus griseus (Daudin, 1803) Varanidae Lytorhynchus diadema (Duméril, Bibron & Duméril, 1854) Colubridae Psammophis schokari (Forsskål, 1775) Psammophis sibilans (Linnaeus, 1758) Cerastes cerastes (Linnaeus, 1758) Viperidae Cerastes vipera (Linnaeus, 1758)

N UTM % area Bare CBA NCBA 96 4 34 1 2 9 10 12 13 1 97 75 9 22 4 21 11 3 4 10 13

95 1 33 1 2 9 9 12 11 1 92 70 9 22 4 21 11 3 4 10 13

5.6 0.1 2.0 0.1 0.1 0.5 0.5 0.7 0.7 0.1 5.5 4.2 0.5 1.3 0.2 1.2 0.7 0.2 0.2 0.6 0.8

35.4 52.9 50.0 41.7 92.3 56.7 36.0 27.3 23.8 36.4 30.0 30.8

45.8 23.5 0.0 8.3 7.7 35.1 14.7 18.2 23.8 9.1 60.0 7.7

18.8 23.5 50.0 50.0 0.0 8.2 49.3 54.5 52.4 54.5 10.0 61.5

REPTILES OF THE PARC NATIONAL DU BANC D’ARGUIN

(Table 1); detailed distributions are presented in Figs. 2-4. In relation to the published data, three new species for the PNBA were detected: 1) The gecko Stenodactylus mauritanicus Guichenot, 1850, recently resurrected from the synonymy of S. sthenodactylus by METALLINOU et al. (2012), located only at the Cap Blanc peninsula (Fig. 2); 2) the lacertid Mesalina pasteuri, located throughout the PNBA (Figs. 3 and 5b); and 3) the snake Psammophis sibilans, located exclusively in Tidra island (Figs. 4 and 5d). On the contrary, the lizard Acanthodactylus boskianus, known from a single observation at Mamghar from 1994 (MNHN 1996.2924), was not observed during recent fieldwork.

Three preliminary patterns of habitat selection were observed among the reptiles of the PNBA (Table 1): 1) species mostly related to bare areas, such as Tarentola ephippiata, Tropiocolotes tripolitanus, Acanthodactylus aureus and A. dumerili / senegalensis; 2) species mostly related to consolidated bare areas, particularly the rocky outcrops of Kerekchet et Teintâne and Dlô Amotai, such as Tarentola annularis and Cerastes cerastes; 3) species mostly related to non-consolidated bare areas, particularly the Azefal and Agneitir dune massifs, such as T. tripolitanus, Trapelus boehmei, Acanthodactylus longipes, Chalcides sphenopsiformis, Varanus griseus, Lytorhynchus diadema and Cerastes vipera.

Tarentola ephippiata was very often found in Acacia trees and tree holes, sometimes in syntopy with T. annularis.

The distribution of observed species richness exhibits spatial asymmetries, and five areas with more than eight species can be observed: Agneitir and Azefal dunes, oued Chibkha river valley, and the Dlô Amotai and

103

Kerekchet et Teintâne rock outcrops (Fig. 6).

These areas tend to present species typical of rocky or dune habitats, species present in open bare areas, and also species exhibiting arboreal behaviour, such as the geckos T. annularis and T. ephippiata. For example, the Dlô Amotai escarpment gathers typical species of rocky habitats, such as T. annularis, S. sthenodactylus and C. cerastes, and also in surrounding areas, species associated to bare areas, such as T. ephippiata, T. boehmei and A. dumerili, and species associated to sandy areas, such as A. longipes, C. sphenopsiformis and V. griseus.

DISCUSSION A total of 15 reptile species have been previously reported as being present in the Cap Blanc peninsula (GENIEz et al., 2004), from which only two (Tarentola chazaliae and A. aureus) were observed at the Cap Blanc Satellite Reserve. Such discrepancy is probably related to the small size (9.2 km2) and location (extreme southern tip) of the continental portion of the Reserve in relation to the Cap Blanc peninsula. Several widely ranged species in Mauritania that are present in neighbouring areas of the PNBA, including Uromastyx dispar, Agama boueti and Echis leucogaster, were also undetected. while general lack of herbaceous vegetation and significant rock outcrops may be related to the absence of the latter two species (authors’ unpublished data), respectively, U. dispar may be present as there are observations very close to the central-eastern border of the PNBA (authors’ unpublished data). Further sampling is needed to determine the potential presence of U. dispar as well as the status of A. boskianus in the PNBA.

104

SOW ET AL.

Figure 2: Distribution of species of Sauria belonging to families Phyllodactylidae, Gekkonidae and Agamidae in the Parc National du Banc dâ&#x20AC;&#x2122;Arguin at a 2 x 2 km UTM scale. Grey symbols in S. petrii map indicate specimens of S. petrii and S. sthenodactylus collected from literature for which a clear diagnosis among species is not possible.

REPTILES OF THE PARC NATIONAL DU BANC D’ARGUIN

105

Figure 3: Distribution of the species of Sauria belonging to families Lacertidae, Scincidae and Varanidae in the Parc National du Banc d’Arguin at a 2 x 2 km UTM scale. Grey symbols in C. sphenopsiformis map indicate tracks.

106

SOW ET AL.

Figure 4: Distribution of the species of Ophidia in the Parc National du Banc dâ&#x20AC;&#x2122;Arguin at a 2 x 2 km UTM scale. Grey symbols in C. cerastes and C. vipera maps indicate tracks that were classified according to the habitat of the area.

During the fieldwork, it became evident that taxonomical classification of observations from A. dumerili and A. senegalensis was nearly impossible using common morphological traits and that specimens with intermediate morphological traits were highly frequent (observed in 95 2 x 2 km UTM grid cells; 5.5% of study area) along most of the PNBA (Fig. 3). As such, both species were lumped for the purposes of the present study (A. dumerili / A. senegalensis). Molecular studies on the likely hybrid zone present at the PNBA are needed to understand how genetic diversity is

spatially structured, if there is interspecific gene flow, where contact zones are located, and finally to revise the systematics of these lizardsâ&#x20AC;&#x2122; group. Preliminary analyses of habitat selection in coastal Mauritania suggested that A. dumerili is found mostly in coastal whitish dunes of marine origin while A. senegalensis is mostly found in continental reddish dunes (INEICH, 1997; CROCHET et al., 2003). Thus, ecological studies are also needed and, in combination with genetic data, should provide knowledge on habitat selection patterns by the distinct genetic demes present in the area.

REPTILES OF THE PARC NATIONAL DU BANC D’ARGUIN

a

b

c

d

107

Figure 5: Some reptile specimens from the Parc National du Banc d’Arguin. (a) Trapelus boehmei, Nw of Baie d’Arguin, 25 November 2008. (b) Mesalina pasteuri, 3 km north of Elb en Nouçç, Azefal, 24 November 2010. (c) Scincus albifasciatus, Mednet ed Dâya, 23 November 2010. (d) Psammophis sibilans, Tidra Island, 04 November 2011.

The subspecies Tarentola ephippiata hoggarensis werner, 1937 is present in the study area. TRAPE et al. (2012) suggested that Sahara populations belong to the full species T. hoggarensis, but detailed morphological and genetic variation analyses of the group T. ephippiata s. l. are still missing. Despite all individuals observed in the PNBA exhibited four clear white marks along the dorsum, it was kept the subspecific designation until phylogenetic relationships are resolved.

Finally, regarding Chalcides, the most recent systematic arrangement proposed for the group (CARRANzA et al., 2008) was followed.

A recent study on the systematics of genus Stenodactylus recognised coastal Atlantic and

Mediterranean populations of S. sthenodactylus as belonging in fact to S. mauritanicus, the later taxon being raised at species level (METALLINOU et al., 2012). A specimen from the Cap Blanc peninsula was included in the analysis and grouped with S. mauritanicus. As such, literature references to the presence of S. sthenodactylus and S. petrii are now mostly uncertain and were depicted as grey dots in S. petrii observations (Fig. 2). In the present study, distribution maps (Figs. 2-4) depict observations corresponding to sequenced specimens or specimens for which detailed photographs were available, allowing clear identifications.

Six groups of species were identified according to distribution patterns: 1) species only

108

SOW ET AL.

Figure 6: Reptile species richness in the Parc National du Banc d’Arguin at a 10 x 10 km UTM scale.

found in the Cap Blanc peninsula and surrounding areas: T. chazaliae, S. mauritanicus and A. aureus. The latter was known exclusively from the Cap Blanc peninsula (CROCHET et al., 2003), while fieldwork confirmed its presence also north of the Cap d’Arguin, in the Kerekchet et Teintâne massif; 2) species only found in the northern part of the PNBA: S. sthenodactylus and C. cerastes; 3) species only found in the southern part of the PNBA: S. petrii, T. tripolitanus, C. sphenopsiformis, Psammophis schokari and C. vipera. These species are typical of the Sahara and have their distributions located largely north of the PNBA (TRAPE & MANé, 2006; TRAPE et al., 2012).

Such striking pattern of absence in northern PNBA areas might be related to the general bareness character of the oued Chibkha floodplain and to lower sampling effort of northern PNBA. For example, although C. vipera was not observed within the PNBA limits in the Cap Blanc peninsula, the species was found very close the northern limit of the Park (INEICH, 1997), which makes its presence within the Park limits highly likely; 4) species with broad range in the PNBA, such as T. annularis, T. ephippiata, T. boehmei (Fig. 5a), A. dumerili / senegalensis, A. longipes, M. pasteuri and V. griseus; 5) species with localised distribution, such as A. boskianus, Scincus albifasciatus (Fig. 5c) and L. diadema; and 6) species restricted to the Tidra island, such as P. sibilans.

Four reptiles were observed at Tidra Island, T. tripolitanus, A. dumerili / senegalensis, C. sphenopsiformis and P. sibilans. The closest known populations of P. sibilans are located in the Chott Boul and Dar es Salam areas (INEICH,

1997; TRAPE & MANé, 2006), in the area of the mouth of Senegal River, at about 600 km to the south. Thus, molecular analyses are needed to determine the level of genetic differentiation of Tidra populations. Further field sampling is needed to determine which species are present in other small islands of the PNBA (Fig. 1).

The PNBA has been suggested as a potential area of sympatry between the vipers C. cerastes and C. vipera, where distinct micro-habitat selection probably limits contact at the local scale (BRITO et al., 2011). This study did not registered syntopic specimens as C. cerastes is apparently restricted to the rocky outcrops of the northern PNBA, while C. vipera was only found on the sand dunes of the southern PNBA (Fig. 4). Further fieldwork sampling is needed to confirm if sympatry could occur in the transition zone between the Dlô Amotai rock and the Azefal dunes.

REPTILES OF THE PARC NATIONAL DU BANC D’ARGUIN

Acknowledgement Field work developed by AS Sow was sponsored by the Mohamed bin zayed Species Conservation Fund (project 11052709). Field work of JCB was partially supported by two grants from National Geographic Society (7629-04 and 8412-08), by Fundação para a Ciência e Tecnologia (FCT: PTDC/BIABEC/099934/2008), and by EU Programme COMPETE. FMF and JCB are supported by FCT (SFRH/BPD/69857/2010 and Programme Ciência 2007, respectively). Logistic support for fieldwork was given by L.O. Yarba and A. Araújo (PN Banc d’Arguin), S.M. Ould Lehlou (Direction des Aires Protégées et du Littoral), Pedro Santos Lda (Trimble GPS), and Off Road Power Shop. z. Boratyński, J.C. Campos, D. Gonçalves, H. Rebelo, P. Sierra, N. Sillero, and P. Tarroso helped in the fieldwork. The FIBA, Fondation Internationale du Banc d'Arguin, provided financial support during the writing of the manuscript.

REFERENCES ANGEL, F. (1938). Liste des reptiles de Mauritanie recueillis par la mission d’études de la Biologie des Acridiens en 1936 et 1937. Description d’une sous-espèce nouvelle d’Eryx muelleri.

Bulletin du Muséum National d’Histoire Naturelle 2eme Série 10: 485-487.

ARAúJO, M.B. (2002). Biodiversity hotspots and zones of ecological transition.

Conservation Biology 16: 1662-1663.

BICHERON, P.; DEFOURNY, P.; BROCKMANN, C.; SCHOUTEN, L.; VANCUTSEM, C.; HUC, M.; BONTEMPS, S.; LEROY, M.; ACHARD, F.; HEROLD, M.; RANERA, F. & ARINO, O. (2008).

GLOBCOVER. Products

109

Description and Validation Report.

Medias-France, Postel, Toulouse, France.

Available at: http://due.esrin.esa.int/globcover/. Retrieved on: 09/21/2009.

BRITO, J.C. (2003). Observations of amphibians and reptiles from North and west Africa - Morocco, Mauritania and Senegal. Boletín de la Asociación Herpetológica Española 14: 2-6.

BRITO, J.C.; FAHD, S.; GENIEz, P.; MARTÍNEzFREIRÍA, F.; PLEGUEzUELOS, J.M. & TRAPE, J.-F. (2011). Biogeography and conservation of viperids from North-west Africa: an application of ecological niche-based models and GIS. Journal of Arid Environments 75: 1029-1037.

BROOKS, T.M.; MITTERMEIER, R.A.; MITTERMEIER, C.G.; DA FONSECA, G.A.B.; RYLANDS, A.B.; KONSTANT, w.R.; FLICK, P.; PILGRIM, J.; OLDFIELD, S.; MAGIN, G. & HILTON-TAYLOR, C. (2002). Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology 16: 909-923.

BUTCHART, S.H.M.; wALPOLE, M.; COLLEN, B.; VAN STRIEN, A.; SCHARLEMANN, J.P.w.; ALMOND, R.E.A.; BAILLIE, J.E.M.; BOMHARD, B.; BROwN, C.; BRUNO, J.; CARPENTER, K.E.; CARR, G.M.; CHANSON, J.; CHENERY, A.M.; CSIRKE, J.; DAVIDSON, N.C.; DENTENER, F.; FOSTER, M.; GALLI, A.; GALLOwAY, J.N.; P.; GREGORY, R.D.; GENOVESI, HOCKINGS, M.; KAPOS, V.; LAMARQUE, J.F.; LEVERINGTON, F.; LOH, J.; MCGEOCH, M.A.; MCRAE, L.; MINASYAN, A.; HERNáNDEz MORCILLO, M.; OLDFIELD, T.E.E.; PAULY, D.; QUADER, S.; REVENGA, C.; SAUER, J.R.; SKOLNIK, B.; SPEAR, D.; STANwELL-SMITH, D.; STUART, S.N.;

110

SOW ET AL.

SYMES, A.; TIERNEY, M.; TYRRELL, T.D.; VIé, J.-C. & wATSON, R. (2010). Global biodiversity: indicators of recent declines.

Science 328: 1164-1168.

CARRANzA, S.; ARNOLD, E.N.; GENIEz, P.; ROCA, J. & MATEO, J.A. (2008): Radiation, multiple dispersal and parallelism in the skinks, Chalcides and Sphenops (Squamata: Scincidae), with comments on Scincus and Scincopus and the age of the Sahara Desert. Molecular Phylogenetics and Evolution 46: 1071-1094.

CARVALHO, S.B.; BRITO, J.C.; CRESPO, E.J. & POSSINGHAM, H.P. (2011). Incorporating evolutionary processes into conservation planning using species distribution data: a case study with the western Mediterranean herpetofauna. Diversity and Distributions 17: 408-421.

CROCHET, P.-A.; GENIEz, P. & INEICH, I. (2003). A multivariate analysis of the fringe-toed lizards of the Acanthodactylus scutellatus group (Squamata: Lacertidae): systematics and biogeographical implications. Zoological Journal of the Linnean Society 137: 117-155.

DEKEYSER, P.L. & VILLIERS, A. (1956).

Contribution à l'étude du peuplement de la Mauritanie. Notations écologiques et biogéographiques sur la faune de l'Adrar.

Mémoires de l'Institut Français d'Afrique Noire 44: 9-222.

GARCIA, R.A.; BURGESS, N.D.; CABEzA, M.; RAHBEK, C. & ARAúJO, M.B. (2012).

Exploring consensus in 21st century projections of climatically suitable areas for African vertebrates. Global Change Biology 18: 1253-1269.

GASSE, F. (2000). Hydrological changes in the African tropics since the Last Glacial

Maximum. Quaternary Science Reviews 19: 189-211.

GENIEz, P.; MATEO, J.A.; GENIEz, M. & PETHER, J. (2004). The Amphibians and Reptiles of Western Sahara: An Atlas and Field Guide. Series: Frankfurt Contributions to Natural History, vol. 19. Edition Chimaira, Frankfurt am Main, Germany.

HIJMANS, R.J.; CAMERON, S.E.; PARRA, J.L.; JONES, P.G. & JARVIS, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.

HOBOHM, C. (2003). Characterization and ranking of biodiversity hotspots: centres of species richness and endemism. Biodiversity and Conservation 12: 279-287.

HOLE, D.G.; HUNTLEY, B.; ARINAITwE, J.; BUTCHART, S.H.M.; COLLINGHAM, Y.C.; FISHPOOL, L.D.C.; PAIN, D.J. & wILLIS, S.G. (2011). Toward a management framework for networks of protected areas in the face of climate change. Conservation Biology 25: 305-315.

INEICH, I. (1997). Les amphibiens et reptiles du littoral mauritanien, In P. Colas (ed.)

Environnement et Littoral Mauritanien. Actes du Colloque, 12-13 Juin 1995, Nouakchott, Mauritanie. CIRAD, Montpellier, France, pp. 93-99.

KATI, V.; DEVILLERS, P.; DUFRêNE, M.; LEGAKIS, A.; VOKOU, D. & LEBRUN, P. (2004). Hotspots, complementarity or representativeness? designing optimal smallscale reserves for biodiversity conservation.

Biological Conservation 120: 471-480.

LE BERRE, M. (1989). Faune du Sahara. 1.

Poissons, Amphibiens, Reptiles. Lechevalier - R. Chabaud, Paris.

MAHé, E. (1985). Contribution à l’Étude

REPTILES OF THE PARC NATIONAL DU BANC D’ARGUIN

Scientifique de la Région du Banc d’Arguin (Littoral Mauritanien 21’’20’/19’’20’ ln).

Peuplements Avifaunistiques. Ph.D. dissertation. Université des Sciences et Techniques du Languedoc, Montpellier, France.

METALLINOU, M.; ARNOLD, E.N.; CROCHET, P.A.; GENIEz, P.; BRITO, J.C.; LYMBERAKIS, P.; BAHA EL DIN, S.; SINDACO, R.; ROBINSON, M. & CARRANzA, S. (2012). Conquering the Sahara and Arabian deserts: systematics and biogeography of Stenodactylus geckos (Reptilia: Gekkonidae). BMC Evolutionary Biology 12: 258.

MOCQUARD, M.F. (1895). Note sur quelques reptiles du cap Blanc. Bulletin du Muséum National d’Histoire Naturelle 1: 310-312.

MONOD, T. (1988). Notes sur la Flore et la Végétation du Parc National du Banc d’Arguin. Series: Etudes Sahariennes et Ouest-Africaines, vols. 1-3. Association des Naturalistes Sahariens et OuestAfricains, Nouakchott, Mauritania.

N.; MITTERMEIER, R.A.; MYERS, MITTERMEIER, C.G.; DA FONSECA, G.A.B. & KENT, J. (2000). Biodiversity hotspots for conservation priorities.

Nature 403: 853-858.

PADIAL, J.M. (2006). Commented distributional list of the reptiles of Mauritania (west Africa). Graellsia 62: 159-178.

PADIAL, J.M.; CASTROVIEJO-FISCHER, S.; QUINTANA, A.z.; áVILLA, E.; PéREzMARÍN, J. & CASTROVIEJO, J. (2002).

111

Notas de distribución de reptiles para el NE de áfrica. Boletín de la Asociación Herpetológica Española 13: 2-5.

PELLEGRIN, J. (1910). Mission en Mauritanie occidentale III: partie zoologique.

Reptiles. Actes de la Société Linnéenne de Bordeaux 64: 21-25.

PLEGUEzUELOS, J.M.; FARIñA,B.; MATEO,J.A. & GENIEz, P. (2004). Nuevos datos sobre los anfibios y reptiles de Mauritania y el Sáhara Occidental. Boletín de la Asociación Herpetológica Española 15: 76-80.

SALVADOR, A. (1982). A revision of the lizards of the genus Acanthodactylus (Sauria: Lacertidae). Bonner Zoologische Monographien 16: 1-167.

SPECTOR, S. (2002). Biogeographic crossroads as priority areas for biodiversity conservation. Conservation Biology 16: 1480-1487.

TRAPE, J.F. & MANé, Y. (2006). Guide des Serpents d’Afrique Occidentale: Savane et Désert. IRD éditions, Montpellier, France.

TRAPE, J.-F.; TRAPE, S. & CHIRIO, L. (2012).

Lézards, Crocodiles et Tortues d’Afrique Occidentale et du Sahara. IRD éditions, Montpellier, France.

VALVERDE, J.A. (1957). Aves del Sáhara Español.

Estudio Ecológico del Desierto. Instituto de Estudios Africanos CSIC, Madrid.

VILLIERS, A. (1954). La collection de serpents de l’I.F.A.N. (acquisitions 1953). Bulletin de l’Institut Fondamental d’Afrique Noire 16: 1234-1247.

112

Basic and Applied Herpetology 28 (2014): 113-136

Herpetofauna del Parque Natural das Fragas do Eume (A Coruña): distribución, estado de conservación y amenazas Pedro Galán Departamento de Bioloxía Animal, Bioloxía Vexetal e Ecoloxía, Facultade de Ciencias, Universidade da Coruña, A Coruña, Spain. * Correspondence: Departamento de Bioloxía Animal, Bioloxía Vexetal e Ecoloxía, Facultade de Ciencias, Universidade da Coruña, Campus da Zapateira s/n, 15071-A Coruña, España. Tel: +34 981167000, Fax: +34 981167065, E-mail: pgalan@udc.es

Recibido: 15 Marzo 2013; revisión recibida: 29 Noviembre 2013; aceptado: 29 Noviembre 2013.

El Parque Natural das Fragas do Eume, situado a baja altitud y con un clima templado, está cubierto en gran parte por un bosque atlántico termófilo. Las fuertes pendientes de las laderas del valle del Eume han impedido tanto la explotación agrícola como la urbanización, que dominan en las zonas circundantes, lográndose la conservación de uno de los mejores bosques atlánticos termófilos de Europa. Muestreos intensivos realizados en este Parque revelaron una rica herpetofauna, compuesta por un alto porcentaje de especies endémicas ibéricas y eurosiberianas centroeuropeas. Se encontraron 13 especies de anfibios y 10 de reptiles, lo que representa el 93% y el 40% respectivamente de las especies presentes en Galicia y el 48% y 21% respectivamente del total de las especies ibéricas. La mayor riqueza de especies se encontró en los bosques de la zona inferior del cauce del Eume y en algunas zonas del centro y norte del Parque. Los hábitats más importantes, según el número de especies que albergan, fueron los bosques de ribera, herbazales húmedos y matorrales para los anfibios en su fase terrestre, y durante su fase acuática, charcas en herbazales y turberas, arroyos y pequeñas escorrentías. En el caso de los reptiles, fueron los linderos arbustivos y herbáceos del bosque, así como matorrales, afloramientos rocosos y taludes. Una de las principales amenazas para la herpetofauna son las plantaciones de eucaliptos, que eliminan los bosques autóctonos y favorecen los incendios. Otras amenazas importantes son los cambios en el uso del suelo, los contaminantes vertidos en los medios acuáticos y la expansión de algunas especies, como el jabalí.

Key words: Anfibios; bosques atlánticos relictos; Galicia; Parque Natural Fragas do Eume; Reptiles.

Herpetofauna of Fragas do Eume Natural Park (A Coruña): distribution, conservation status and threats. The Natural Park of Fragas do Eume, with its coastal location and thus low altitude and temperate weather conditions, is mostly covered by a thermophilous Atlantic forest. The steepness of Eume valley slopes have hindered both agricultural exploitation and urbanization, which dominate the surrounding plain and hills, thus protecting one of Europe’s best-conserved thermophilous Atlantic forests.

Intensive sampling in this Park revealed a rich herpetofauna assemblage, with a high percentage of both Iberian endemic species and Eurosiberian Central European species. Thirteen species of amphibians and 10 of reptiles are present in the Park, representing, respectively, 93% and 40% of the species present in Galicia and 48% and 21%, respectively, of total Iberian species. The highest species richness was found especially in the forests of the lower area of the Eume riverbed and in certain areas of the center and north of the Park. The most important habitats of the Park, according to the number of species that they harbor, were the riparian forest, wet grasslands and shrublands for amphibians during their terrestrial phase, and ponds in grasslands and peatlands, streams and small runoff during their aquatic reproductive phase. For reptiles, shrubby and herbaceous edges of Atlantic forest, as well as scrublands, rocky outcrops and slopes were the main habitats. One of the main threats to herpetofauna are the eucalyptus plantations, which eliminate the autochthonous forest and favor fires. Another important threats are changes in land use, pollutant spills into aquatic environments and expansion of certain species, such as wild Boar.

Key words: Amphibians; Fragas do Eume Natural Park; Galicia; relict Atlantic forest; Reptiles.

DOI: http://dx.doi.org/10.11160/bah.13009/

Supplementary material available online

114

GALÁN

Las comarcas costeras de Galicia han poseído, desde épocas históricas, una elevada densidad de población humana, lo que ha provocado una profunda transformación de los medios naturales. En el pasado, el territorio se modificó intensamente a causa de la actividad agrícola y ganadera. En la actualidad existe un incremento de la transformación del paisaje debido al desarrollo urbanístico e industrial, así como a las extensas plantaciones con especies arbóreas alóctonas (eucalipto principalmente). Por todo ello, los hábitats naturales que ocuparon una mayor extensión en el pasado en esta zona (como los bosques atlánticos), se han visto reducidos a pequeños fragmentos, aislados y alterados. En este contexto, el Parque Natural das Fragas do Eume, declarado como tal en 1997, alberga la mayor superficie de bosque atlántico termófilo de baja altitud (robledales acidófilos de Quercus robur y alisedas de Alnus glutinosa) que existe en la actualidad en todo el noroeste ibérico (VALES, 1994; COSTA TENORIO et al., 1997). La supervivencia de esta masa forestal en una zona costera y densamente poblada se debe a la peculiar orografía de la zona, con fuertes pendientes originadas por el angosto cañón fluvial del río Eume, que ha limitado su explotación ganadera o agrícola, así como el asentamiento de poblaciones humanas y la urbanización. Este tipo de bosque cubría en el pasado una gran parte del territorio noroccidental ibérico (VALES, 1994), por lo que la actual biodiversidad que existe en este espacio natural es un reflejo de la que debió ser mayoritaria en el pasado, con anterioridad a las transformaciones humanas del territorio.

A pesar de que el Parque Natural das Fragas do Eume goza de una gran popularidad, recibiendo un elevado número de visitantes cada

año, y de que ha sido objeto de diversas investigaciones sobre una parte de su biodiversidad (e.g. briofitos: REINOSO FRANCO, 1984, 1985; líquenes: LóPEz DE SILANES, 1988; helechos relictos: QUINTANILLA, 1997; QUINTANILLA & AMIGO, 1999; flora en general: LOSA QUINTANA, 1973; IzCO et al., 1990; PULGAR SAñUDO et al., 2006 o coleópteros: NOVOA et al., 2003; BASELGA & NOVOA, 2008), no se han realizado hasta la fecha estudios detallados sobre la composición y distribución de su herpetofauna. únicamente se dispone de algunos listados, que mencionan a las especies más relevantes (DE CASTRO, 1977; CARAMELO REGO et al., 1995; GONzáLEz et al., 1995; LEIRO et al., 2003; MOURIñO LOURIDO et al., 2004; FERNáNDEz DÍAz & NEGREIRA SOUTO, 2005). Tampoco se ha hecho una evaluación global de las principales amenazas para la conservación de los anfibios y reptiles que alberga, a pesar de que existen dentro de él cinco especies consideradas como vulnerables en el Catálogo Gallego de Especies Amenazadas (CONSELLERÍA DE MEDIO AMBIENTE E DESENVOLVEMENTO SOSTIBLE, 2007; GALáN, 2009). Como prueba de su vulnerabilidad, en la primavera de 2012, una parte importante de este espacio natural sufrió un incendio que afectó a 370 ha de la zona central del Parque (el 4% de su superficie), de un total de 750 ha quemadas, cuyas consecuencias sobre su biodiversidad no han sido aún evaluadas.

En el presente artículo se pretende dar una visión de conjunto sobre las especies que componen la herpetofauna de este espacio natural, detallando su distribución en él en cuadrículas UTM de 1 x 1 km, su abundancia relativa y los hábitats ocupados, y exponiendo las principales amenazas para su conservación.

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

MATERIALES Y MéTODOS El Parque Natural das Fragas do Eume se extiende a lo largo de más de 30 km del cauce del río que le da nombre, en sentido este-oeste, desde el interior de Galicia, en la Serra da Loba, en el límite provincial entre A Coruña y Lugo, hasta las proximidades de la ría de Ares, junto a la costa del Golfo ártabro, ocupando una superficie de 9125 ha (Fig. 1). Su rango de altitudes va desde el nivel del mar hasta los 720 m (en los pisos colino y montano inferior), con cotas que superan los 600 m en las sierras de Queixeiro y da Loba, en el este, y menos de

115

100 m en gran parte de su zona occidental.

Pertenece a la región Eurosiberiana, provincia Atlántica-Europea, subprovincia CántabroAtlántica (RIVAS-MARTÍNEz, 1987). La zona occidental del Parque (tramo bajo del río Eume) se emplaza en el dominio climático Oceánico húmedo (con unos 1400 mm de precipitación anual y 15,1ºC de media anual cerca de la costa), mientras que la zona media y oriental se encuentra en un área de transición entre éste y el dominio Oceánico de montaña, que prevalece en las sierras de su extremo oriental (con unos 1900 mm de precipitación anual y 11,7ºC de media anual en las zonas altas de

Figura 1: Parque Natural das Fragas do Eume, A Coruña, Galicia. La línea negra indica los límites del Parque, en color azul se indica el río Eume y el resto de la red fluvial (en azul más grueso el embalse del río Eume). En verde, las masas remanentes de bosque atlántico (el resto de las zonas, en color amarillo, están mayoritariamente cubiertas por matorrales y plantaciones de eucaliptos). En rojo, las principales carreteras que cruzan el Parque.

Se señalan también algunos de los topónimos más importantes, las tramas UTM de 10 x 10 km (en trazo más grueso) y las de 1 x 1 km, que fue la escala elegida para representar la distribución de las especies en las figuras siguientes. Los colores indicados hacen referencia a la versión online del presente artículo.

116

GALÁN

esas sierras) (FERNáNDEz DÍAz & NEGREIRA SOUTO, 2005; PULGAR SAñUDO et al., 2006).

El tramo bajo del río Eume discurre por un valle muy abrupto, de origen tectónico, con profundas gargantas y laderas de pendientes pronunciadas, donde se sitúa un extenso bosque atlántico (Fig. S1) tanto en las laderas (robledales galaico-asturianos occidentales de la asociación Blechno spicanti-Quercetum roboris, con Quercus robur como especie dominante) como en las riberas de ríos (ripisilvas galaico-portuguesas de la asociación Senecio bayonensis-Alnetum glutinosae, dominadas por Alnus glutinosa) (FERNáNDEz DÍAz & NEGREIRA SOUTO, 2005; PULGAR SAñUDO et al., 2006). La peculiar orografía de este Parque y la densa cobertura arbórea generan unas condiciones de umbría y elevada humedad ambiental. Este hecho, unido a la situación de baja altitud y proximidad al mar (que originan escaso contraste térmico durante todo el año) de gran parte del Parque, ha permitido la supervivencia de numerosas especies relictas, entre las que destacan helechos subtropicales (Culcita macrocarpa o Woodwardia radicans).

Además de éstos, la presencia de diversos taxones, como Laurus nobilis, Castanea sativa o Hypericum androsaemum, entre otros, testimonian la evolución de estos bosques a partir de las laurisilvas terciarias (COSTA TENORIO et al., 1997). La relativa estabilidad climática que ha mantenido esta zona a lo largo de dilatados períodos de tiempo ha permitido la supervivencia de numerosas especies, desaparecidas en otras zonas de baja altitud (BASELGA & NOVOA, 2008; GALáN, 2012a).

Además de estos bosques, en las zonas elevadas existen extensas formaciones de matorral (Fig. S1), con diversas especies (Erica australis, Ulex gallii, U. europaeus, Calluna vulgaris), entre las que se insertan pequeñas zonas higro-

turbosas. En diversas áreas del Parque, especialmente en su parte oriental, existen núcleos de población humana, con caseríos y aldeas, rodeados de campos de cultivo y pastizales para el ganado. A lo largo de todo el espacio protegido existen también extensas plantaciones de árboles alóctonos, principalmente de Eucalyptus globulus, especie que llega a dominar en algunas zonas y se mezcla también con las masas de bosque atlántico, generando en muchos casos un bosque mixto (Fig. S1).

Para este trabajo, a pesar de que se dispone de datos propios sobre la herpetofauna de este espacio a lo largo de un período de 40 años, se han utilizado únicamente los datos obtenidos en muestreos realizados durante los últimos 11 años (2003-2013, ambos inclusive), ya que el objetivo es dar a conocer la distribución y abundancia actual de la herpetofauna en este Parque y también debido a la imposibilidad de georreferenciar los datos más antiguos. En estos 11 años se recorrieron de nuevo las zonas ya conocidas personalmente y se intentó además visitar la totalidad de las 139 cuadrículas UTM de 1 x 1 km que componen este Parque (incluyendo las periféricas que únicamente comprenden una parte de su superficie). Así, se muestrearon 134 cuadrículas UTM de 1 x 1 km (el 96,4%), aunque únicamente se obtuvieron datos de presencia de anfibios y/o reptiles en 103 (el 76,9% de las muestreadas, 74,1% del total). Este número, relativamente bajo, se debe a que amplias extensiones del Parque son formaciones densas de bosque (incluyendo plantaciones de eucaliptos y pinos) o de matorral alto, donde las densidades de anfibios y reptiles son muy bajas y además la detección de estas especies es difícil. Estas cuadrículas de 1 x 1 km se integran principalmente dentro de las cuadrículas UTM de 10 x 10 km NJ70 y NJ80, aunque también comprenden la zona norte de la NH89, el extre-

117

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

Tabla 1: Frecuencias de aparición de las 10 especies de reptiles presentes en el Parque Natural das Fragas do Eume en los 16 tipos de hábitats terrestres que se diferenciaron en él. N: número de puntos de muestreo en cada tipo de hábitat terrestre. Especies: Pb: Podarcis bocagei; Im: Iberolacerta monticola; Ls: Lacerta schreiberi; Tl: Timon lepidus; Cs: Chalcides striatus; Af: Anguis fragilis; Ca: Coronella austriaca; Nn: Natrix natrix; Nm: Natrix maura; Vs: Vipera seoanei. Tot sp: número total de especies de reptiles encontrado en cada tipo de hábitat.

Tipos de hábitats terrestres

N

Bosques atlánticos (Quercus) y mixtos

54

Bosques de ribera (Alnus) y orillas de ríos y arroyos

71

Linderos arbustivos de bosques con Rubus y Pteridium

67

Pb

Im

Ls

Tl

Cs

Af

2

1

1

1

6

4

4

2

2

13

7

Ca

Nn Nm

3 4 2

2

10

2

1

1

1

Linderos herbáceos de bosques

55

1

2

Linderos herbáceos de matorral

25

1

1

Herbazales ruderales de bordes de caminos y cultivos

35

1

7

1

Herbazales sobre suelos húmedos y praderas de siega

59

1

5

2

Matorrales de Ulex, Erica y Calluna

50

Turberas y matorrales higroturbosos

7

Roquedos y laderas rocosas con matorral disperso

23

7

6

8

6

4

4 3

Taludes rocosos

43

8

13

2

Taludes de tierra

23

8

1

1

Muros de construcciones

2

Vs Tot sp

3

1

1

7

3

7 5 4

1

3

2

2

1

1

5

2

1

1 1

2

1

6 4

103

40

18

6

8

2

1

1

Plantaciones de eucaliptos

31

2

Plantaciones de pinos

15 669

79

49

37

5

8

44

10

14

1

8

11

8

12

2

2

12

6

8

1

5

Nº medios terrestres con presencia de cada especie

6

1

Amontonamientos de piedras o escombros

Total

4

1

6 3

1

2 0

mo oeste de la cuadrícula NJ90, así como unas pequeñas zonas del extremo noroeste de la NH99 (sólo dos cuadrículas de 1 x 1 km) y del extremo sureste de la NJ71 (sólo una cuadrícula de 1 x 1 km), todas ellas dentro del huso 29T. Para el muestreo de los anfibios y reptiles se utilizaron diferentes metodologías. La principal,

común para los dos grupos, consistió en la realización de transectos a lo largo de los diferentes hábitats que lo integran, que se repitieron durante todos los períodos del año y se realizaron tanto de día como por la noche. Como la heterogeneidad ambiental del Parque es elevada, para poder adscribir cada observación de reptil o anfibio en

118

GALÁN

Figura 2: Localización de los puntos de muestreo realizados en el Parque Natural das Fragas do Eume (A Coruña) para detectar anfibios y reptiles. En algunos casos, un punto puede señalar más de una estación de muestreo, dada la escala del mapa.

fase terrestre a un tipo concreto de hábitat, se diferenciaron 16 tipos de medios terrestres, que incluían la diversidad de hábitats existente (Tabla 1). A lo largo de los transectos realizados se seleccionaron aleatoriamente una serie de puntos de muestreo en el campo, se anotó el hábitat de estos puntos (referido a una de las 16 categorías diferenciadas) y se dedicó un tiempo comprendido entre 5 y 10 minutos para buscar herpetos en ellos. En total, se muestrearon 669 puntos repartidos por todo el Parque (Tabla 1; Fig. 2). En el caso de los muestreos nocturnos, para detectar anfibios activos en su fase terrestre, el número de puntos de muestreo fue muy inferior

Figura 3: Mapas de distribución de las especies de urodelos en el Parque Natural das Fragas do Eume en cuadrículas UTM de 1 x 1 km.

119

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

Tabla 2: Frecuencias de aparición de las 13 especies de anfibios presentes en el Parque Natural das Fragas do Eume en los 14 tipos de medios terrestres que se diferenciaron en él para los muestreos nocturnos.

N: número de puntos de muestreo en cada tipo de hábitat terrestre. Especies: Ss: Salamandra salamandra; Cl: Chioglossa lusitanica; Lb: Lissotriton boscai; Lh: Lissotriton helveticus; Tm: Triturus marmoratus; Ao: Alytes obstetricans; Dg: Discoglossus galganoi; Bs: Bufo spinosus; Bc: Bufo calamita; Hm: Hyla molleri; Ri: Rana iberica; Rt: Rana temporaria; Pp: Pelophylax perezi. Se indica también el número de especies de anfibios encontrado en cada tipo de hábitat.

Tipos de hábitats terrestres

N Ss Cl Lb Lh Tm Ao Dg Bs Bc Hm Ri Rt Pp

Bosques atlánticos (Quercus) y mixtos 25 7

3

1

Bosques de ribera (Alnus) y orillas de ríos

20 6

5

4

Linderos arbustivos de bosques con Rubus y Pteridium

11 1

6 2

2

5

5

1

Tot sp

1

5

2

8

1

3

Linderos herbáceos de bosques

10 2

3

3

3

Linderos herbáceos de matorral

9

1

1

1

3

Herbazales ruderales de bordes de caminos y cultivos

9

1

2

Herbazales sobre suelos húmedos y praderas de siega

16 3

1

Matorrales de Ulex, Erica y Calluna

12 2

Taludes rocosos

14 3

6

Taludes de tierra

10 3

3

Muros de construcciones

9

2

Amontonamientos de piedras o escombros

4

Plantaciones de eucaliptos

10 1

Plantaciones de pinos

6 165 31 19 7

Total Nº medios terrestres con presencia de cada especie

1

1

2 1

1

1 4

1 1

5

2

2

8 7 2 2

1

12

2

1

2

1

2 1

5

4

(165 puntos), debido a las mayores dificultades de desplazamiento durante la noche, pero también estuvieron representados todos los hábitats terrestres del Parque, excepto dos (turberas y laderas rocosas, a los que no se pudo acceder en las horas nocturnas; Tabla 2), empleándose la misma metodología de muestreo que durante el día.

La búsqueda de anfibios en medios acuáticos se realizó muestreando todos los tipos de

0 3

1

1

4

25

1

0

6

15

2

2

1

1

2

10

1

0

2

7

1

charcas o corrientes de agua que se encontraron en estos transectos, pasando repetidas veces una red de mano por el agua (entre 5 y 20 veces, en función del tamaño del medio acuático), anotando las larvas, huevos y/o adultos de cada especie de anfibio que se encontraban. Todos ellos fueron devueltos inmediatamente al agua tras su identificación. Al igual que se hizo con los medios terrestres, los diferentes tipos de

120

GALÁN

Tabla 3: Frecuencias de aparición de las 13 especies de anfibios presentes en el Parque Natural das Fragas do Eume en los 17 tipos de medios acuáticos que se diferenciaron en él. N: número de medios acuáticos de cada tipo muestreados (en el caso de Embalse se refiere a los diferentes puntos de muestreo en un mismo embalse; también ser realizaron muestreos en distintos puntos del río Eume). Especies: Ss: Salamandra salamandra; Cl: Chioglossa lusitanica; Lb: Lissotriton boscai; Lh: Lissotriton helveticus; Tm: Triturus marmoratus; Ao: Alytes obstetricans; Dg: Discoglossus galganoi; Bs: Bufo spinosus; Bc: Bufo calamita; Hm: Hyla molleri; Ri: Rana iberica; Rt: Rana temporaria; Pp: Pelophylax perezi. Se indica también el número de especies de anfibios encontrado en cada tipo de medio acuático.

Tipos de hábitats acuáticos

N Ss Cl Lb Lh Tm Ao Dg Bs Bc Hm Ri Rt Pp

Ríos

17

2

3

10

14

2 2

Arroyos

32 11 22 3

1

1

2

23

Escorrentías

58 11 9 10 9

2

5

14 11

Acequias de regadío

11 2

3

Charcas anejas a ríos

19 4

10 2

Manantiales

4

1

1

2

1

2

39 8

7

5

13 2

2

3

1

1

Charcas en matorral

6

5

3

3

1

Charcas en bosque

7

3

3

3

5

2

3

1

2

2

Charcas en rocas

6 16 6

Charcas en excavaciones

4

1

Charcas someras en desmontes

8

Depósitos de agua abiertos

7

2

3

Lavaderos

5

1

2

Embalse

6

Total Nº medios acuáticos con presencia de cada especie

5

1

5

3

4

5

1

1

7

4 1

2

7

8

3

4

4

1

9 8

2

7

3

5

3

7

2 4

4 1

4

2

7 2

2

1

2

1

7

1

5

1

1

4

7

3

17 35

5

6

74 58 22

3

9

2

3

10 12

2 1

16 13 6

medios acuáticos se agruparon en una serie de categorías, 17 en este caso (Tabla 3) y se muestreó un total de 258 medios acuáticos dentro de los límites del Parque.

En cada uno de los puntos de muestreo, tanto en el medio terrestre como en el acuático, se prestó también especial atención a las alteraciones observadas en el medio natural, anotando todas las que se comprobaron.

21 3

1

258 50 35 62 40 13 12 5

9 8

1

6

1

2

8 3

4

Charcas de herbazal

Charcas en roderas en pistas

1 2

5

2

Charcas de turbera

1

1 2

Tot sp

9

7

Cada observación de un anfibio o reptil fue georreferenciada con un GPS (Datum ED50). La representación de las observaciones se realizó mediante cuadrículas UTM de 1 x 1 km. Para la realización de los mapas se ha utilizado el programa FreeHand MX (Adobe Systems, San Jose, California, USA) para ordenadores Macintosh.

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

RESULTADOS Dentro de los límites del Parque Natural das Fragas do Eume se encontraron 13 especies de anfibios y 10 de reptiles (Fig. S2).

Anfibios Las especies de anfibios observadas con mayor frecuencia (≥ 40 cuadrículas UTM de 1 x 1 km) fueron Salamandra salamandra, Bufo spinosus y Rana iberica.

Salamandra salamandra, perteneciente en estas poblaciones a la subespecie S. s. gallaica, aunque prácticamente en límite con S. s. bernardezi en la zona norte del espacio natural, fue el anfibio más extendido en el Parque (Fig. 3) y el más observado en los muestreos nocturnos, ocupando además un mayor número de tipos de hábitats terrestres (Tabla 2), aunque principalmente en las zonas de bosque y de matorral. Sus larvas aparecieron en el 19,4% de los medios acuáticos muestreados, predominando en arroyos, escorrentías y charcas en herbazales (Tabla 3).

Rana iberica es el anfibio más frecuente después de S. salamandra y está también extendida por todo el Parque, escaseando únicamente en el extremo nororiental, donde predominan las mesetas y matorrales (Fig. 4). En todas las zonas apareció generalmente asociada a las corrientes de agua, sobre todo ríos (en el 82,4% de los puntos de muestreo en este medio), arroyos (en el 71,9% de los muestreados) y pequeñas escorrentías en cunetas (Tabla 3), aunque también en charcas estacionales en herbazales y otros medios lénticos; en total, en el 28,7% de los medios acuáticos muestreados. Debido a su vinculación a las corrientes de agua, únicamente apareció en

121

dos tipos de medios terrestres (bosques de ribera y herbazales húmedos, Tabla 2).

Bufo spinosus también se observó con alta frecuencia en la mayor parte del Parque y en una amplia diversidad de hábitats en su fase terrestre (10 de 14, Tabla 2). Las larvas aparecieron en el 13,6% de los medios acuáticos muestreados, sobre todo en zonas remansadas de ríos y en las márgenes del embalse del Eume, aunque también en charcas de herbazal estacionales y escorrentías de cunetas de caminos (Tabla 3).

Otras especies de anfibios que también se encontraron con frecuencias relativamente elevadas (en 22-33 cuadrículas UTM de 1 x 1 km) fueron Lissotriton boscai, Rana temporaria y Chioglossa lusitanica.

Lissotriton boscai es el tritón más abundante en el Parque, extendido por casi toda su superficie, y además el anfibio que apareció en una mayor diversidad de medios acuáticos (16 de 17, Tabla 3), estando presente en el 24,0% del total muestreado. En los recorridos nocturnos es difícil de detectar por su pequeño tamaño, por lo que únicamente apareció en cuatro tipos de medios terrestres (Tabla 2), lo que claramente subestima su abundancia real en este tipo de medios.

Rana temporaria, que en esta zona muestra ecotipos de baja altitud, de pequeño tamaño y pigmentación oscura reducida (con las características morfológicas que utilizó el naturalista Víctor López Seoane para describir la subespecie R. t. parvipalmata), apareció distribuida por la mayor parte del Parque, ocupando en su fase terrestre, tanto zonas de bosque como de matorral y herbáceas (Tabla 2; Fig. 4). En su fase reproductora acuática, sus larvas se encontraron en el 22,5% de los medios acuáticos que se muestrearon, especialmente en charcas estacionales en herbaza-

122

GALÁN

Figura 4: Mapas de distribución de las especies de anuros en el Parque Natural das Fragas do Eume en cuadrículas UTM de 1 x 1 km.

les, en escorrentías en cunetas de pistas y caminos y en charcas de rebose o borde de arroyo (Tabla 3).

Chioglossa lusitanica se encuentra ampliamente distribuida en el Parque, si bien casi siempre asociada a las masas de bosque atlántico, los

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

bosques de ribera y a las corrientes de agua, escaseando o estando ausente en las zonas elevadas y mesetas con matorral o cultivos de su extremo oriental (Fig. 3). En las zonas donde el bosque atlántico se encuentra bien conservado y la orografía es abrupta, puede observarse lejos de las corrientes de agua. Se encuentra muy vinculada a los desniveles del terreno, especialmente a los taludes rocosos o incluso muros de construcciones próximas al agua (Tabla 2). Apareció en el 13,6% del total de medios acuáticos muestreados, sobre todo arroyos (presente en el 68,7% de los muestreados), aunque también en escorrentías de cunetas en pistas y carreteras (15,5% de las muestreadas). Contrariamente, en los puntos de muestreo en los ríos (sobre todo en el Eume), sólo apareció en dos (11,8%), mientras que no fue localizada su presencia en el embalse.

Otras cuatro especies de anfibios fueron menos frecuentes, apareciendo en sólo 10-18 cuadrículas de 1 x 1 km, aunque en general se encuentran ampliamente distribuidas en el Parque: Lissotriton helveticus, Pelophylax perezi, Discoglossus galganoi y Triturus marmoratus.

Lissotriton helveticus, aunque más escaso que L. boscai, también apareció bien repartido por las diversas zonas del Parque (Fig. 3). Utiliza una amplia variedad de medios acuáticos (13 de 17), aunque se encontró en ellos con menor frecuencia que el tritón ibérico, en el 15,5% de los puntos acuáticos muestreados (Tabla 3).

Pelophylax perezi se localizó sobre todo en la zona periférica nordeste del Parque y en algunas de las orillas del embalse del Eume, faltando (salvo en zonas muy concretas) en las áreas más densamente forestadas, generalmente situadas en la zona occidental, central y meridional (Fig. 4). Los hábitats acuáticos donde apareció con mayor frecuencia fueron las charcas de herbazal y las formadas en

123

zonas excavadas, así como en las orillas del embalse y en determinadas escorrentías de cuneta (Tabla 3). Se encontró en el 8,5% de los medios acuáticos prospectados.

Discoglossus galganoi apareció de forma dispersa en diferentes puntos del Parque, tanto en zonas de bosque como de herbazal (Tabla 2; Fig. 4). Se observó reproduciéndose en diferentes tipos de charcas estacionales o efímeras, aunque también estuvo presente en determinadas corrientes de agua (Tabla 3), ocupando el 6,6% del total de medios acuáticos muestreados.

Triturus marmoratus es el urodelo más escaso del Parque, aunque apareció también de forma dispersa por gran parte de él. Se encontró en el 5,0% de los medios acuáticos examinados, con

Figura 5: Riqueza de especies de herpetos en el Parque Natural das Fragas do Eume. Se indica el número de especies de anfibios (a) y de reptiles (b) encontrado en cada cuadrícula UTM de 1 x 1 km.

124

GALÁN

Figura 6: Mapas de distribución de las especies de saurios en el Parque Natural das Fragas do Eume en cuadrículas UTM de 1 x 1 km.

preferencia por diversos tipos de charcas formadas en excavaciones, en zonas de matorral o rocosas, así como en acequias de regadío (Tabla 3).

Las especies de anfibios más escasas, encontradas en menos de 10 cuadrículas de 1 x 1 km, fueron Alytes obstetricans, Bufo calamita e Hyla molleri. Estos tres anfibios se encontraron, de manera muy dispersa, en distintas zonas del Parque, en charcas de diferente naturaleza (Tabla 3; Fig. 4). Alytes obstetricans y B. calamita se hallaron sobre todo en zonas elevadas cubiertas de matorral, ocupando en

su fase acuática charcas de turbera, de matorral o herbazal (Tabla 3). Bufo calamita posee, sin embargo, una notable población (que ocupa, al menos, cuatro cuadrículas de 1 x 1 km) en el extremo norte del Parque, en las zonas de matorral y turbera del monte de Fontardión y su entorno (Fig. 4). Hyla molleri es el anfibio más escaso en el Parque, con sólo seis observaciones en medios acuáticos, concentradas en dos cuadrículas de 1 x 1 km y ninguna observación en hábitats terrestres.

Las zonas de mayor riqueza de especies de

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

anfibios se reparten por diferentes zonas del Parque, como reflejo de su alta heterogeneidad ambiental (Fig. 5a). Sin embargo, destaca su tercio occidental, en el tramo final del río Eume, con cuadrículas de 1 x 1 km que llegan a las nueve especies (entorno del monasterio de Caaveiro) y 10 especies (zona entre A Alameda y Cal Grande, en el Coto de Ombre), donde existen extensas áreas de bosque atlántico en favorable estado de conservación. También aparecen puntualmente zonas de elevada diversidad de anfibios en el extremo norte, con 10 especies en una cuadrícula (en el entorno de O Gallel, zona donde se alternan turberas con áreas de matorral y de bosque) y en el extremo sur, con ocho especies en una cuadrícula, en una zona de pastizales, matorrales y bosques.

Reptiles Las especies encontradas con mayor frecuencia (> 20 cuadrículas de 1 x 1 km) fueron Podarcis bocagei, Iberolacerta monticola, Lacerta schreiberi y Anguis fragilis (Fig. 6).

Podarcis bocagei es el reptil más extendido en el Parque y observado con mayor frecuencia (Fig. 6), asociado a todo tipo de linderos, taludes de tierra y, sobre todo, a muros de construcciones (Tabla 1). Sólo es más escaso en las mesetas del extremo oriental y, naturalmente, en las zonas de baja radiación solar, como en las áreas de bosque denso.

Iberolacerta monticola se encuentra en el Parque asociada a las partes bajas del cañón fluvial del Eume y de sus afluentes, como el Fraibermuz, distribuyéndose en poblaciones aisladas, ligadas a los afloramientos rocosos, taludes de roca o construcciones humanas, en claros en medio del bosque atlántico y de ribera (Tabla 1).

Aparece sobre todo aguas abajo del embalse del

125

Eume. Está ausente o es mucho más escasa en las zonas elevadas de este espacio natural, con cobertura de matorral o repoblaciones de eucalipto, por lo que falta de buena parte de su zona central y de toda la oriental (Fig. 6).

Los otros reptiles frecuentes en el Parque, L. schreiberi y A. fragilis, fueron además los que ocuparon una mayor diversidad de hábitats terrestres (12 de 16; Tabla 1). Lacerta schreiberi, al igual que A. fragilis, se encontró en todo tipo de linderos y claros herbáceos del bosque (aunque predominando el primero en los linderos arbustivos, con Rubus spp., y el segundo en los herbáceos, Tabla 1), frecuentemente en los bordes de caminos y senderos, a lo largo de todo el espacio natural. Ambas especies, como también sucede con I. monticola, pueden ocupar zonas de bosque denso, sobreviviendo en pequeños claros o en sus linderos, si bien a diferencia de I. monticola, también ocupan zonas elevadas de matorral, donde sus poblaciones son abundantes (Fig. 6; Tabla 1).

Los reptiles más escasos (< 12 cuadrículas) fueron Natrix natrix, Vipera seoanei, Coronella austriaca, Timon lepidus, Chalcides striatus y Natrix maura.

El ofidio observado con mayor frecuencia en el Parque fue Natrix natrix, aunque Coronella austriaca y Vipera seoanei también aparecieron distribuidas de forma dispersa por gran parte de él (Fig. 7). Natrix natrix ocupa una amplia variedad de hábitats terrestres (encontrada en 8 de 16, Tabla 1), aunque es más frecuente en los bosques de ribera.

Coronella austriaca y Vipera seoanei también ocupan hábitats muy diversos, especialmente linderos, zonas arbustivas y de matorral.

Timon lepidus y Chalcides striatus son muy escasos en la mayor parte del Parque. Sólo aparecieron de manera muy restringida en sus

126

GALÁN

Figura 7: Mapas de distribución de las especies de ofidios en el Parque Natural das Fragas do Eume en cuadrículas UTM de 1 x 1 km.

zonas periféricas, especialmente en las áreas deforestadas y rocosas con matorral de su extremo norte (monte Fontardión y su entorno, donde hay una población apreciable de C. striatus que ocupa al menos cuatro cuadrículas de 1 x 1 km), así como en unas laderas rocosas con vegetación dispersa, orientadas al sur, próximas al Cañón del Eume (Fig. 6). En este mismo punto, con características ambientales especialmente cálidas y secas debidas a su orientación y escasa cobertura vegetal, se produjo la única observación de Natrix maura (Fig. 7), el reptil más escaso del Parque.

La zona de mayor riqueza de especies de reptiles se sitúa en el entorno de la central hidroeléctrica abandonada de Ventureira, en cuya cuadrícula de 1 x 1 km se han detectado 10 especies diferentes (Fig. 5b).

Otras zonas relativamente diversas en reptiles se han localizado en el entorno de la

presa del embalse del Eume (centro-norte del Parque) y en la zona de A Alameda y su entorno (oeste del Parque).

Amenazas En la Tabla 4 se indican las alteraciones observadas en los puntos de muestreo realizados, tanto en los medios terrestres como acuáticos. En los primeros destaca la elevada proporción de zonas con actividad de jabalí (Sus scrofa), principalmente áreas hozadas con el suelo muy removido e incluso piedras volteadas (encontrándose en una de ellas restos de un A. fragilis parcialmente devorado), así como la presencia de árboles alóctonos, principalmente eucaliptos, el tráfico por pistas y el movimiento de maquinaria (por ejemplo, para efectuar la extracción de los eucaliptos y otros árboles en las labores de tala). En los medios acuáticos,

127

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

Tabla 4: Porcentaje de puntos de muestreo establecidos en los medios terrestres (N total = 669) y acuáticos (N total = 258) dentro de los límites del Parque Natural das Fragas do Eume en los que se observaron los diferentes tipos de alteraciones.

Alteraciones

Medios terrestres

Medios acuáticos

Plantaciones de árboles alóctonos, especialmente eucaliptos

6,9

15,1

Talas de arbolado autóctono

1,8

1,6

Excavaciones y desmontes

2,8

2,3

Abandono del campo: muros cubiertos de maleza

5,8

Abandono del campo: antiguas praderas y herbazales cubiertos de maleza

3,4

Abandono del campo: charcas de manantial o acequias de regadío cubiertas de maleza

3,1

Vertidos de residuos sólidos

5,4

Vertidos de residuos líquidos

0,7

7,4

Agricultura: vertidos de purines en cultivos y herbazales

7,2

22,1

Incendios: zonas quemadas en bosques mixtos y atlánticos

1,2

Incendios: zonas quemadas en áreas de matorral

2,2

Incendios: zonas quemadas en eucaliptales

2,5

Tráfico por pistas, paso de maquinaria

6,7

Obras públicas: acondicionamiento de pistas y carreteras, eliminando vegetación de linderos

3,1

Obras públicas: acondicionamiento de pistas y carreteras, eliminando charcas en cunetas y herbazales Obras públicas: construcciones, rehabilitación de muros de piedra Jabalí (Sus scrofa): zonas hozadas y revolcaderos

las alteraciones más destacadas han sido las producidas por la agricultura y la ganadería (con vertidos de purines o restos de fertilizantes), que afectaron a un elevado número de medios acuáticos muestreados (Tabla 4), así como los vertidos líquidos y los residuos sólidos. Diversas alteraciones afectaron tanto a los medios terrestres como a los acuáticos, destacando las plantaciones de eucaliptos, el tráfico rodado y el paso de maquinaria, el vertido de residuos, las obras públicas (modificaciones en pistas, carreteras, etc.) y el efecto del jabalí

14,0

8,9 2,4 11,8

Visón americano (Neovison vison): observaciones Gato doméstico (Felis silvestris catus): observaciones

10,1

8,9 1,6

2,7

(revolcaderos en charcas y zonas hozadas en la periferia de medios acuáticos, además de en bosques y herbazales) (Tabla 4).

Hay que añadir además el hecho de que un porcentaje muy elevado de los lacértidos del Parque (el 80% o más de los ejemplares de L. schreiberi, I. monticola y P. bocagei hallados en determinadas zonas como Caaveiro, Ventureira, A Ribeira y el perímetro del embalse del Eume), aparecen intensamente parasitados por garrapatas (Ixodes spp.).

128

GALÁN

DISCUSIóN En la herpetofauna del Parque Natural das Fragas do Eume predominan las especies endémicas del noroeste ibérico, tanto de anfibios (C. lusitanica, L. boscai, R. iberica) como de reptiles (P. bocagei, I. monticola, L. schreiberi, V. seoanei), aunque también son abundantes las eurosiberianas de origen centroeuropeo (S. salamandra, L. helveticus, A. obstetricans, B. spinosus, R. temporaria, A. fragilis o C. austriaca). Con respecto a su afinidad biogeográfica, considerados conjuntamente anfibios y reptiles, están presentes siete elementos lusitánicos (los endemismos noroccidentales anteriormente mencionados), cuatro elementos atlánticos, tres ibéricos, tres paleárticos, tres europeos y tres mediterráneos occidentales. En anfibios están presentes en este espacio el 48% de las especies de la península Ibérica, que asciende al 68% si consideramos sólo las de la región Eurosiberiana de ésta (y el 93% de las especies gallegas). En reptiles, este porcentaje desciende al 21% de las especies ibéricas, pero aumenta al 53% al considerar sólo las especies eurosiberianas (y el 40% de las especies de Galicia). Estas cifras son indicativas de la importancia para la herpetofauna de este espacio natural (GALáN REGALADO, 1999).

Anfibios La mayor diversidad se alcanza en los anfibios, donde están presentes todas las especies de Galicia, con la única excepción de Pelobates cultripes, cuya distribución se encuentra muy alejada del Parque (GALáN et al., 2010). Son más abundantes las especies de anfibios que viven o se reproducen en corrientes de agua (muy numerosas en el Parque), escaseando, en general, las especies

dependientes de charcas de tamaño grande, permanentes y con abundante vegetación acuática (muy escasas en el Parque, debido a su peculiar orografía, con fuertes pendientes), como P. perezi, T. marmoratus e H. molleri. El Embalse del Eume no es en la mayor parte de su extensión adecuado para los anfibios, pues sus orillas suelen tener fuertes pendientes, estando cubiertas de vegetación arbórea, sin que se desarrolle una orla de vegetación palustre. Sin embargo, en algunas zonas relativamente limitadas sí aparecen orillas adecuadas, donde se han encontrado poblaciones de alguna de estas especies.

En el uso del espacio durante la fase terrestre de los anfibios, las especies de pequeño tamaño fueron detectadas con muy baja frecuencia en los muestreos nocturnos. Esto es especialmente notorio en el caso de los tritones (Tabla 2), por lo que sus frecuencias de aparición en los hábitats terrestres que muestra esta Tabla son muy bajos y poco realistas, en contraste con otras especies más grandes (S. salamandra, B. spinosus, R. temporaria), mucho más fácilmente detectables en esta fase y cuyo número de observaciones, relativamente elevado, permite una mejor apreciación del uso que hacen de los hábitats en el Parque. En los muestreos en los medios acuáticos sí se pudo localizar a la totalidad de las especies de anfibios y con frecuencias relativamente altas, por lo que la Tabla 3 muestra de manera más realista la utilización de los diferentes puntos de agua para la reproducción que realizan estas especies. Se puede observar en esta Tabla como las escorrentías en cunetas de pistas y carreteras, los arroyos, las acequias, así como las charcas de herbazal y de borde de río, fueron los hábitats acuáticos utilizados por un mayor número de especies de anfibios en el Parque.

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

129

Reptiles

Hábitats importantes

En el caso de los reptiles, las especies más termófilas y xerófilas, como T. lepidus o C. striatus, son muy escasas, debido a las características ambientales que predominan en el Parque (densa cobertura vegetal, elevada humedad edáfica, etc.), excepto en su extremo norte (monte de Fontardión y su entorno), donde existen extensas zonas abiertas de matorral y C. striatus es relativamente abundante. Natrix maura es extremadamente escasa, posiblemente por la causa anteriormente mencionada y encontrarse aquí en el extremo norte de su distribución en Galicia (PRIETO ESPIñEIRA, 2011). No se detectó a Coronella girondica, presente en zonas próximas más termófilas (ASENSI CABIRTA, 2011).

Aunque la mayor parte de los mapas presentados subestiman la presencia de las diferentes especies, por las dificultades de muestreo debidas a las características de este Parque (densa e intrincada cobertura vegetal y compleja orografía), en el caso de determinadas especies esta subestimación es más acusada. Esto sucede en todos los ofidios (excepto N. maura, sumamente escasa) y, especialmente, en A. fragilis y L. schreiberi.

Es muy probable que estas especies, y muy destacadamente los dos saurios, se encuentren presentes en la mayor parte de las Fragas do Eume, muy posiblemente en todas las cuadrículas. Esto se puede apreciar fácilmente en el caso de A. fragilis, que pasa frecuentemente desapercibido por sus costumbres ocultas, pero cuando una zona de las Fragas ha sido visitada con mucha asiduidad (como ha ocurrido en su extremo occidental), el lución aparece en todas las cuadrículas muestreadas (Fig. 6).

Se ha comprobado el elevado valor de los bosques de ribera como hábitat, tanto para los anfibios (ocho especies detectadas en ellos) como para los reptiles (siete especies, Tablas 1 y 2). Estos bosques muestran en la actualidad un grado de deforestación menor que el de los robledales, y cubren el 76% de la longitud de los cauces dentro del Parque (TEIXIDO et al., 2009, 2010).

Determinados hábitats de origen antrópico son de elevado valor para la herpetofauna.

Los herbazales húmedos (generalmente praderas de siega), las acequias de regadío en prados y los depósitos de agua abiertos son muy importantes para los anfibios, mientras que los muros de construcciones y los taludes de pistas o carreteras lo son para los reptiles. La especie de reptil más amenazada del Parque, I. monticola, mantiene algunas de sus mejores poblaciones asociadas a antiguas construcciones humanas (como el monasterio de Caaveiro, la abandonada central hidroeléctrica de Ventureira o determinadas aldeas, como Fragachá), que le proporcionan sustratos favorables y zonas soleadas donde termorregular en áreas densamente forestadas. Sin embargo, el abandono del campo por parte de la población rural hace que muchos de esos hábitats acaben siendo inadecuados para la herpetofauna, al cubrirse de maleza tanto los muros de piedra como los herbazales de siega o las antiguas acequias de regadío. Este fenómeno se encuentra muy extendido en el Parque en la actualidad (Tabla 4). Por otro lado, determinados trabajos de restauración de antiguas construcciones las convierten también en inhabitables para la herpetofauna. Un claro ejemplo de esto es la rehabilitación del monas-

130

GALÁN

terio de Caaveiro, que ha reducido de manera extrema a una de las mejores poblaciones de I. monticola que existía en el Parque.

Amenazas Una de las principales amenazas para este espacio que se ha podido comprobar es la penetración de los cultivos de Eucalyptus en él.

En la actualidad estas plantaciones arbóreas se encuentran en muchas zonas, tanto como monocultivos como intercaladas entre las masas de bosque atlántico original. Las plantaciones de eucaliptos suponen un claro impacto ambiental, eliminando la vegetación autóctona, entre otros efectos negativos (CORDERO RIVERA, 2012, y referencias citadas en ese artículo). En el caso de las Fragas do Eume, estas plantaciones han incrementado su superficie en un 197% entre 1957 y 2003; paralelamente, los bosques autóctonos han mostrado un fuerte declive en esta zona, representando en la actualidad sólo el 30% de su superficie según TEIXIDO et al. (2010).

Estos autores comprueban que las pérdidas de bosques autóctonos se deben principalmente a las plantaciones de eucaliptos. La fragmentación de las masas forestales también se ha incrementado muy notablemente en el período 1957-2003 (TEIXIDO et al., 2010). En la actualidad, los bosques originales se distribuyen en el Parque en tres parches de gran tamaño, existiendo un elevado número de parches muy pequeños (< 10 ha), donde es muy escasa o nula la superficie no afectada por los efectos de borde (TEIXIDO et al., 2009).

Además de la pérdida y de la fragmentación del hábitat, las plantaciones de eucaliptos incrementan notablemente el riesgo de incendios forestales, al tratarse de una especie

pirófita con una gran capacidad de propagar el fuego. Precisamente el 31 de marzo de 2012 se inició un incendio en una de estas plantaciones de eucaliptos que, favorecido por el viento, penetró en el Parque afectando a 370 ha de su parte central (Fig. S3). Los eucaliptos mezclados con el bosque atlántico favorecieron la penetración del fuego, que arrasó una parte significativa del suelo de los bosques de su zona central, entre el monasterio de Caaveiro y el Cañón do Eume (Fig. S3). El impacto de este incendio sobre la herpetofauna se está estudiando en la actualidad. Un año después del fuego, una de las consecuencias más evidentes es el intenso rebrote y germinación de los eucaliptos (Fig. S3).

Otra amenaza para la biodiversidad del Parque es el proyecto de construcción de una mina de andalucita a cielo abierto en su periferia norte (zona de Pico Vello), que puede afectar también al interior del espacio protegido y originar contaminación en las aguas por los efluentes.

A pesar del aparente favorable estado de conservación de este espacio (salvo lo ya comentado de la presencia de Eucalyptus y sus consecuencias), tanto en los medios terrestres como en los acuáticos se observó un cierto número de alteraciones, siendo las más destacadas las producidas por las actividades de los jabalíes, la agricultura y la ganadería (con vertidos de purines o restos de fertilizantes), así como la silvicultura, el tráfico rodado y el paso de maquinaria pesada, la presencia de residuos sólidos, las obras públicas (modificaciones en pistas, carreteras, etc.) y los vertidos líquidos. El río Eume sufre una importante contaminación derivada de vertidos que han incrementado notablemente la acidez de sus aguas (L AGARES & GAGO, 2008; PITA-

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

PARADA, 2009), lo que condiciona gravemente la presencia de anfibios en él.

Lo angosto del valle fluvial donde se sitúa gran parte de este Parque, con pendientes muy pronunciadas en las laderas, hace que los medios acuáticos lénticos sean muy escasos y sólo se originen en algunas zonas bajas. Muchas veces, únicamente se encuentran encharcamientos en las cunetas de las carreteras y pistas de este Parque, como por ejemplo, en la vía que une Pontedeume con el monasterio de Caaveiro, una de las más transitadas. Tales medios son imprescindibles para la reproducción de muchas especies de anfibios de la zona (L. boscai, L. helveticus, D. galganoi, R. temporaria), que no pueden hacerlo en medios lóticos.

Las obras públicas realizadas para la mejora de estas vías pueden eliminar estas charcas de cuneta, con la consiguiente eliminación de las poblaciones de anfibios que se reproducían en ellas, como hemos comprobado en otro espacio natural cercano (GALáN, 2011a).

También en la carretera mencionada se produce un elevado número de atropellos de anfibios (especialmente de S. salamandra y B. spinosus, aunque también de otras especies como C. lusitanica o las tres especies de tritones). Esta mortalidad es especialmente notable durante las noches otoñales lluviosas (cuando hemos contabilizado más de un centenar de S. salamandra atropelladas en los 9 km de esta carretera) y en el mes de marzo, cuando la especie más afectada es B. spinosus. En cuanto a las especies animales invasoras que pueden afectar a los herpetos, hemos detectado la presencia de Neovison vison, tanto en el río Eume como en uno de sus afluentes, en cuatro puntos de muestreo. Este mustélido puede incidir negativamente sobre las poblaciones de anfibios, como se ha comprobado en otras zonas

131

(PALAzóN & RUIz-OLMO, 1997; MELERO & PALAzóN, 2011), incluyendo Galicia (GALáN, 1997; ROMERO, 2007). Igualmente preocupante, si no más, es el incremento poblacional del jabalí (S. scrofa), que conlleva un marcado efecto negativo sobre las poblaciones de herpetos (JOLLEY et al., 2010). Hemos encontrado extensas zonas hozadas a lo largo de pistas y senderos, así como revolcaderos en charcas de herbazal donde se reproducían diversas especies de anfibios (Tabla 4), aunque no hemos evaluado su efecto sobre ellos. Sin embargo está bien documentado que estas actividades del jabalí son muy negativas para la fauna y flora (MASSEI & GENOV, 2004; JOLLEY et al., 2010), por lo que, muy probablemente, este suido supone una amenaza muy importante para los herpetos de la zona, como sucede en otros espacios naturales de Galicia (GALáN, 2012b).

Sobre la infestación por Ixodes spp. que muestran un alto porcentaje de los lacértidos del Parque, es posible que esté relacionada con la elevada densidad de determinados ungulados, tanto domésticos (sobre todo cabras cimarronas, Capra aegagrus hircus) como salvajes (corzos, Capreolus capreolus, y jabalíes principalmente, aunque también ciervos, Cervus elaphus). Las poblaciones de estos mamíferos han experimentado un incremento muy notable en el Parque en las últimas décadas (P. Galán, datos no publicados; L. Costa, comunicación personal) y son portadores de garrapatas, aunque desconocemos si ésta es la causa de la parasitación observada en los reptiles y las consecuencias que puede tener sobre su salud.

Las obras de remodelación de construcciones de piedra afectan a las poblaciones de I. monticola, como hemos comprobado en las

132

GALÁN

realizadas en el monasterio de Caaveiro y otras zonas (GALáN, 2012a). Por otro lado, la sucesión natural de la vegetación tiende a eliminar los claros en el bosque y a cubrir los linderos, erradicando poblaciones de reptiles como I. monticola, L. schreiberi y A. fragilis, entre otras especies. éste es un factor muy a tener en cuenta en estas zonas de clima Atlántico, donde el crecimiento de la vegetación arbustiva es muy rápido.

Considerada en su conjunto, la diversidad de anfibios y reptiles de este Parque es muy elevada (sobre todo de los primeros), acogiendo además a cinco especies catalogadas como vulnerables en Galicia (cuatro anfibios: C. lusitanica, H. molleri –antes H. arborea–, R. iberica y R. temporaria, y un reptil: I. monticola). Su singularidad biogeográfica, ecológica y paisajística es además muy alta, aunque también lo son las amenazas que sufre, derivadas principalmente de la estructura de la propiedad del terreno (con múltiples propietarios, extendidos a lo largo de cinco ayuntamientos, fruto de una tradición minifundista, que a menudo se oponen frontalmente a la consideración de espacio protegido). Esto complica su gestión y las medidas de conservación, así como favorece las plantaciones de eucaliptos (frecuentemente demandadas por los propietarios de los terrenos, que al no estar sometidos a usos agrícolas o ganaderos, los consideran “improductivos”), que eliminan los bosques autóctonos y facilitan la propagación del fuego. Confiemos que prevalezcan los valores de conservación de este importante patrimonio natural, dedicando la Administración la atención que se merece esta parte de su biodiversidad y controle la expansión de la vegetación alóctona, impidiendo nuevos incendios como el del pasado año.

Implicaciones para la conservación En la herpetofauna del Parque Natural das Fragas do Eume están presentes cinco especies (cuatro anfibios y un reptil) consideradas como vulnerables en la legislación autonómica de Galicia (CONSELLERÍA DE MEDIO AMBIENTE E DESENVOLVEMENTO SOSTIBLE, 2007). Según nuestras observaciones, de todas estas especies, H. molleri presenta sólo poblaciones marginales en el Parque, siendo el anfibio más escaso en él (aunque en la vecindad de este espacio existen poblaciones numerosas, como en Goente, en charcas formadas en canteras abandonadas), mientras que las otras tres especies (C. lusitanica, R. iberica y R. temporaria), por el contrario, tienen poblaciones ampliamente repartidas y localmente numerosas. Sin embargo, en las zonas cubiertas por eucaliptos hemos comprobado que estas especies generalmente no se encuentran presentes, por lo que estas plantaciones representan una seria amenaza para ellas. En el caso de C. lusitanica, VENCES (1993) ya estudió el efecto negativo de las plantaciones de eucaliptos sobre sus poblaciones. En estos casos, las condiciones del medio terrestre se vuelven tan negativas para este anfibio (sobre todo por la pérdida de la humedad del suelo), que queda restringido al cauce de las corrientes de agua, limitando su capacidad de dispersión y disminuyendo su densidad (VENCES, 1993).

El único reptil catalogado como vulnerable presente, I. monticola, se puede considerar como el más amenazado en el Parque, ya que hemos comprobado su distribución en pequeñas poblaciones aisladas, a menudo muy reducidas, y constatado declives importantes en las últimas décadas (GALáN, 2012a). Esta especie posee aquí poblaciones viviendo prácticamente al nivel del mar y en hábitats forestales, muy diferentes a sus

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

característicos medios de montaña (GALáN et al., 2007), lo que le confiere gran singularidad a dichas poblaciones.

Otras especies como B. calamita y A. obstetricans han declinado de forma muy marcada en esta zona, al igual que en otros puntos de Galicia (GALáN, 2008; GALáN et al., 2013), siendo en la actualidad escasos en el Parque. Han aparecido, no obstante, en diversos puntos de este espacio, generalmente en zonas elevadas cubiertas de matorral.

Por todo ello, su situación en este espacio natural parece no diferir de la que poseen en el resto de la zona atlántica gallega (GALáN, 2008; GALáN et al., 2013).

Se han detectado malformaciones en dos especies de anfibios en este espacio natural: un adulto de T. marmoratus con polimelia en la extremidad anterior izquierda y un juvenil de Rana temporaria al que le faltaba la extremidad anterior izquierda, careciendo de datos sobre las causas de estas malformaciones (GALáN, 2011b).

Una de las razones principales de que en este Parque existan zonas en un estado favorable de conservación es la peculiar orografía del terreno, con pendientes muy pronunciadas, que han impedido tanto la explotación agrícola o ganadera en el pasado, como, al menos en parte, la urbanización o la creación de infraestructuras en el presente, como sucede en las áreas circundantes (aunque existe un embalse en medio del Parque, que anegó importantes áreas de bosque). Esto ha permitido que estas masas forestales hayan llegado hasta nuestros días en un estado de conservación favorable y que hayan sobrevivido en ellas numerosas especies relictas, entre las que se encuentran C. lusitanica o I. monticola. Esta zona muestra un gran contraste con las áreas que la rodean,

133

densamente antropizadas y con hábitats muy diferentes, dominados por cultivos, matorrales, eucaliptales y áreas industriales o urbanizadas. Sin embargo, existen otros bosques con características muy similares a los del Eume (termófilos, ubicados en cañones fluviales angostos, con parecida composición botánica) en zonas próximas, como las Fragas del Mandeo, del Belelle o del Sor, que albergan herpetofaunas muy parecidas (P. Galán, datos no publicados), pero son de tamaño mucho más reducido y su grado de alteración es con frecuencia mayor (VALES, 1994, 2012).

Lo que le da originalidad a las Fragas do Eume es su gran extensión relativa (el Parque comprende más de 9000 hectáreas). Sin embargo, este bosque atlántico termófilo no está presente en toda su superficie (Figs. 1, S1) y ello se refleja en la distribución y composición de su herpetofauna. En esta distribución se observa un claro contraste entre la zona central y occidental (con el angosto cañón fluvial y los bosques densos y, en general, bien conservados) y su tercio oriental (con mesetas cubiertas de matorral y plantaciones de eucaliptos, en ocasiones muy extensas). En esta última zona no están presentes, por sus características ambientales, C. lusitanica o I. monticola, escaseando también otras especies como R. iberica o P. bocagei.

Agradecimiento Deseo expresar mi agradecimiento a todo el personal del Parque Natural das Fragas do Eume, que me proporcionó los permisos para realizar los muestreos y me prestó su colaboración en todo momento; muy especialmente a Luis Costa Pérez, su director durante muchos años, y a Rogelio Fernández Díaz, anterior direc-

134

GALÁN

tor. Varios investigadores me han acompañado en diferentes épocas en los muestreos realizados; quiero destacar especialmente la colaboración de Ricardo Ferreiro Sanjurjo, Cristina Brea Portela, Pablo Serantes Gómez, Marta Rúa, Victoria Valero Arijón, Marián Gómez, Silvia Rodríguez Fernández y Gloria Tubío Gómez.

REFERENCIAS ASENSI CABIRTA, M. (2011). Cobra lagarteira meridional Coronella girondica (Daudin, 1803), In Sociedade Galega de Historia Natural (ed.) Atlas dos Anfibios e Réptiles de Galicia. Sociedade Galega de Historia Natural, Santiago de Compostela, España, pp. 90-91.

BASELGA, A. & NOVOA, F. (2008). Coleoptera in a relict forest of Spain: implications of hyperdiverse taxa for conservation strategies. Annals of the Entomological Society of America 101: 402-410.

CARAMELO REGO, C.; MARTÍNEz MARTÍNEz, P.; REIRIz VARGAS, S. & VALES MOSQUERA, E. (1995). Espacios Naturais de Galicia. 1. Provincia de A Coruña.

Bahía Edicións. A Coruña, España.

CONSELLERÍA DE MEDIO AMBIENTE E DESENVOLVEMENTO SOSTIBLE (2007).

Decreto 88/2007 do 19 de abril, polo que se regula o Catálogo galego de especies ameazadas. Diario Oficial de Galicia 89: 7409-7423.

CORDERO RIVERA, A. (2012). Bosques e plantacións forestais: dous ecosistemas claramente diferentes. Recursos RuraisSerie Cursos 6: 7-17.

COSTA TENORIO, M.; MORLA JUARISTI, C. & SAINz OLLERO, H. (1997). Los Bosques Ibéricos. Una Interpretación Geobotánica.

Planeta, Barcelona, España.

CASTRO, A. (1977). Sobre os vertebrados da Fraga de Caaveiro. Braña, Boletín da Sociedade Galega de Historia Natural 1: 105-116.

FERNáNDEz DÍAz, R. & NEGREIRA SOUTO, M. (2005). Parque Natural Fragas do Eume, In A. Cordero Rivera, R. Barreiro Lozano (coords.) & y F. Rodríguez Iglesias (ed.)

Conservación II. Serie: Proyecto Galicia.

Ecología, vol. 46. Hércules de Ediciones, A Coruña, España, pp. 146-181.

GALáN, P. (1997). Presencia de poblaciones asilvestradas de visón americano (Mustela vison Schreber, 1777) en La Coruña (NO España). Galemys 9: 35-37.

GALáN, P. (2008). Cambios en la presencia del sapo partero común (Alytes obstetricans) en diferentes períodos y medios acuáticos: posible declive de la especie en Galicia.

Boletín de la Asociación Herpetológica Española 19: 107-113.

GALáN, P. (2009). Plan de Conservación de los Anfibios Amenazados de Galicia. Informe inédito, Dirección Xeral de Conservación da Natureza, Xunta de Galicia.

GALáN, P. (2011a). El impacto sobre los anfibios de pequeñas obras públicas en espacios naturales protegidos. Boletín de la Asociación Herpetológica Española 22: 138-143.

GALáN, P. (2011b). Anfibios con malformaciones en el Parque Natural das Fragas do Eume (A Coruña, Galicia). Boletín de la Asociación Herpetológica Española 22: 65-67.

GALáN, P. (2012a). Distribución de Iberolacerta monticola en la provincia de A Coruña (Galicia, Noroeste de España). Supervivencia de un relicto climático. Boletín de la Asociación Herpetológica Española 23: 81-87.

GALáN, P. (2012b). Pelobates cultripes (western Spadefoot Toad). Depredation.

Herpetological Review 43: 467-468.

DE

HERPETOFAUNA DEL PARQUE NATURAL FRAGAS DO EUME

GALáN, P.; VILA, M.; REMóN, N. & NAVEIRA, H.F. (2007). Caracterización de las poblaciones de Iberolacerta monticola en el Noroeste ibérico mediante la combinación de datos morfológicos, ecológicos y genéticos.

Munibe (Suplemento/Gehigarria) 25: 34-43.

GALáN, P.; CABANA, M. & FERREIRO, R. (2010).

Estado de conservación de Pelobates cultripes en Galicia. Boletín de la Asociación Herpetológica Española 21: 90-99.

GALáN, P.; RODRÍGUEz, S. & TUBÍO, G. (2013). Aproximación al conocimiento del estado de conservación de Bufo calamita en Galicia. Boletín de la Asociación Herpetológica Española 24: 95-101.

GALáN REGALADO, P. (1999). Conservación de la Herpetofauna Gallega. Situación Actual de los Anfibios y Reptiles de Galicia. Universidade da Coruña, A Coruña, España.

GONzáLEz, I.; FERNáNDEz, R. & SALVADORES, R. (1995). Guía de Espacios Naturais de Galicia. Galaxia, Vigo, España.

IzCO, J.; AMIGO, J. & GUITIáN, J. (1990).

Los robledales galaico-septentrionales.

Acta Botanica Malacitana 15: 267-276.

JOLLEY, D.B.; DITCHKOFF, S.S.; SPARKLIN, B.D.; HANSON, L.B.; MITCHELL, M.S. & GRAND, J.B. (2010). Estimate of herpetofauna depredation by a population of wild pigs. Journal of Mammalogy 91: 519-524.

LAGARES, V. & GAGO, X.V. (2008). Un vertido al Eume altera la acidez del río y causa la muerte de cientos de peces. La Voz de Galicia 21/06/2008. Disponible en http://www.lavozdegalicia.es/galicia/2008/06/21/0003_6924206.htm.

Consultado el 25/02/2013.

LEIRO, A.; DAPORTA, M. & CAAMAñO RIVAS, V.M. (2003). Espazos Naturais. Provincia da Coruña. Promocións Culturais Galegas,

135

Vigo, España.

LóPEz DE SILANES, M.E. (1988). Flora Liquénica de la Fraga de Caaveiro, A Coruña. Tesis Doctoral, Universidad de Santiago de Compostela, Santiago de Compostela, España.

LOSA QUINTANA, J.M. (1973). Estudio de las comunidades arbóreas naturales de la cuenca media del Río Eume (La Coruña).

Trabajos Compostelanos de Biología 3: 1-63.

MASSEI, G. & GENOV, P.V. (2004). The environmental impact of wild boar. Galemys 16: 135-145.

MELERO, Y. & PALAzóN, S. (2011). Visón americano – Neovison vison (Schreber, 1777), In A. Salvador & J. Cassinello, J. (eds.) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid, España.

Disponible en http://www.vertebradosibericos.org/mamiferos/pdf/neovis.pdf.

Consultado el 18/05/2013.

MOURIñO LOURIDO, J.; OTERO PéREz, X.L.; SALVADORES RAMOS, R.; ALONSO IGLESIAS, P.; SIERRA-ABRAÍM, F.; ARCOS FERNáNDEz, F. & VázQUEz, A. (2004). Os Espazos Naturais de Galicia. Nigratrea, Vigo, España.

NOVOA, F.; BASELGA, A.; GONzáLEz, J. & CAMPOS, A. (2003). Coleópteros del Parque Natural de las Fragas del Eume (Galicia, noroeste de la Península Ibérica), I: Adephaga, Hydrophiloidea y Staphilinoidea. Boletín de la Asociación Española de Entomología 27: 71-91.

PALAzóN, S. & RUIz-OLMO, J. (1997). El Visón Europeo (Mustela lutreola) y el Visón Americano (Mustela vison) en España.

Organismo Autómono de Parques Nacionales, Ministerio de Medio Ambiente, Madrid, España.

136

GALÁN

P ITA -PARADA , R. (2009). El tratamiento en el río Eume frena los síntomas, pero no la enfermedad. La Voz de Galicia 04/04/2009. Disponible en http://www.lavozdegalicia.es/galicia/2009/04/04/0003_7633572.htm.

Consultado el 25/02/2013.

PRIETO-ESPIñEIRA, X. (2011). Cobra viperina Natrix maura (Linnaeus, 1758), In Sociedade Galega de Historia Natural (ed.)

Atlas dos Anfibios e Réptiles de Galicia.

Sociedade Galega de Historia Natural, Santiago de Compostela, España, pp. 94-95.

PULGAR SAñUDO, I.; AMIGO VázQUEz, J. & GIMENEz DE AzCáRATE CORNIDE, J. (2006). Guía da flora do Parque Natural Fragas do Eume. Xunta de Galicia, Dirección Xeral de Conservación da Natureza, A Coruña, España.

QUINTANILLA, L.G. (1997). Distribución de los Helechos Relictos Macaronésicos en el Parque Natural Fragas do Eume (A Coruña).

Importancia Biogeográfica en la Pteridoflora de Galicia. Tesis de Licenciatura, Universidad de Santiago de Compostela, Santiago de Compostela, España.

QUINTANILLA, L.G. & AMIGO, J. (1999).

Catálogos de las pteridofloras de los espacios naturales protegidos de Galicia.

Botanica Complutensis 23: 99-110.

REINOSO FRANCO, J. (1984). Contribución al conocimiento de la flora briofítica de Galicia.

Briófitos de la Fraga de Caaveiro (La Coruña), I. Musgos. Lazaroa 6: 237-247.

REINOSO FRANCO, J. (1985). Contribución al conocimiento de la flora briofítica de Galicia.

Briófitos de la fraga de Caaveiro. II. Hepáticas.

Acta Botanica Malacitana 10: 17-26.

RIVAS-MARTÍNEz, S. (1987). Memoria del Mapa de Series de Vegetación de España.

ICONA, Ministerio de Agricultura, Pesca y Alimentación, Madrid, España.

ROMERO, R. (2007). El Visón Americano (Mustela vison) y la Nutria (Lutra lutra) en la Isla de Sálvora. Informe inédito, Ministerio de Medio Ambiente, Organismo Autónomo Parques Nacionales, Parque Nacional das Illas Atlánticas.

TEIXIDO, A.L.; QUINTANILLA, L.G. & CARREñO, F. (2009). Fragmentación del bosque y pérdida del hábitat de helechos amenazados en el Parque Natural Fragas do Eume (Nw de España). Ecosistemas 18: 60-73.

T EIXIDO , A.L.; Q UINTANILLA , L.G.; CARREñO, F. & GUTIéRREz, D. (2010).

Impacts of changes in land use and fragmentation patterns on Atlantic coastal forest in northern Spain.

Journal of Environmental Management 91: 879-886.

VALES, C. (1994). Proposta de creación da Reserva da Biosfera das Fragas do Eume, In A. Craig, A. Fernández, J. Izco, J. Loidi, D. Oliver, G. Peterken, J. Timbal & C. Vales (eds.). Os Bosques Atlánticos Europeos. Bahía Edicións, A Coruña, España, pp. 183-243.

VALES, C. (2012). Lume nas fragas do Eume. La Voz de Galicia 03/04/2012. Disponible en http://www.lavozdegalicia.es/noticia/opinion/2012/04/03/lume-nas-fragas-doeume/0003_201204G3P18992.htm.

Consultado el 03/04/2012.

VENCES, M. (1993). Habitat choice of the salamander Chioglossa lusitanica: the effects of eucalypt plantations. AmphibiaReptilia 14: 201-212.

Basic and Applied Herpetology 28 (2014): 137-143

Variation in the erythrocyte size among larvae, juveniles and adults of Hypsiboas cordobae (Anura, Hylidae) Mariana Baraquet*, Nancy Edith Salas, Adolfo Ludovico Martino Ecología, Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, Córdoba, Argentina. * Correspondence: Ecología, Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto. Ruta Nacional N° 36 - km 601, (X5804BYA) Río Cuarto, Córdoba, Argentina. Phone: +54 358 4676167, Fax: +54 358 4676230, E-mail: mbaraquet@exa.unrc.edu.ar

Received: 29 November 2012; received in revised form: 31 May 2013; accepted: 18 June 2013.

we aimed at determining sizes and shape of erythrocytes and evaluating the differences among larva, juvenile and adult Hypsiboas cordobae. Length and width of 40 randomly chosen erythrocytes and their respective nuclei from individuals of different ages collected in the experimental field “Las Guindas” (Córdoba, Argentina) were measured. Erythrocyte and nuclear areas were estimated assuming an ellipsoidal shape, and the aspect ratio, which reflects the shape of the cell, was calculated. The erythrocytes were oval, and their nuclei were also oval and centrally located. Erythrocyte size increased with age, whereas nuclei were larger in tadpoles than in juveniles. The cell and nucleus shapes also changed with age from the spherical shape in larvae to the more ellipsoidal one in adults. Discriminant analysis confirmed the existence of highly significant (P < 0.0001) differences in erythrocyte and nuclear areas among larvae, juveniles and adults, with a classification rate of 93.33%.

Key words: age-related differences; erythrocyte; haematology; Hypsiboas cordobae.

Variación en el tamaño de los eritrocitos entre larvas, juveniles y adultos de Hypsiboas cordobae (Anura, Hylidae). Determinamos el tamaño y forma de los eritrocitos de Hypsiboas cordobae, evaluando las diferencias entre larvas, juveniles y adultos. Medimos la longitud y anchura de 40 eritrocitos seleccionados aleatoriamente en individuos de diferentes edades colectados en el campo experimental “Las Guindas” (Córdoba, Argentina). Estimamos las áreas de los eritrocitos y de sus núcleos asumiendo formas elipsoidales, y calculamos la razón de aspecto, indicativa de la forma de la célula. Tanto los eritrocitos como los núcleos mostraron forma ovalada, apareciendo los últimos en posición central. El tamaño de los eritrocitos aumentó con la edad, mientras que los núcleos fueron mayores en larvas que en juveniles. Las formas tanto de la célula como del núcleo también cambiaron con la edad, siendo esféricas en larvas y más ovaladas en adultos. Mediante un análisis discriminante confirmamos la existencia de diferencias altamente significativas (P < 0.0001) entre larvas, juveniles y adultos en las área de eritrocitos y núcleos, con una tasa de clasificación del 93.33%.

Key words: diferencias relacionadas con la edad; eritrocitos; hematología; Hypsiboas cordobae.

The majority of studies in haematology of anurans are limited to blood cell counts (ATATüR et al., 1998, 1999; DöNMEz et al., 2009) and erythrocyte size determination (HARTMAN & LESSLER, 1964; MATSON, 1990; ATATüR et al., 1998, 1999, 2001; zHELEV et al., 2006; GAO et al., 2007; DOI: http://dx.doi.org/10.11160/bah.12010/

GRENAT et al., 2009A,B), while studies on cell size variation among larvae, juveniles and adults are very scarce. One of the most important functions of erythrocytes is to carry oxygen and carbon dioxide, and their size and shape are indicators of the area available for gas exchange. For instance, a small

138

SHORT NOTES

erythrocyte possesses a comparatively greater rate of exchange than a large one. The study of erythrocytes in different species provides an interesting comparison of the erythrocyte size in relation to activity and habitat (HARTMAN & LESSLER, 1964; MARTÍNEz et al., 1985; SEVINç et al., 2000; wOJTASzEK & ADAMOwICz, 2003). Amphibians show an extensive range in erythrocyte sizes, being these relatively large in comparison with other vertebrates (DUELLMAN & TRUEB, 1994; GREGORY, 2001; CAMPBELL, 2004, 2012).

Little is known about the relationship between ontogenetic growth and erythrocyte size, which could be relevant to organism biology especially in animals such as amphibians that have indeterminate growth (DAVIS, 2008; ARIKAN & çIçEK, 2011). Amphibian larval growth and metamorphosis have effects on blood cells such as erythrocytes (DAVIS, 2009; DAS & MAHAPATRA, 2012). As part of the changes happening during metamorphosis involving the substitution of specific larval organs or cells by adult ones (OHMURA & wAKAHARA, 1998), larval erythrocytes are replaced by adult ones (DORN & BROYLES, 1982; YAMAGUCHI & wAKAHARA, 1997; TAMORI & wAKAHARA, 2000; wAKAHARA & YAMAGUCHI, 2001). Consequently, larval and adult erythrocytes differ in size and morphology, being large and elongated in larvae and smaller and rounder in adults (BENBASSAT, 1974; DAVIS, 2008).

In the present paper we examine and evaluate differences in morphology and size of erythrocytes of larvae, juveniles and adults Hypsiboas cordobae (Barrio, 1965). Hypsiboas cordobae is restricted to highlands of Córdoba and San Luis provinces, in central Argentina (BARRIO, 1965; FAIVOVICH et al., 2004). This

restricted distribution with a broad altitudinal range, its consideration by the IUCN Red List of Threatened Species as a taxon of Data Deficient, and the lack of information about its haematology make it an interesting species for study.

A total of 46 individuals of H. cordobae were collected from the experimental field “Las Guindas” (Alpa Corral, province of Córdoba, Argentina, 32º35’35.22’’ S, 64º42’38.92’’w; 930 m above sea level) in October and November months between 2007 and 2009. These included 15 tadpoles in stages 35 to 39 according to GOSNER (1960), 10 recently metamorphosed individuals (hereafter juveniles) with the tail completely reabsorbed obtained from captive-raised larvae, and 21 adults. Blood samples were obtained by angularis vein puncture in juveniles and adults (NöLLER, 1959), and directly from the heart after anaesthesia via immersion in 1% tricaine methanesulfonate in larvae. Smears of fresh blood were air-dried and stained with a 10% solution of Giemsa for 5 min.

Slides were observed under a trinocular microscope Primo Star (Pack 5) and the image processing software AxioVision 4.8 (Carl zeiss, Oberkochen, Germany). The photographs were used to measure erythrocytes with Adobe Photoshop 9.0 (Adobe Systems, San Jose, California, USA). On each blood smear, length (L) and width (w) of 40 randomly chosen erythrocytes and their respective nuclei were measured using a scale of 20 microns as a reference. Erythrocyte and nuclear areas were calculated assuming an ellipsoid shape according to the formula L x w x p / 4. we compared each variable among larvae, juveniles and adults using analyses of the variance (ANOVAs) followed by Tukey's

139

SHORT NOTES

HSD post hoc comparisons. Then, we used a discriminant function analysis to know the variables that better defined the variation among these groups.

Adult individuals showed the largest erythrocyte and nucleus areas (Table 1; Erythrocyte area: F2,43 = 35.69, P < 0.0001.

Nucleus area: F2,43 = 9.13, P = 0.0005). Larval nuclei were larger than juvenile ones, whereas the opposite was true for erythrocyte size (Table 1), although in the latter case differences among age groups were not significant.

The L / w ratio results revealed significant differences among age groups in shape of both erythrocytes (F2,43 = 5.48, P = 0.0077) and nucleus (F2,43 = 43.05, P < 0.0001). For both parameters, adults showed oval or elliptical shapes while in larvae they were rounder or more spherical (L / w closer to one, Table 1).

In juveniles, erythrocyte shape was similar as in larvae while nucleus shape resembled that of adults.

Discriminant analysis based on length and width of erythrocytes and nuclei yielded two highly significant functions (P < 0.0001).

The first function, with an eigenvalue of 6.12, explained 89.26 % of the observed variation. The high canonical correlation

(0.92715) indicated a high weight of the function, while the low wilks’ Lambda (0.08084) indicated that the two selected variables (length and width of nuclei) were appropriate for discriminating age groups (Fig. 1). A total of 93.33% of the cases was correctly classified (100% of larvae, 90% of juveniles and 90.48% of adults).

Our results showing differences in erythrocyte and nuclear size and shape among larvae, juveniles and adults agree with previously reported differences between larval and adult erythrocytes in amphibians. Many studies report that during metamorphosis, larger and elongated erythrocytes of larvae are replaced by smaller and rounder cells in adults (BENBASSAT, 1974; BROYLES, 1981; DORN & BROYLES, 1982; DUELLMAN & TRUEB, 1994; YAMAGUCHI & wAKAHARA, 1997, 2001; HASEBE et al., 1999; DAVIS, 2008; ARIKAN & çIçEK, 2011; CAMPBELL, 2012). However, we observed that the erythrocyte and nuclear sizes in larvae were smaller than in adults, and that both cells and nuclei were more elongated in adults than in larvae.

Our results are in agreement with those by YAMAGUCHI & wAKAHARA (1997) in the salamander Hynobius retardatus, who found

Table 1: Mean  standard deviation of erythrocyte and nuclear measurements of larvae (N = 15), juveniles (N = 10) and adults (N = 21) of Hypsiboas cordobae. Lower case letters indicate different groups defined by post hoc tests (P < 0.05). Lar = Larvae; Juv = Juveniles; Adu = Adults.

Erythrocytes L (mm)

w (mm)

Nuclei

A (mm ) 2

L/w

L (mm)

w (mm)

A (mm2)

L/w

20.47  1.00 13.90  0.45 223.98  16.71a 1.48  0.05

8.22  0.33 6.07  0.19 39.26  2.51b 1.39  0.11

Adu 23.66  1.14 15.06  1.05 280.58  28.22b 1.58  0.10

9.92  0.83 5.55  0.64 43.57  7.91c 1.80  0.14

Lar Juv

20.87  0.84 13.69  0.58 224.73  12.13a 1.53  0.10

8.40  0.63 5.03  0.59 33.38  5.88a 1.69  0.13

140

SHORT NOTES

Figure 1: Representation of the first two canonical functions from the discriminant analysis performed on erythrocyte and nucleus variables of larvae, juveniles and adults of Hypsiboas cordobae.

larger erythrocytes in adults than in larvae.

Furthermore, these authors also showed that in larvae, erythrocyte shape is round or spherical while in adults is oval or elliptical, and indicated that during the transition, erythrocytes showed an intermediate form between typical larval and adult cells, which also coincides with what we have observed in H. cordobae.

Because erythrocytes are responsible for storing and transporting oxygen (HARTMAN & LESSLER, 1964) their characteristics determine in part the efficiency of this transport from respiratory systems to tissues (HOLLAND & FORSTER, 1966). Thus, amphibian erythrocyte size relates to the respiratory needs of the individuals (ARSERIM & MERMER, 2008), and therefore increasing the amount of hemoglobin per cell, as it would happen in larger erythrocytes, would be one way to meet the bodyâ&#x20AC;&#x2122;s increasing demands for oxygen as individuals grow in size.

However, DAVIS et al. (2009) argued that the increased size of erythrocytes with growth might merely reflect the allometric scaling of

body and cells (i.e. as capillary size grows, cell sizes increase).

The age-related variation in erythrocyte morphology clearly warrants further studies to clarify the physiological mechanism involved and the implications of these changes.

Our results may be helpful as reference values for future investigations and could also be used in combination with other hematological parameters for the study about the changes that occur in blood cells during metamorphosis and identifying hematopoietic organs in H. cordobae.

Acknowledgement The first two authors thank the National Scientific and Technical Research Council (CONICET) for support. The Secretary of Science and Technology of National University of RĂ­o Cuarto (SECyT-UNRC) provided funds by Grant PPI 18C/225. we thank P. Grenat and J. Valetti for their help in the field and sample. Our study was authorized by Cordoba Environmental Agency (A.C.A.S.E.).

SHORT NOTES

REFERENCES ARSERIM, S.K. & MERMER, A. (2008).

Hematology of the Uludağ frog, Rana macrocnemis Boulenger, 1885 in Uludağ National Park (Bursa, Turkey). Ege Üniversitesi Su Ürünleri Dergisi 25: 39-46.

ARIKAN, H. & çIçEK, K. (2011). Changes in blood-serum proteins, erythrocyte count, and size of Pelophylax bedriagae (Camerano, 1882) during metamorphosis (Anura: Ranidae). Herpetozoa 24: 3-11.

ATATüR, M.K.; ARIKAN, H. & MERMER, A. (1998). Erythrocyte sizes of some Urodeles from Turkey. Turkish Journal of Zoology 22: 89-91.

ATATüR, M.K.; ARIKAN, H. & çEVIK, İ.E. (1999). Erythrocyte sizes of some anurans from Turkey. Turkish Journal of Zoology 23: 111-114.

ATATüR, M.K.; ARIKAN, H.; çEVIK, İ.E. & MERMER, A. (2001). Erythrocyte measurements of some Scincids from Turkey.

Turkish Journal of Zoology 25: 149-152.

BARRIO, A. (1965). Las subespecies de Hyla pulchella Duméril y Bibron (Anura, Hylidae). Physis 25: 115-128.

BENBASSAT, J. (1974). The transition from tadpole to frog haemoglobin during natural amphibian metamorphosis. I. Protein synthesis by peripheral blood cells in vitro.

Journal of Cell Science 15: 347-357.

BROYLES, R.H. (1981). Changes in the blood during amphibian metamorphosis, In L.I. Gilbert & E. Frieden (eds.) Metamorphosis.

A Problem in Developmental Biology. Plenun Press, New York, pp. 461-490.

CAMPBELL, T.w. (2004). Hematology of Lower Vertebrates. American College of Veterinary Pathologists & American

141

Society for Veterinary Clinical Pathology, Middleton, wisconsin, USA. CAMPBELL, T.w. (2012). Hematology of amphibians, In M.A. Thrall, G. weiser, R. Allison & T.w. Campbell (eds.)

Veterinary Hematology and Clinical Chemistry, 2nd ed. wiley-Blackwell, Ames, Iowa, pp. 313-317.

DAS, M. & MAHAPATRA, P.K. (2012). Blood cell profiles of the tadpoles of the Dubois’s tree frog, Polypedates teraiensis Dubois, 1986 (Anura: Rhacophoridae). Scientific World Journal 2012: 701746.

DAVIS, A.K. (2008). Ontogenetic changes in erythrocyte morphology in larval mole salamanders, Ambystoma talpoideum, measured with image analysis. Comparative Clinical Pathology 17: 23-28.

DAVIS, A.K. (2009). Metamorphosis-related changes in leukocyte profiles of larval bullfrogs (Rana catesbeiana). Comparative Clinical Pathology 18: 181-186.

DAVIS, A.K.; MILANOVICH, J.R.; DEVORE, J.L. & MAERz, J.C. (2009). An investigation of factors influencing erythrocyte morphology of red-backed salamanders (Plethodon cinereus). Animal Biology 59: 201-209.

DöNMEz, F.; TOSUNOğLU, M. & GüL, ç.

(2009). Hematological values in hermaphrodite, Bufo bufo (Linnaeus, 1758). NorthWestern Journal of Zoology 5: 97-103.

DORN, A.R. & BROYLES, R.H. (1982).

Erythrocyte differentiation during the metamorphic hemoglobin switch of Rana catesbeiana. Proceedings of the National Academy of Sciences 79: 5592-5596.

DUELLMAN, w.E. & TRUEB, L. (1994). Biology of Amphibians. The John Hopkins University Press, Baltimore, Maryland, USA.

142

SHORT NOTES

FAIVOVICH, J.; GARCÍA, P.C.A.; ANANIAS, F.; LANARI, L; BASSO, N.G. & wHEELER, w.C. (2004). A molecular perspective on the phylogeny of the Hyla pulchella species group (Anura, Hylidae). Molecular Phylogenetics and Evolution 32: 938-950.

GAO, z.; wANG, w.; ABBAS, K.; zHOU, X.; YANG, Y.; DIANA, J.S.; wANG, H.; wANG, H.; LI, Y. & SUN, Y. (2007). Haematological characterization of loach Misgurnus anguillicaudatus: Comparison among diploid, triploid and tetraploid specimens.

Comparative Biochemistry and Physiology A 147: 1001-1008.

GOSNER, K.L. (1960). A simplified table for staging anuran embryos and larvae.

Herpetologica 16: 183-190.

GREGORY, T.R. (2001). The bigger the Cvalue, the larger the cell: genome size and red blood cell size in vertebrates. Blood Cells, Molecules, and Diseases 27: 830-843.

GRENAT, P.R.; BIONDA, C.; SALAS, N.E. & MARTINO, A.L. (2009a). Variation in erythrocyte size between juveniles and adults of Odontophrynus americanus.

Amphibia-Reptilia 30: 141-145.

GRENAT, P.R.; SALAS, N.E. & MARTINO, A.L. (2009b). Erythrocyte size as diagnostic character for the identification of live cryptic Odontophrynus americanus and O. cordobae (Anura: Cycloramphidae).

Zootaxa 2049: 67-68.

HARTMAN, F.A. & LESSLER, M.A. (1964).

Erythrocyte measurements in fishes, amphibia, and reptiles. Biological Bulletin 126: 83-88.

HASEBE, T.; OSHIMA, H.; KAwAMURA, K. & KIKUYAMA, S. (1999). Rapid and selective removal of larval erythrocytes from systemic circulation during metamorphosis of the

bullfrog, Rana catesbeiana. Development, Growth & Differentiation 41: 639-643.

HOLLAND, R.A.B. & FORSTER, R.E. (1966).

The effect of size of red cells on the kinetics of their oxygen uptake. Journal of General Physiology 49: 727-742.

MARTÍNEz, F.J.; MENDIOLA, P. & DE COSTA, J. (1985). Parámetros hematológicos de Rana perezi (Amphibia: Salientia). Anales de Biología 5: 73-78.

MATSON, T.O. (1990). Erythrocyte size as a taxonomic character in the identification of Ohio Hyla chrysoscelis and H. versicolor.

Herpetologica 46: 457-462.

NöLLER, H.G. (1959). Eine einfache Technik der Blutentnahme beim Frosch. Pflüger’s Archiv für die Gesamte Physiologie des Menschen und der Tiere 269: 98-100.

OHMURA, H. & wAKAHARA, M. (1998).

Transformation of skin from larval to adult types in normally metamorphosing and metamorphosis-arrested salamander, Hynobius retardatus. Differentiation 63: 237-246.

SEVINç, M.; UğURTAŞ, I.H. & YILDIRIMHAN, H.S. (2000). Erythrocyte measurements in Lacerta rudis (Reptilia, Lacertidae).

Turkish Journal of Zoology 24: 207-209.

TAMORI, Y. & wAKAHARA, M. (2000).

Conversion of red blood cells (RBCs) from the larval to the adult type during metamorphosis in Xenopus: specific removal of mature larval-type RBCs by apoptosis.

International Journal of Developmental Biology 44: 373-380. wAKAHARA, M. & YAMAGUCHI, M. (2001).

Erythropoiesis and conversion of RBCs and hemoglobins from larval to adult type during amphibian development.

Zoological Science 18: 891-904.

SHORT NOTES

wOJTASzEK, J. & ADAMOwICz, A. (2003).

Haematology of the fire-bellied toad, Bombina bombina L. Comparative Clinical Pathology 12: 129-134.

YAMAGUCHI, M. & wAKAHARA, M. (1997).

Hemoglobin transition from larval to adult types occurs within a single erythroid cell population during metamorphosis of the salamander Hynobius retardatus.

International Journal of Developmental Biology 41: 581-589.

143

YAMAGUCHI, M. & wAKAHARA, M. (2001).

Contribution of ventral and dorsal mesoderm to primitive and definitive erythropoiesis in the salamander Hynobius retardatus. Developmental Biology 230: 204-216. zHELEV, z.M.; ANGELOV, M.V. & MOLLOV, I.A. (2006). A study of some metric parameters of the erythrocytes in Rana ridibunda (Amphibia: Anura) derived from an area of highly developed chemical industry. Acta Zoologica Bulgarica 58: 235-244.

144

Basic and Applied Herpetology 28 (2014): 145-151

Data on nesting, incubation, and hatchling emergence in the two native aquatic turtle species (Emys orbicularis and Mauremys leprosa) from Doñana National Park Carmen Díaz-Paniagua*, Ana Cristina Andreu, Adolfo Marco, Marta Nuez, Judith Hidalgo-Vila, Natividad Perez-Santigosa Estación Biológica de Doñana-CSIC, Sevilla, Spain. * Correspondence: Estación Biológica de Doñana-CSIC, Avda. Américo Vespucio s/n, 41092 Sevilla, Spain. Phone: +34 954232340, Fax +34 954 621125, E-mail: poli@ebd.csic.es

Received: 18 June 2013; received in revised form: 2 October 2013; accepted: 4 October 2013.

we monitored reproductive females of Emys orbicularis and Mauremys leprosa during the summer of 2001 in Doñana National Park. Radiographs revealed that females of both species may lay at least two clutches from May to July. we recorded incubation temperatures in one nest of each species, and found them to be 24.7ºC in E. orbicularis and 28.7ºC in M. leprosa. Egg incubation lasted 83 days in E. orbicularis, with all the hatchlings remaining in the nest until we extracted them in October, and 46-53 days in M. leprosa, with three hatchlings emerging one to 12 days after hatching, and three hatchlings remaining in the nest. we detected M. leprosa hatchlings in their first trip to the pond from late August to early October and E. orbicularis hatchlings from September 18th to September 23rd.

Key words: aquatic turtles; incubation; nests; reproduction.

Nidos, incubación y emergencia de crías en las dos especies de quelonios acuáticos (Emys orbicularis y Mauremys leprosa) del Parque Nacional de Doñana. Durante el verano de 2001, se hizo un seguimiento intensivo de hembras grávidas de Emys orbicularis y Mauremys leprosa en Doñana. Mediante radiografías se detectó que ambas especies podían poner al menos dos puestas entre mayo y julio. Se obtuvieron datos sobre la temperatura de un nido de E. orbicularis (temperatura media de incubación = 24,7ºC) y de otro de M. leprosa (Temperatura media de incubación = 28.7ºC). El periodo de incubación de los huevos fue de 83 días en E. orbicularis, manteniéndose las crías dentro del nido tras la eclosión de los huevos hasta que fueron extraídas en octubre. En M. leprosa, la incubación duró entre 46 y 53 días; tres crías emergieron del nido entre uno y 12 días tras la eclosión, y otras tres permanecieron en el interior hasta que fueron extraídas. Además, se detectaron crías de M. leprosa recién nacidas en sus primeros viajes al medio acuático tras la eclosión entre finales de agosto y primeros de octubre, y de E. orbicularis entre el 18 y el 23 de septiembre.

Key words: incubación; nidos; quelonios acuáticos; reproducción.

The European pond turtle (Emys orbicularis) and the Mediterranean pond turtle (Mauremys leprosa) are two autochthonous aquatic turtle species found in the Iberian Peninsula. Currently, the conservation status of the populations of both species in Spain is considered to be vulnerable (PLEGUEzUELOS DOI: http://dx.doi.org/10.11160/bah.13010/

et al., 2002). Information on the reproductive biology of these species is generally sparse, although KELLER (1997) determined their female breeding frequency and clutch size in Doñana National Park (DNP, Huelva, southwest Spain). Referring only to M. leprosa, COMBESCOT (1955) described the gonadal

146

SHORT NOTES

cycle and ANDREU & VILLAMOR (1989) ascertained the timing of main reproductive events. In this study we intensively monitored gravid females of both species in DNP, with the aim of locating their nests and obtaining information about their incubation and hatchling emergence periods.

From May 18th to June 1st of 2001, five E. orbicularis females and 10 M. leprosa females were captured from a pond in DNP. On the day of capture, each female was x-rayed (radiation parameters: 65 mA, 75 kw, 0.5 s) in order to detect eggs in her oviducts and subsequently returned to the pond. The pond was sampled a second time between June 10th and 19th; seven E. orbicularis and nine M. leprosa females were captured, x-rayed, and released.

Of these females, five and seven individuals of each species, respectively, had been x-rayed during the first sampling.

From June 10th to July 26th, we radiotracked (Biotrack 10 Tw-3 single-celled tag radiotransmitters, wareham, Dorsett, UK) four E. orbicularis and two M. leprosa gravid females in order to locate their nests. Their location was determined daily from 7:00 to 0:00 h at intervals of approximately three hours. This monitoring was complemented with the observation of movements of nontagged turtles around the pond. In addition, we conducted during this period intensive nest searches around several ponds. we signalled nests and measured and weighed their eggs with great care. For observation of the eggs, we placed a vertically-oriented glass window in one side of each nest. From mid-August onwards, the nests were monitored daily in order to record hatching and emergence dates, as well as body length and mass of emerged hatchlings. This methodo-

Table 1: Carapace length, body mass and number of shelled eggs (N eggs) detected in seven x-rayed females of Emys orbicularis and 13 x-rayed females of Mauremys leprosa.

Id

1 2 3 4 5 6 7

Emys orbicularis Carapace Body N eggs (X-ray date) length (mm) mass (g) May 14th June 10th 151.9 138.7 146.1 137.9 146.9 154.5 150.9

680 508 637 560 624 693 685

% of egg-bearing females Mean number of eggs per clutch

8 7 6 7 0

83.3 7.0

6 6 8 6 0 5 8

85.7 6.5

Id

1 2 3 4 5 6 7 8 9 10 11 12 13

Mauremys leprosa Carapace Body N eggs (X-ray date) length (mm) mass (g) May 13th-June 1st June 10th-19th 205.3 149.9 173.8 194.2 178.9 185.9 193.2 173.6 205.3 173.6 188.0 196.8 187.9

1120 505 1161 1031 796 868 981 705 1274 705 761 985 826

% of egg-bearing females Mean number of eggs per clutch

9 0 9 9 0 7 7 0 0 0

50.0 8.2

4

0 0 6 0 0 4 6 0 40.0 5.0

147

SHORT NOTES

logy had been successfully used in nests of Testudo graeca (DÍAz-PANIAGUA et al., 1997). we placed a temperature data logger (Tidbit, HOBO, Onset Computer Corporation, Bourne, Massachusetts, USA) within each nest alongside the eggs to record nest temperature every 30 min during the incubation period. On October 18th, after a considerable decrease in ambient temperature, when we considered that embryo development had probably been completed, the remaining eggs and hatchlings were collected from the nests.

From August onwards, we erected a fence with 30 cm of height and 100 m of length along the entrance to the pond where females were collected in order to intercept

hatchlings making their first trip to the pond after emergence. Several pitfall traps were set up along the fence, being checked daily until October.

Results of radiographs to detect gravid females are shown in Table 1. we observed gravid females of both species in May and in June samplings. we detected females with second clutches in both species. we did not see radiotracked females digging nests. we observed only one E. orbicularis female digging a nest and laying eggs on July 7th at 19:30. The nest was close to the pond (Table 2), in an area of wet, compact sand with a thick cover of helophytes. It contained eight eggs, two of which were found broken, and only four of the remaining eggs hatched.

Table 2: Main characteristics of Emys orbicularis and Mauremys leprosa nests monitored in Doñana National Park.

E. orbicularis Clutch date Number of eggs Distance to the shore (m) Vegetation cover Nest width (cm) Nest deptha (mm) Mean (± SD; range) egg length (mm) Mean (± SD; range) egg width (mm) Mean (± SD; range) egg mass (g) Mean (± SD) body mass of hatchlings (g) Mean (± SD) carapace length of hatchlings (mm) Mean (± SD) plastron length of hatchlings (mm) Hatching date Hatching rate Nest emergence date Incubation duration (days) Mean nest temperature in August (ºC) Mean minimum nest temperature in August (ºC) Mean maximum nest temperature in August (ºC) Mean nest temperature until hatching (ºC) Mean minimum temperature until hatching (ºC) Mean maximum temperature until hatching (ºC) a

From soil surface to the bottom of the nest.

July 7th 8 8 thick 7.5 x 7.5 40-68 31.8 (± 0.80; 30.5-33.0) 22.2 (± 3.72; 20.5-31.4) 8.34 (± 0.27; 7.9-8.7) 4.75 (± 0.44) 26.15 (± 0.73) 22.28 (±0.43) September 27th-October 6th 50% Not detected 83 25.38 23.69 27.65 24.67 21.07 27.65

M. leprosa July 15th-22nd 8 25 sparse 18 x 14 90-155 33.7 (± 1.17; 32.0-35.0) 20.7 (± 0.47; 20.1-20.5) 8.43 (± 0.51; 7.9-9.3) 4.55 (±1.43) 27.8 (±0.64) 23.5 (±1.25) September 6th-18th 62.5% September 17th onwards 46-53 29.28 27.12 32.27 28.65 24.44 32.27

148

SHORT NOTES

Figure 1: Variation in mean daily temperature during the incubation period in Emys orbicularis and Mauremys leprosa nests monitored in DoĂąana National Park.

From June 5th to July 25th, we found in the meadows surrounding the pond a total of 70 M. leprosa nests that had been preyed upon, probably by rats according to the pattern of eggshell breakage and the tracks found around the nests. while we were excavating some of the predated nests, we identified three M. leprosa nests whose nesting date was estimated to be after July 15th.

One of them, found on July 27th, contained eight eggs and was intact, while the other two, found on July 26th and 27th, had been partially preyed upon and contained, respectively, two and one intact eggs. These nests were located at 20 to 25 m from the shore of the pond, in open areas characterized by sparse grass vegetation and low substrate moisture. Only eggs in the non-predated nest hatched, so we used only this nest for further analyses on hatching and emergence of M. leprosa (Table 2); one of the eggs in this nest was found broken, while six of the remaining ones hatched.

The size and mass of the eggs, as well as the data on hatching and hatchling emergence are shown in Table 2. The eggs of M. leprosa hatched earlier and had shorter incubation periods than those of E. orbicularis. The variation in mean daily incubation temperature is shown in Fig. 1. Incubation temperature was higher in the M. leprosa nest than in the E. orbicularis nest (Table 2).

Hatchling main biometric parameters are shown in Table 2. In addition to obtaining emergence data from the monitored nests, we also intercepted, using the fence, four E. orbicularis and five M. leprosa hatchlings, as well as three other newborn M. leprosa hatchlings near other ponds (Fig. 2). we intercepted the first M. leprosa hatchlings travelling to the pond in late August and the last one on October 6th.

Emys orbicularis hatchlings were intercepted between September 18 th and September 23rd. In the E. orbicularis nest, all the hatchlings remained in the nest,

SHORT NOTES

149

Figure 2: Number of Mauremys leprosa and Emys orbicularis hatchlings intercepted as they traveled to the pond after emerging from their nests. Dates of hatchling emergence in the monitored M. leprosa nest are also included. In E. orbicularis, no hatchlings emerged from the monitored nest.

meaning that their emergence was delayed at least one month relative to their hatching. In the M. leprosa nest, two hatchlings emerged the day after they hatched, another one 12 days later, and the remaining three did not emerge, meaning that their emergence was delayed longer than one month.

Emys orbicularis and M. leprosa have similar breeding habitats and periods in DNP, although M. leprosa is much more abundant (KELLER et al., 1995). Second clutches were detected in females of both species, being more frequent in E. orbicularis, as found in a previous study (ROQUES et al., 2006). In DoĂąana, only one M. leprosa female had been observed to have a second clutch (ANDREU & VILLAMOR, 1989), even though a large number of females have been intensively monitored (KELLER, 1997). However, PEREz et al.

(1979) suggested that females could be capable of developing up to three clutches per

year, based on an inspection of ovarian follicles. Laying multiple clutches per year is a common reproductive strategy in chelonian species as it increases the reproductive output of females (wILBUR & MORIN, 1988).

In E. orbicularis, females can develop second clutches by fertilizing eggs with stored sperm, and clutches may exhibit multiple paternity (ROQUES et al., 2006).

In this study, radiotracking of gravid females was not adequate for nest detection, probably because females interrupted their nest travel when they observed us in the surroundings of the pond. Our results should be interpreted cautiously, as they come from only one monitored nest of each species. we found pronounced differences in incubation temperature and duration between both species. The higher mean temperature detected in the M. leprosa nest was probably related to its location, considerably

150

SHORT NOTES

more exposed to ambient temperature fluctuations and drier than the location of the E. orbicularis nest. This type of exposure was also observed for nests destroyed by predators, which were located 10-200 m away from the pond, in a wide open area of grassland. At lower incubation temperatures, embryo development is slower and thus the incubation period is longer (PACKARD & PACKARD, 1988; DEEMING & FERGUSON, 1991). For M. leprosa, we found a notable proportion of hatchlings emerging at the end of the summer; these hatchlings probably came from eggs of earlier clutches. On the other hand, in the nest of E. orbicularis, the lower incubation temperature, and the consequent slower development, probably resulted in hatching taking place on later, colder dates, which in turn could have delayed hatchling emergence. A delay in emergence is common in chelonians, and hatchlings may stay in the nest after hatching for short and variable periods (e.g. DÍAzPANIAGUA et al., 1997) or even overwinter in the nest (GIBBONS & NELSON, 1978; CONGDON & GIBBONS, 1985; JACKSON, 1994; DEPARI, 1996). The two nests monitored in this study contained late clutches, while the first hatchlings intercepted in August might have come from early clutches. Because newborn hatchlings of both species have been commonly observed in the spring in different localities (Mauremys leprosa: HERNáNDEz GIL et al., 1993; ARAUJO et al., 1997. Emys orbicularis: SERVAN, 1983; SEGURADO et al., 2005), it is possible that the hatchlings extracted from our monitored nests, especially those in the E. orbicularis one, could have started overwintering in the nest.

Acknowledgement This study was funded by Junta de Andalucía (Grupo de Investigación RNM 128) and Ministerio de Agricultura y Medio Ambiente-OAPN (proyecto 158/2010).

REFERENCES ANDREU, A.C. & VILLAMOR, M.C. (1989).

Calendario reproductivo y tamaño de puesta en el galápago leproso, Mauremys leprosa (Schweigger, 1812) en Doñana, Huelva.

Doñana Acta Vertebrata 16: 167-172.

ARAúJO, P.; SEGURADO, P. & SANTOS, N. (1997).

Bases para a Conservação das Tartarugas de Água Doce, Emys orbicularis e Mauremys leprosa.

Series: Estudos de Biologia e Conservação da Natureza, vol. 24. Instituto de Conservação da Natureza. Lisboa, Portugal.

COMBESCOT, C. (1955). Sexualité et cycle génital de la tortue d’eau algérienne, Emys leprosa Schw. Bulletin de la Société d’Histoire Naturelle de l’Afrique du Nord 45: 366-377.

CONGDON, J.D. & GIBBONS, J.w. (1985).

Egg components and reproductive characteristics of turtles: Relationships to body size. Herpetologica 41: 194-205.

DEEMING, D.C. & FERGUSON, M.w.J. (1991).

Physiological effects of incubation temperature on embryonic development in reptiles and birds, In D.C. Deeming & M.w.J. Ferguson (eds.) Egg Incubation. Its Effects on Embryonic Development in Birds and Reptiles.

Cambridge University Press, Cambridge, UK, pp. 147-172.

DEPARI, J.A. (1996) Overwintering in the nest chamber by hatchling painted turtles, Chrysemys picta, in northern New Jersey.

Chelonian Conservation and Biology 2: 5-12.

SHORT NOTES

DÍAz-PANIAGUA, C.; KELLER, C. & ANDREU, A.C. (1997). Hatching success, delay of emergence and hatchling biometry of the spur-thighed toroise, Testudo graeca, in south-western Spain. Journal of Zoology 243: 543-553.

GIBBONS, J.w. & NELSON, D.H. (1978).

The evolutionary significance of delayed emergence from the nest by hatchling turtles. Evolution 32: 297-303.

HERNáNDEz GIL, V.; DICENTA LóPEzHIGUERA, F.; ROBLEDANO AYMERICH, F.; GARCÍA MARTÍNEz, M.L.; ESTEVE SELMA, M.A. & RAMÍREz DÍAz, L. (1993).

Anfibios y Reptiles de la Región de Murcia.

Universidad de Murcia, Murcia, Spain.

JACKSON, D.R. (1994). Overwintering of hatching turtles in northern Florida.

Journal of Herpetology 28: 401-402.

KELLER, C. (1997). Ecología de Poblaciones de Mauremys leprosa y Emys orbicularis en el Parque Nacional de Doñana. Ph.D. dissertation, Universidad de Sevilla, Sevilla, Spain.

KELLER, C.; DÍAz-PANIAGUA, C.; ANDREU, A.C. & BRAVO, M.A. (1995). Distribution of freshwater turtles in the Doñana National Park (Sw Spain). Implications for the management of an isolated population, In International Congress of Chelonian Conservation:France, Gonfaron, Tortoise Village, 6th to 10th of July 1995: Proceedings.

SOPTOM, Gonfaron, France, pp. 192-195.

PACKARD, G.C. & PACKARD, M.J. (1988) The physiological ecology of reptilian eggs and

151

embryos, In C. Gans & R.B. Huey (eds.)

Defense and Life History. Series: Biology of the Reptilia, vol. 16 Ecology B. Alan R. Liss, New York, USA, pp. 523-605.

PEREz, M.; COLLADO, E. & RAMO, C. (1979).

Crecimiento de Mauremys caspica leprosa (Schweigger, 1812) (Reptilia, Testudines) en la Reserva Biológica de Doñana. Doñana Acta Vertebrata 6: 161-178.

PLEGUEzUELOS, J.M.; MáRQUEz, R. & LIzANA, M. (2002): Atlas y Libro Rojo de los Anfibios y Reptiles de España. Dirección General de la Conservación de la Naturaleza - Asociación Herpetológica Española, Madrid, Spain.

ROQUES, S.; DÍAz-PANIAGUA, C.; PORTHEAULT, A.; PéREz-SANTIGOSA, N. & HIDALGOVILA, J. (2006). Sperm storage and low incidence of multiple paternity in the European pond turtle, Emys orbicularis: a secure but costly strategy? Biological Conservation 129: 236-243.

SEGURADO, P.; AYRES FERNáNDEz, C. & CORDERO RIVERA, A. (2005). La cistude d’Europe dans la Péninsule ibérique.

Manouria 8: 19-20.

SERVAN, J. (1983). émergence printanière des jeunes Cistudes en Brenne. Bulletin de la Société Herpétologique de France 28: 35-37. wILBUR, H.M. & MORIN, P.J. (1988). Life history evolution in turtles, In C. Gans & R.B. Huey (eds.) Defense and Life History. Series: Biology of the Reptilia, vol. 16 Ecology B. Alan R. Liss, New York, USA, pp. 387-439.

152

Basic and Applied Herpetology 28 (2014): 153-159

Helminths from the red-eared slider Trachemys scripta elegans (Chelonia: Emydidae) in marshes from the eastern Iberian Peninsula: first report of Telorchis attenuata (Digenea: Telorchiidae) Jesús Cardells, María Magdalena Garijo*, Clara Marín, Santiago Vega Universidad Cardenal Herrera-CEU, Facultad de Veterinaria, Moncada, Valencia, Spain. * Correspondence: Instituto de Ciencias Biomédicas, Universidad Cardenal Herrera-CEU. Phone: +34 961369000 ext. 1268, Fax: +34 961369007, E-mail: jcardells@uch.ceu.es

Received: 18 September 2012; received in revised form: 15 March 2013; accepted: 29 April 2013.

The present work describes the presence of a digenean in the red-eared turtle Trachemys scripta elegans (wiedNeuwied, 1839) in marshes of the Valencian Community. The faeces and intestinal tract of 105 animals were examined. Only one helminth species was found and identified as the digenean trematode Telorchis atenuatta (Goldberger, 1911), present in the 7.6% of the animals analysed. This is the first report of the parasite in sliders from Spain. Although conclusions are preliminary due to the limited sampling, our results suggest that the presence of red-eared turtles in new habitats may increase the risk of introducing new microorganisms and new diseases with them, altering the sanitary status of the autochthonous terrapins Mauremys leprosa (Schweigger, 1812) and Emys orbicularis (Linnaeus, 1758).

Key words: helminths; parasites; Telorchis atenuatta; terrapins; Trachemys.

Helmintos del galápago Trachemys scripta elegans (Chelonia: Emydidae) en los marjales de la Comunidad Valenciana: primera cita de Telorchis attenuata (Digenea: Telorchiidae). El presente trabajo describe la presencia de un digénido en la tortuga de Florida Trachemys scripta elegans (wied-Neuwied, 1839) en los marjales de la Comunidad Valenciana. Se examinaron los tractos intestinales y excrementos de 105 animales.

Solamente se encontró una especie de helminto, identificado como el trematodo digénido Telorchis atenuatta (Goldberger, 1911), detectado en el 7,6% de los animales analizados. Se trata de la primera cita de este parásito en tortugas en España. Aunque las conclusiones son preliminares debido a lo reducido del muestreo, los resultados sugieren que la presencia de galápagos de Florida en hábitats nuevos puede aumentar el riesgo de introducción de microorganismos y enfermedades, alterando el estado sanitario de los galápagos autóctonos Mauremys leprosa (Schweigger, 1812) y Emys orbicularis (Linnaeus, 1758).

Key words: galápagos; helmintos; parásitos; Telorchis atenuatta; Trachemys.

The red-eared slider Trachemys scripta elegans is an invasive species frequently treated as a pet (SALzBERG, 1995; TELECKY, 2001), that has become patent in the Spanish marshes in the last years (MARCO et al., 2003).

Natural reproduction of this species has been repeatedly observed in Europe under Mediterranean climatic conditions. Recent studies alert of the danger associated with DOI: http://dx.doi.org/10.11160/bah.12006/

invasive species introduction due to the alteration of turtle resident communities through various processes including predation, competitive exclusion or parasites transfer (ARVY & SERVAN 1998; CADI & JOLY, 2003, 2004). Some authors have also reported weight loss and high mortality in the autochthonous European pond turtle (Emys orbicularis) when coexisting with T. scripta

154

SHORT NOTES

(CADI & JOLY, 2004; PéREz et al., 2006).

In Spain, two native species, the Mediterranean pond turtle (Mauremys leprosa) and E. orbicularis are currently sharing habitat with T. scripta (PLEGUEzUELOS, 2002; COX et al., 2006). In 2005 the Valencian Community (east of Spain) reported the existence of twelve marshals in which native turtles coexisted with the slider turtle (BATALLER & FORTEzA, 2005). In 2008 this number decreased to eight, as a consequence of invasive species control programs (BATALLER et al., 2008). Previous studies reported the presence of nematodes of the genera Falcaustra, Serpinema, Physaloptera, Aplectana and trematodes of the genus Patagium in T. scripta and native turtles in Spain (ESCH et al., 1979; ROCA et al., 2005; HIDALGO-VILA et al., 2006, 2009; VILLARáN & DOMÍNGUEz, 2009; ALARCOS et al., 2010).

The goal of this study was to analyse the existence of parasites in wild exotic turtles in Valencian Community’s marshes. As a result of the survey we describe for the first time the presence of a digenean trematode Telorchis attenuata in wild red-eared slider populations from Spain.

Between July and October 2008, a total of 105 specimens of the subspecies T. scripta elegans from three marshes in the Valencian Community were examined: 32 from Peñíscola, 25 from Almenara and 48 from La Safor. In all those places T. scripta elegans is sharing territory with autochthonous species.

Animals were captured with netting and floating traps and were carried in individual boxes to a necropsy room at the University CEUCardenal Herrera. Of the total number of animals examined, 73 were females and 32 males. weight was recorded and grouped into three

categories. Forty-eight animals weighted less than 500 g; 33 between 500 and 1000 g, and the other (24) exceeded 1000 g. Individual faecal samples were collected and observed under a stereo microscope to assess for the presence of adult nematodes. Moreover, faeces were processed by a standard flotation concentration method, and the concentrate obtained was observed under the microscope in order to detect helminth eggs. Red-eared sliders were sacrificed by a sodium thiopental injection (Dolethal®, Vétoquinol, Lure, France) and digestive tracts were removed, opened and content diluted in Ringer’s solution and observed under the stereo microscope. The recovered helminths were counted and preserved in formaldehyde 10% being fixed under pressure between two slides during 24 hours. Then, trematodes were stained with hematoxylin and mounted in lactophenol for posterior identification (HIDALGO-VILA et al., 2009).

From all individuals examined, only eight turtles were parasitized, all of them infected with adult trematodes (prevalence: 7.6%). The only identified species was Telorchis atenuatta (Goldberger, 1911) (Fig. 1). The mean intensity of parasitism was 11.3 helminths per host (min-max, 1-33). The parasitic burden found in the positive animals is shown in Table 1.

After processing faeces, no adults were found under the stereomicroscope; however, all the positive animals at the necropsy were simultaneously excreting eggs in faeces, which were observed by concentration. No other nematodes, cestodes or acantocephalans were observed in the coprological analysis or in necropsies.

All the positive turtles came from a single locality (Almenara), except one turtle coming from La Safor. From the infected turtles, six were determined as females and two as males.

155

SHORT NOTES

Figure 1: Adult specimen of Telorchis attenuata (Goldberg, 1911).

Regarding weight, three weighted less than 500 g, three between 500 and 1000 g, and the remaining two weighted more than 1000 g.

Previous studies carried out in Spain showed the presence of nematodes, trematodes and cestodes in the autochthonous turtles M. leprosa and E. orbicularis (LรณPEz-NEYRA, 1947; LรณPEz-ROMรกN, 1974; LLUCH et al., 1987; CORDERO DEL CAMPILLO et al., 1994; KIRIN, 2001; ROCA et al., 2005; HIDALGOVILA et al., 2006; VILLARรกN & DOMร NGUEz, 2009; ALARCOS et al., 2010). Regarding the invasive species T. scripta, a study in southwest Spain reported four nematode genera, but no trematodes (HIDALGO-VILA et al., 2009). Our study, however, shows exclusively the presence

of trematodes. This lack of congruence between studies might be due to the fact that in many cases exotic traded turtles come from eggs originated in farms, and thus have not been previously in contact with natural habitats (wARwICK et al., 2001; HIDALGOVILA et al., 2009).

ESCH & GIBBONS (1967) found an increment in parasitism intensity of nematodes and trematodes in turtles during the first four years of life, progressively decreasing between the five and ten years. Authors suggest that this variation might be related to changes in diet and sexual maturity. The basis for this generalization rests in the knowledge that in many turtle species, juveniles are obligate carnivores while adults are primarily herbivores (MOLL & LEGLER, 1971; PARMENTER & AVERY, 1990; ESCH et al., 1993; DERSLICK 1999). In our study, the fact that all but one of the parasitized animals were captured in the same area might suggest a stronger relation to dietary habits than to age or sex. According to other authors, T. scripta can accidentally ingest intermediate hosts of trematodes, like snails, when feeding on vegetables (ESCH et al., 1979; KENNEDY et al., 1986).

Table 1: Sex, weight (in grams) and number of trematodes (Intensity) detected on the T. scripta elegans specimens included in this study.

Individual

Sex

weight (g)

Intensity

1 2 3 4 5 6 7 8

Female Male Female Male Female Female Female Female

1200 700 500 350 800 650 300 1800

1 12 1 11 18 6 33 8

156

SHORT NOTES

The trematode Telorchis has been previously described in different parts of the world parasitizing water turtles. In Mexico, T. attenuata was found in the intestine of T. scripta (MORAVEC & VARGAS-VáSQUEz, 1998; PéREz-PONCE et al., 2001); in Tunisia, T. temimi was identified in E. orbicularis (MISHRA & GONzáLEz, 1978), and in the same host three species of the genus (T. assula, T. parvus and T. stossichi) were detected in Austria (HASSL & KLEEwEIN, 2010). In Spain, the species T. solivagus was found in M. leprosa (LóPEz-ROMáN, 1974, LLUCH et al., 1987). However, the species identified in this study, T. attenuata, was not previously cited in Spain, although it was in the original distribution range of the host species (MORAVEC & VARGAS-VáSQUEz, 1998). One possibility could be that T. scripta elegans individuals were already parasitized when they reached the marshes and that they could survive thanks to the presence of adequate intermediate hosts. Another possibility could be that Trachemys was not sampled previously in this region. The life cycle of Telorchis is not well known, but assuming a typical digenean cycle, the first intermediate host could be a freshwater snail and the second one, where the infective metacercaria develops, a hemipteral larvae (CHENG, 1978). The main snail genera acting as intermediate hosts in Telorchis infecting reptiles (T. corti) are Lymnaea spp., Planorbis spp. and Physella spp. (BARRAGáN-SáENz et al., 2009). All of them have been previously described in Spain. However, it seems that for Telorchis spp., survival depends on other resources rather than on intermediate hosts’ availability (RADTKE et al., 2002).

The introduction of T. scripta in new habitats may be accompanied with the arrival of new microorganisms and diseases (DASzAK

et al., 2001, POLO-CAVIA et al., 2010). In order to assess this possibility, it would be necessary to extend the study to autochthonous turtles living in syntopy. Considering the presence of trematodes in autochthonous turtles in other areas from Spain, like the ones detected in M. leprosa from Castilla y León (ALARCOS et al., 2010), or the species Patagium pellucidum in the same host from Extremadura (ROCA et al., 2005), we do not discard the possibility that they might also be present in the study area.

Acknowledgement Conselleria de Medi Ambient, Aigua, Habitatge i Urbanisme funded the project.

Jose María Gil helped during sampling.

REFERENCES ALARCOS, G.; CASANOVA, J.C.; FLECHOSO DEL CUETO, F. & LIzANA M. (2010). Parásitos en heces de galápagos autóctonos (Emys orbicularis y Mauremys leprosa) en Castilla y León, España, In XI Congreso Luso-Español de Herpetología / XV Congreso Español de Herpetología. Anfibios y Reptiles ante el Cambio Global. Facultad de Biología, Universidad de Sevilla, Sevilla, Spain, p. 225.

ARVY, C. & SERVAN, J. (1998). Imminet competition between Trachemys scripta and Emys orbicularis in France.

Mertensiella 10: 33-40.

BARRAGáN-SáENz, F.A.; SáNCHEz-NAVA, P.; HERNáNDEz-GALLEGOS, O. & SALGADOMALDONADO, G. (2009). Larval stages of trematodes in gasteropods from Lake Chicnahuapan, state of Mexico. Parasitology Research 105: 1163-1167.

SHORT NOTES

BATALLER, J.V. & FORTEzA, A. (2005).

Mejora del Hábitat de las Poblaciones de Galápago Europeo (Emys orbicularis) en la Comunidad Valenciana. Memoria de Actuaciones (2003-2005). Generalitat Valenciana, Conselleria de Territori i Habitatge, Valencia, Spain.

BATALLER, J.V.; BARTOLOMé, M.A.; PRADILLO A.; SARzO, B.; VILALTA, M.; CERVERA, F. & MONSALVE, M.A. (2008).

Control de Poblaciones de Galápagos Exóticos en Humedales de la Comunidad Valenciana. Informe de Actividades del Equipo Técnico de Seguimiento de Fauna Amenazada. Generalitat Valenciana, Conselleria de Medi Ambient, Aigua, Urbanisme i Habitatge, Valencia, Spain.

CADI, A. & JOLY, P. (2003). Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Canadian Journal of Zoology 81: 1392-1398.

CADI, A. & JOLY, P. (2004). Impact of introduction of red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle. Biodiversity and Conservation 13: 2511-2518.

CHENG, T. (1978). Parasitología General. AC Ed., Madrid, Spain.

CORDERO DEL CAMPILLO, M.; CASTAñóNORDóñEz, L. & REGUERA-FEO, A. (1994). Índice Catálogo de Zooparásitos Ibéricos. 2nd ed.

Secretariado de Publicaciones, University of León, León, Spain.

COX, N.; CHANSON, J. & STUART, S. (2006).

The Status and Distribution of Reptiles and Amphibians of the Mediterranean Basin.

The world Conservation Union (IUCN), Gland, Switzerland and Cambridge, UK.

157

DASzAK, P.; CUNNINGHAM, A.A. & HYATT, A.D. (2001). Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78: 103-116.

DERSLIK, M.J. (1999). Dietary notes on the red-eared slider (Trachemys scripta) and river cooter (Pseudemys concinna) from Southern Illinois. Transactions of the Illinois State Academy of Science 92: 233-241.

ESCH, G.w. & GIBBONS, w. (1967).

Seasonal incidence of parasitism in the painted turtle, Chrysemys picta marginata (Agassiz, 1857). Journal of Parasitology 53: 818-821.

ESCH, G.; GIBBONS, w. & BOURQUE, J. (1979). The distribution and abundance of enteric helminths in Chrysemys s. scripta from various habitats on the Savannah River Plant in South Carolina. Journal of Parasitology 65: 624-632.

ESCH, G.w.; MARCOGLIESE, D.J.; GOATER, T.M. & JACOBSON, C. (1993). Aspects of the evolution and ecology of helminth parasites in turtles: a review. In J.V. Gibbons (ed.) Life History and Ecology of the Slider Turtle. Smithsonian Institution Press, washington DC, USA, pp. 299-307.

HASSL, A.R. & KLEEwEIN, A. (2010).

Identifying parasites as substitution causes in populations of local and allocthonous turtles in Lower Austria, In 32nd Annual Meeting of the Austrian Society for Hygiene, Microbiology and Preventive Medicine (ÖGHMP). österreichische Gesellschaft für Hygiene, Mikrobiologie und Präventivmedizin, Vienna, Austria.

HIDALGO-VILA, J.; RIBAS, A.; FLORENCIO, M.; PéREz-SANTIGOSA, M. & CASANOVA, J.C. (2006). Falcaustra donanaensis sp. nov.

158

SHORT NOTES

(Nematoda: Kathlaniidae) a parasite of Mauremys leprosa (Testudines, Bataguridae) in Spain. Parasitology Research 99: 410-413.

HIDALGO-VILA, J.; DÍAz-PANIAGUA, C.; RIBAS, A.; FLORENCIO, M.; PéREz-SANTIGOSA, M. & CASANOVA, J.C. (2009). Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in southwestern Spain: Transmission from native turtles.

Research in Veterinary Sciences 86: 463-465.

KENNEDY, C.R.; BUSH, A.O. & AHO, J.M. (1986). Patterns in helminth communities: why are birds and fish different?.

Parasitology 93: 205-215.

KIRIN, D.A. (2001). New data on the helminth fauna of Emys orbicularis L (1758) (Reptilia, Eymydidae) in South Bulgaria.

Comptes Rendus de l’Académie Bulgare des Sciences 54: 95-98.

LLUCH, J.; ROCA, V.; NAVARRO, P. & MASCOMA, S. (1987). Helmintofauna de los herpetos ibéricos: estado actual de conocimientos, consideraciones ecológicas y estimaciones coprológicas. In V. Sans-Coma; S. Mas-Coma & J. Gosálbez (eds.)

Mamíferos y Helmintos. Kretes Ed., Barcelona, Spain, pp. 143-161.

LóPEz-NEYRA, C.R. (1947). Helmintos de los Vertebrados Ibéricos. CSIC, Instituto Nacional de Parasitología de Granada, Granada, Spain.

LóPEz-ROMáN, R. (1974). Trematodes de las Tortugas de España, I. Redescripción de Telorchis solivagus Odhner, 1902 (Telorchiidae, Digenea) parásito de Clemmys leprosa Schweigger. Revista Ibérica de Parasitología 34: 185-195.

MARCO, A.; HIDALGO-VILA, J.; PéREzSANTIGOSA, C.; DÍAz-PANIAGUA, C. & ANDREU, A. (2003). Potencial invasor de

galápagos exóticos comercializados e impacto sobre ecosistemas mediterráneos.

In L. Capdevilla-Argüelles; B. zilletti & N. Pérez-Hidalgo (eds.) Contribuciones al Conocimiento de las Especies Exóticas Invasoras. Grupo Especies Invasoras Ed., Serie Técnica 1, León, Spain, pp. 76-78.

MISHRA, G.S. & GONzáLEz, J.P. (1978). Parasites of fresh water turtles in Tunisia. Archives de l’Institut Pasteur de Tunis 55: 303-326.

MOLL, E.O. & LEGLER, J.M. (1971). Life history of a neotropical slider turtle, Pseudemys scripta (Schoepff ), in Panama.

Bulletin of the Los Angeles County Museum of Natural History 11: 101-102.

MORAVEC, F. & VARGAS-VáSQUEz, J. (1998).

Some endohelminths from the freshwater turtle Trachemys scripta from Yucatán, Mexico.

Journal of Natural History 32: 455-468.

PARMENTER, R.R. & AVERY, H.w. (1990). The feeding ecology of the slider turtle, In J.w.

Gibbons (ed.) Life History and Ecology of the Slider Turtle. Smithsonian Institution Press, washington DC, USA, pp. 257-266.

PéREz, N.; DÍAz, C.; HIDALGO-VILA, J.; MARCO, A.; ANDREU, A. & PORTHEAULT, A. (2006). Características de dos poblaciones reproductoras del galápago de Florida, Trachemys scripta elegans, en el suroeste de España. Revista Española de Herpetología 20: 5-17.

PéREz-PONCE, G.; JIMéNEz-RUIz, A.; MENDOzA-GARFIAS, B. & GARCÍAPRIETO, L. (2001). Helminth parasites of garter snakes and mud turtles from several localities of the Mesa Central of Mexico.

Comparative Parasitology 68: 9-20.

PLEGUEzUELOS, J.M. (2002). Las especies introducidas de anfibios y reptiles, In J.M. Pleguezuelos; R. Márquez & M. Lizana

SHORT NOTES

(eds.). Atlas y Libro Rojo de los Anfibios y Reptiles de España. Dirección General de Conservación de la Naturaleza-Asociación Herpetológica Española, Madrid, Spain, pp. 501-532.

POLO-CAVIA, N.; GONzALO, A.; LóPEz, P. & MARTÍN, J. (2010). Predator recognition of native but not invasive turtle predators by naïve anuran tadpoles. Animal Behaviour 80: 461-466.

RADTKE, A.; MCLENNAN, D.A. & BROOKS, D.R. (2002). Resource tracking in north American Telorchis spp (Digenea: Plaguiorchiformes: Telorchidae). Journal of Parasitology 88: 874-879.

ROCA, V.; SáNCHEz, N. & MARTÍN, J.E. (2005). Intestinal helminth parasitizing Mauremys leprosa (Chelonia: Bataguridae) from Extremadura (western Spain). Revista Española de Herpetología 19: 47-55.

159

SALzBERG, A. (1995). Report on import/export turtle trade in the United States, In J.J. Behler; I. Das; B. Fertard; P. Pritchard; B. Branch; L. Durrel & J. Fretey. (eds.) Proceedings of the International Congress of Chelonian Conservation. Soptom Eds., Gonfaron, France, pp. 314-322.

TELECKY, T.M. (2001). United States import and export of live turtles and tortoises.

Turtle and Tortoise Newsletter 4: 8-13.

VILLARáN, A. & DOMÍNGUEz, J. (2009).

Infestación múltiple de Mauremys leprosa por nematodos. Boletín de la Asociación Herpetológica Española 20: 37-39. wARwICK, C.; LAMBIRIS, A.J.L.; wESTwOOD, D. & STEEDMAN, C. (2001). Reptile-related salmonelosis. Journal of the Royal Society of Medicine 94: 124-126.

160

BOOK REVIEWS

161

Natural history and conservation of the Orinoco crocodile (Crocodylus intermedius) en Colombia Merchán, M. (Ed.), A. Castro, M. Cárdenas, R. Antelo y F. Gómez 2012. Asociación Chelonia. Serie Monografías Vol. IV. Madrid, 240 pp. ISBN 978-84-615-3543-9

The Orinoco crocodile (Crocodylus intermedius) is a species listed by the International Union for Conservation of Nature (IUCN) as Critically Endangered. It is the only crocodile species distributed in a single watershed, the vast Orinoco Basin, shared by Colombia and Venezuela, where it is distributed in watercourses along the great plains of the lowlands from this region, known as Los Llanos del Orinoco, and some adjacent areas.

In this monography, authors compile all available information on the species, conducting a thorough review of the literature and adding new data resulting from the research done in the colombian Llanos in 2010 and 2011. The book is divided into seven chapters, reviewing the main biological and ecological aspects of the Orinoco aligator, and the evolution of its conservation status. After an introductory chapter contextualizing the work, the main biological and behavioral characteristics of the species are described on basis to both modern and historical records obtained from traveler notes and chroniclers from the XVIII and XIX centuries, unveiling the abundance of the species in the past. The third chapter describes the physical, biological and human peculiarities of the Colombian Llanos, providing a good characterization of the species habitat and distribution.

Chapters four and five analyze the legal framework affecting the conservation of the species in Colombia, as well as the factors that brought the species to the brink of extinction, and the conservation efforts implemented in Colombia and Venezuela from the 70s to present. It also included a chapter on methods for the detection and interpretation of prints and tracks as a useful tool for analysing animal behavior. Finally, the last chapter presents the results and conclusions of the studies done by the Association in the Colombian Llanos Chelonia during 2010 and 2011, including unpublished distribution and behavioral data of the species in the wild.

The book has over 100 color photographs, and over twenty detailed maps regarding the sampling paths visited in the conservation project of the species. It also includes a glossary of local terms and “lenguaje llanero”, mostly referred to local wildlife. This publication has been developed within the project actions "Conservation of the Orinoco Crocodile (Crocodylus intermedius) in the eastern plains of Colombia", leaded by the non profit spanish association Chelonia, and the Regional Autonomous Corporation of the Orinoco (Corporinoquia), environmental authority with jurisdiction over most of the Colombian Orinoco, which supports and complements the work of other institutions involved in the conservation of this species. The publication has also involved the Biodiversity Foundation (Spain), Fonds de Dotation pour la Biodiversité (France), Lacoste (France), and the Colombian organizations Natural Protected Areas corporation (PNA) and Forest Conservation and Development foundation (CDF).

162

BOOK REVIEWS

The work is, therefore, the most comprehensive source of information regarding the species published to date, with interest for scientific, divulgation and awareness for conservation scopes.

The book is available in PDF format in English and Spanish, at the following address: http://caimanllanero.jimdo.com/descargas/ Historia natural y conservación del caimán llanero (Crocodylus intermedius) en Colombia. El caimán llanero, caimán del Orinoco o cocodrilo del Orinoco (Crocodylus intermedius) es una especie catalogada por la Unión Internacional para la Conservación de la Naturaleza (UICN) en la categoría en peligro crítico de extinción.

Es la única especie de cocodrilo que se distribuye en una única cuenca hidrográfica, la gran cuenca del Orinoco, compartida por Colombia y Venezuela, ocupando cursos de agua de las grandes llanuras de las tierras bajas de esta región, conocida como Los Llanos del Orinoco, y algunas áreas adyacentes.

En esta obra los autores han compilado la información existente sobre la especie, realizando una profunda revisión bibliográfica e incorporando datos inéditos producto de las investigaciones realizadas en los Llanos colombianos en 2010 y 2011. El libro se divide en siete capítulos en los que se repasan los principales aspectos biológicos y ecológicos del caimán llanero, así como sobre la evolución de su estado de conservación. Tras un capítulo introductorio contextualizando el trabajo, se presentan las principales características biológicas y comportamentales de la especie, e incluyendo registros modernos e históricos, a partir del análisis de obras de viajeros y cronistas de los siglos XVIII y XIX, que dejan entrever la abundancia de la especie en el pasado. El tercer capítulo describe las particularidades físicas, biológicas y humanas de los Llanos colombianos, proporcionando una caracterización del hábitat y área de distribución de la especie. Los capítulos cuatro y cinco analizan el marco legal que afecta a la conservación de la especie en Colombia, así como los factores que la han llevado al borde de la extinción y las iniciativas de conservación iniciadas en Colombia y Venezuela desde los años 70 hasta la actualidad. Se ha incluido también un capítulo relativo a métodos para la localización e interpretación de huellas y rastros, como medio de análisis y comprensión de su comportamiento.

Finalmente, la obra concluye con un capítulo en el que se exponen los resultados y conclusiones de los muestreos realizados por la Asociación Chelonia en los Llanos colombianos durante los años 2010 y 2011, incluyendo datos inéditos de distribución y notas de comportamiento de la especie en estado silvestre.

El libro incluye más de 100 fotografías a todo color, y una veintena de mapas detallados sobre los recorridos efectuados dentro del proyecto de conservación de la especie. También incluye un glosario de términos locales y de “lenguaje llanero”, referidos principalmente a fauna local.

La publicación ha sido desarrollada dentro de las acciones del proyecto “Conservación del cocodrilo del Orinoco (Crocodylus intermedius) en los Llanos Orientales de Colombia”, dirigido por la Asociación Chelonia, entidad española sin ánimo de lucro, y la Corporación Autónoma Regional de la Orinoquia (Corporinoquia), autoridad ambiental con jurisdicción sobre la mayor parte de la Orinoquia colombiana, que apoya y complementa la labor de otras instituciones involucradas en la conservación de la especie. Ha contado con la participación de la Fundación Biodiversidad (España), Fonds de Dotation pour la Biodiversité (Francia), la compañía Lacoste (Francia), y las organizaciones colombianas Corporación áreas Naturales Protegidas (ANP) y Fundación Conservación y Desarrollo Forestal (CDF).

La obra es, por tanto, la más completa fuente de información sobre la especie publicada hasta la fecha, con elevado interés no sólo por su contribución científica, sino también por su carácter divulgativo y de sensibilización para la conservación.

La obra está disponible en formato PDF, tanto en español como en inglés, en la siguiente dirección electrónica: http://caimanllanero.jimdo.com/descargas/

163

PUBLICATION GUIDELINES AIMS AND SCOPE Basic and Applied Herpetology (B&AH) is the official journal of the Spanish Herpetological Society (AHE). B&AH publishes original research papers dealing with any aspect of amphibians and reptiles worldwide. Updated reviews about especially interesting issues and book reviews will also be accepted if they fit with the general purpose of the journal. There is no maximum limit to the length of the papers submitted although authors can be requested to shorten their paper if necessary. Authors can submit short notes if these are organized around hypotheses appropriately argued and analysed quantitatively. The editors reserve the right to publish the accepted manuscripts as original research papers or as short notes at their convenience, regardless of the format of the original manuscript. B&AH will not accept distribution notes or punctual or sporadic observations. This kind of papers must be submitted to the Boletín de la Asociación Herpetológica Española http://www.herpetologica.es/publicaciones/boletin-de-la-asociacion-herpetologica-espanola Submission of a manuscript implies, without further acceptance by authors, that the work described has not been published before (except in the form of an abstract), that it has not been submitted or published elsewhere, and that its content and publication in B&AH has been approved by all co-authors. By submitting a manuscript, the authors agree that the copyright for their article is transferred to the AHE if and when the article is accepted for publication. The copyright covers the exclusive and unlimited rights to reproduce and distribute the article in any form of reproduction.

To minimize turnaround time, authors are encouraged to follow the instructions below.

Manuscripts not in the correct format may be returned to the authors for modification.

Instructions to authors are posted on the web page of B&AH

http://bah.herpetologica.es MANUSCRIPT SUBMISSION Manuscripts should be submitted preferably as e-mail attachments to the journal address: bah@herpetologica.org Manuscripts will be prepared using word-processing software (preferably MS word). Please do not submit material as PDF files.

Although less recommendable, manuscripts can also be sent through postal mail in a mass storage device (CD-ROM, pen-drive, etc.) to one of the following addresses: Manuel Ortiz Santaliestra. Editor, Basic and Applied Herpetology. Instituto de Investigación en Recursos Cinegéticos UCLM-CSIC-JCCM. Ronda de Toledo s/n 13071 Ciudad Real (Spain).

Ana Perera Leg. Editor, Basic and Applied Herpetology. CIBIO. Campus Agrário de Vairão.

Rua Padre Armando Quintas-Castro 4485-661 Vairão (Portugal).

Postal mail from Spain or Portugal should be addressed to the editor in your own country. Mail from the rest of countries should be addressed to M. Ortiz (for papers concerning amphibians) or A. Perera (for papers concerning reptiles). Studies with a general subject or dealing with both taxa can be sent to either editor. It is not necessary to send a hard copy of the manuscript. The storage device must contain only the files corresponding to the submitted paper, without duplicate files or different versions of the same file. Devices will not be returned to the authors regardless of the acceptance or rejection of the paper.

For the original submission, include figures and tables in the same file as the main text of the manuscript. If high-resolution figures are necessary, send them as separate files once the paper has

164

been accepted for publication and potential corrections of such figures has been introduced. Original files containing figures in the software they were created must be sent to the journal upon acceptance of the paper for publication. Do not submit original high-resolution figures with the initial submission unless the originals must be seen by the editors and the reviewers. with the manuscript submission, authors are requested to suggest the names and contact information of at least three qualified reviewers. All the manuscripts will be evaluated by at least two independent reviewers. The editors reserve the right to choose reviewers other than, or in addition to, those suggested by the authors. Duration of the review process will vary depending on the number of manuscripts in edition, the availability of reviewers and the time needed by reviewers and editors.

Nevertheless, decisions are expected to be communicated within a 90-day period after manuscript submission. The editors’ decision will be based on the reviewers’ evaluations. There are three categories of response: accept after minor revision, accept after major revision, and reject. If a paper is rejected because it requires profound changes, but its content is considered of interest by the editors, authors will be encouraged to resubmit a corrected version. In those cases, the resubmitted manuscript will be evaluated again by reviewers. Authors must include with their revised manuscripts a rebuttal letter including a detailed explanation of how they have dealt with each of the reviewers’ and editors’ comments. Revised manuscripts should be returned to the editors as soon as possible, always within a maximum time of 60 days. After that time, revised manuscripts can be considered a new submission and sent out for review.

GALLEY PROOFS AND ADVANCED ONLINE PUBLICATION when a manuscript is accepted, the provisional abstract and article information (title, authors and affiliations) will be published on the B&AH website and a digital object identifier (DOI) will be assigned. In parallel, a galley proof will be elaborated and sent to the authors, who should return it back corrected as soon as possible. Corrections in proofs should be limited to typographical errors. The costs of any other changes will be charged to the authors. Corrected proofs will be published on the B&AH website and will be available open access. Authors will receive a PDF copy of the article in its final version for personal use.

FORMAT AND STYLE B&AH publishes papers in English or Spanish. However, manuscripts in English will be given preference in the review and edition process. Manuscripts in English may include a Spanish version of the abstract and key words. Such abstract will be added by the editors if it is not included in the original version of the manuscript. Manuscripts in Spanish must include an English version of the abstract and key words. Moreover, authors can include, at their convenience, an additional translation of the abstract and key words to one of the following languages: Portuguese, French, German or Italian.

Manuscripts must be typed double-spaced, aligned left (not justified), and using a normal font (Times New Roman) of size 12. All paragraphs but the abstracts must be indented (1.25 cm).

Manuscripts should have line numbers (continuous for the whole document), page numbers and wide margins (2.5 cm) throughout, including tables and figures. Use consistent punctuation; insert only a single space between words and after punctuation. Type text without end-of-line hyphenation, except for compound words. Use italics only for scientific names of genera and species.

Numbers one to nine should be written in full in the text unless they precede units of measurement (5 mm), are designators (experiment 4), or are separated by a dash (2-3 scales). Higher numbers

165

should be written in Arabic numerals except at the beginning of a sentence. Close up digit numbers except for numbers of five or more digits, in which a space should be used (4000, 45 000). Do not use thousands separator. Measurement units and their abbreviations should conform to those of the SI (Système International d’Unités). For significance tests, give the name of the test followed by a colon, the test statistic and its value, the degrees of freedom (as a subscript to the test statistic) or sample size (as N = x) whichever is the convention for the test, and the probability value (ANOVA: F3,8 = 9.733; P = 0.005). The name of the test can be omitted if can be inferred from the context (“The ANOVA revealed that differences were significant (F3,8 = 9.733; P = 0.005)”). Probability values will be quoted preferably as exact values (P = 0.018), or as below the pre-established threshold significance value (P < 0.05, P < 0.001). Use a space before and after each symbol or mathematical operator (3.54 ± 0.17). Do not use a space after numbers followed by an abbreviator (5%, 24ºC).

MANUSCRIPT SECTIONS Manuscripts should be arranged as follows: title page, abstract page(s), text, tables, figure captions and figures. Each section will include the following information: Title page: • Title: short and informative. In bold characters.

• Names and surnames of the authors (without initials).

• Affiliations: multiple author names should be matched to affiliations by superscript numbers.

• Correspondence: full postal address (including telephone and fax numbers) and e-mail address of the corresponding author, who should be indicated with an asterisk in the list of authors.

• Running title: not exceeding 50 characters.

• word count of the text (including references and excluding tables, figure captions and figures), number of tables and number of figures in the manuscript.

Abstract page(s): • Main abstract: in the manuscript language, no more than 250 words (no more than 150 words for short notes).

• Main key words: 3-6 key words arranged in alphabetical order in the manuscript language, separated by semicolons, and preceded by the term Key words followed by a colon.

In addition, abstract page(s) should include: a) For manuscripts in English: • Title in Spanish (optional). In bold characters.

• Abstract in Spanish (optional): no more than 250 words (no more than 150 words for short notes).

• Key words in Spanish (optional): 3-6 key words arranged in alphabetical order, separated by semicolons, and preceded by the term Key words followed by a colon.

• Title in Portuguese, French, German or Italian (optional). In bold characters.

• Abstract in Portuguese, French, German or Italian (optional): no more than 250 words (no more than 150 words for short notes).

• Key words in Portuguese, French, German or Italian (optional): 3-6 key words arranged in alphabetical order, separated by semicolons, and preceded by the term Key words followed by a colon. b) For manuscripts in Spanish: • Title in English (mandatory). In bold characters.

• Abstract in English (mandatory): no more than 250 words (no more than 150 words for short notes).

166

• Key words in English (mandatory): 3-6 key words arranged in alphabetical order, separated by semicolons, and preceded by the term Key words followed by a colon.

• Title in Portuguese, French, German or Italian (optional). In bold characters.

• Abstract in Portuguese, French, German or Italian (optional): no more than 250 words (no more than 150 words for short notes).

• Key words in Portuguese, French, German or Italian (optional): 3-6 key words arranged in alphabetical order, separated by semicolons, and preceded by the term Key words followed by a colon.

Text, with the following sections for original research papers: • Introduction: without heading. Must be clear and concise, including a justification for the study and a review of the state-of-the-art of the subject. Authors are encouraged to present the objectives of the study at the end of the introduction.

• Materials and Methods: authors must include all the information necessary to replicate the study. when presenting the procedures for data analysis, authors are recommended to state the probability values considered as significant (usually P < 0.05).

• Results: must be clear and concise, without repetition of the results shown in tables and figures.

• Discussion: do not repeat the results but explore their significance. Nevertheless, it is recommendable to start the discussion with a brief summary of the more relevant results.

• Acknowledgements (optional): limit wording, for example: o“J. McAllister and C. Smith helped during the study” instead of “we thank to James McAllister for his participation in the experimental design, and to Cathy Smith for her help during field work” o“Financed by the Regional Government (ref ###)” instead of “Thanks to the Regional Government for financing the study through the project ###” • References (see below) Introduction should begin on the first line of the first page of the text, without heading. write main headings for the rest of the sections, with the exception of acknowledgement, in small caps (MATERIALS AND METHODS, RESULTS, DISCUSSION, REFERENCES) on a separate line and keeping an empty line right before and after each heading. In addition to main headings, authors can use subheadings that will be written in bold italics (e.g. Experimental design, Data analysis), on a separate line and keeping an empty line right before and after each subheading.

Acknowledgements should be placed between the discussion and the references. The heading (Acknowledgement) will be written in italics, on a separate line and keeping an empty line right before and after.

Authors submitting reviews can replace the main headings corresponding to Materials and Methods, Results and Discussion by different headings at their convenience, using small caps for main headings and bold italics for subheadings.

Short notes will be structured and arranged as original research papers, although headings of the sections Materials and Methods, Results and Discussion will be omitted.

Tables: should be numbered consecutively in Arabic numerals arranged as they are quoted in the text. Each table should be typed on a separate page together with a clear descriptive legend. Tables should not include vertical rules, and the main body of the table should not contain horizontal rules. Keep tables as simple as possible and make them understandable without reference to the text.

167

Figure captions: should be typed (double-spaced) and grouped together on a page separate from the figures. They should explain with clarity all the elements in the figure. Make figures understandable without reference to the text.

Figures: illustrations, whether maps, drawings, diagrams or photographs, should be kept to the minimum needed to clarify the text. They should be numbered consecutively in Arabic numerals arranged as they are quoted in the text and submitted on separate pages (one figure per page), each bearing the figure number and, if desired (e.g. in photographs), the name(s) of the figure author(s). If good-quality versions of figures are necessary to be examined during the review process, authors will include such version in the original submission, as separate files, according to the instructions given in the next paragraph. In the text, ‘Figure’ should be abbreviated (Fig. 2) except when beginning a sentence. Authors are encouraged to use a sans serif font (Helvetica, Arial, Geneva) for all text associated with figures. The labelling must be clearly legible and stand reduction to the final print size. Include a scale of distance or dimension where appropriate.

Once the manuscript is accepted for publication, good-quality versions of figures should be submitted in their original format with a minimum resolution of 300 dpi. For figures consisting in a picture modified with symbols, text, etc., authors will be requested to send the original, unmodified, good-quality picture once the manuscript is accepted. For figures not originally in a digital format (photographs, slides, drawings) authors are recommended to use a dedicated scanner or send the original to the editors by postal mail. In these cases, the originals will be returned to authors after digitalization. Given that B&AH assumes the costs of publishing colour prints and slides, these will be accepted only when they are strictly necessary at the editors’ discretion. In some cases, colour figures can be accepted only for the digital version, being displayed in greyscale format in the printed version.

REREFENCES For references in the text give full surnames of the first author followed by the publication year and separated by a comma (Pleguezuelos, 1997). For papers with two authors, use the term “&” to separate surnames (Semlitsch & Bodie, 2003). Papers with three or more authors will be quoted with the surname of the first author followed by ‘et al.’ (note italics) (Stuart et al., 2004). To distinguish between two papers by the same author(s) in the same year use lower-case letters (a,b) after the year, without space, arranged in alphabetical order as the references are quoted in the text (Harris et al., 2004a,b). List multiple citations in chronological order, using alphabetical order for citations within the same year. Separate citations with semicolons (Tyler, 1991; wake, 1991; Blaustein et al., 1994a,b; Stuart et al., 2004). If the citation is part of the sentence, move the surname(s) of the author(s) out of the brackets and delete the comma.

“As pointed by Pleguezuelos (1997)” “Blaustein et al. (1994a) reviewed the situation of amphibians” The reference list should include all and only the references mentioned in the text, tables and figures. Cite references in the reference list in alphabetical order according to the authors' surnames. Multiple citations for the same author should be organized as follows: single citations first (in chronological order), two-author citations second (in alphabetical order), three or more authors third (in chronological order). Spell out (i.e. do not abbreviate) the names of all journals. The references should conform to the following formats:

168

Articles in periodicals: • Stuart, S.N.; Chanson, J.S.; Cox, N.A.; Young, B.E.; Rodrigues, A.S.L.; Fishman, D.L. & waller, R.w. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783-1786.

• wiens, J.J. & Penkrot, T.A. (2002). Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Systematic Biology 51: 69-91.

Books: • Dodd, Jr., C.K. (ed.) (2009). Amphibian Ecology and Conservation. A Handbook of Techniques.

Oxford University Press, Oxford.

• Vitt, L.J. & Caldwell, J.P. (2009). Herpetology: An Introductory Biology of Amphibians and Reptiles, 3rd ed. Academic Press, Burlington, Massachusetts.

Book chapters: • King, R.B. (2009). Population and conservation genetics, In S.J. Mullin & R.A. Seigel (eds.)

Snakes: Ecology and Conservation. Cornell University Press, Ithaca, New York, pp. 78-122. web pages (authors are recommended to keep the use of web pages to a minimum; use peerreviewed literature instead when possible): • IUCN (2010). The IUCN Red List of Threatened Species, v. 2010.3. International Union for Nature Conservation and Natural Resources, Gland, Switzerland. Available at http://www.iucnredlist.org/. Retrieved on 10/31/2010.

SUPPORTING MATERIAL Authors can submit with their manuscripts supporting material related to the work (additional tables and figures, detailed protocols, data logs, audio and video recordings, etc.). The supporting material will be uploaded to the online site of B&AH with a reference code that will be used to quote such material in the final version of the article. In the initial version of the manuscript, supporting material should be quoted as “SM” followed by a number according to the same format as for tables and figures. Supporting material must be submitted as independent files. Name each file with the code used in the initial version of the manuscript (SM1, SM2, etc.). Authors may also refer to supporting material available from a different online site (e.g. GenBank, MorphoBank), in which case the exact access reference will be indicated in the final version of the article.

BIOETHICAL CONSIDERATIONS Because right animal use and care is an area of major concern to the AHE, authors must guarantee that all animals used for research purposes are treated ethically and in accordance with the laws and regulations established by governmental authorities and bioethics committees of each institution.

Therefore, authors are recommended to state in the Acknowledgement section that they have followed the corresponding regulation and legislation on animal care. Authors should cite in this section the information regarding collection permits and experimental protocols approved by bioethics or animal care committees. Editors might request from authors as much information as they consider necessary to confirm the fulfilment of such premises. Failure to comply with these bioethical principles will suppose immediate rejection of the article, regardless of the reviewers’ recommendation.

Las normas de publicación en castellano están disponibles para su consulta en la página web de Basic and Applied Herpetology (http://bah.herpetologica.es/)

BASIC & APPLIED HERPETOLOGY REVISTA ESPAÑOLA DE HERPETOLOGÍA

On behalf of the Spanish Herpetological Society, the editorial board of Basic and Applied Herpetology wants to acknowledge the work of the following experts who have worked as manuscript reviewers for the elaboration of the present volume (in alphabetical order): César Ayres (Spanish Herpetological Society, Spain) Mariana C. Cabagna zenklusen (Universidad Nacional del Litoral, Argentina) Elisa Cabrera Guzmán (University of Sydney, Australia) Miguel ángel Carretero (Universidade do Porto, Portugal) Juan E. Carvajal-Cogollo (Universidad Nacional de Colombia, Colombia) Ylenia Chiari (University of South Alabama, USA) Andrew K. Davis (University of Georgia, USA) Damien Esquerre (Museo Nacional de Historia Natural, Chile) Andrés García-Aguayo (Universidad Nacional Autónoma de México, Mexico) Philippe Golay (Elapsoïdea, Switzerland) Juan Carlos López García (Universidad de Sevilla, Spain) Luca Luiselli (Centre of Environmental Studies Demetra s.r.l., Italy) Fernando Martínez Freiría (Universidade do Porto, Portugal) José Antonio Mateo (Govern Balear, Spain) Jorge Mella (Universidad Central de Chile, Chile) Andrés Sebastián Quinteros (Universidad Nacional de Salta, Argentina) Aurelio Ramírez Bautista (Universidad Autónoma del Estado de Hidalgo, Mexico) Vicente Roca Velasco (Universitat de València, Spain) Javier Rodríguez-Robles (University of Nevada Las Vegas, USA) Luis M. San José (Université de Lausanne, Switzerland) Vicente Sancho (Generalitat Valenciana, Spain) Neftalí Sillero (Universidade do Porto, Portugal) Jean-François Trape (Institut de Recherche pour le Développement, Senegal) Guillermo Velo Antón (Universidade do Porto, Portugal)

AHE

© 2014