Animal Biodiversity and Conservation issue 29.2 (2006)

Formerly Miscel·lània Zoològica

2006

and

Animal Biodiversity Conservation 29.2

"Heliconie erato (Heliconius erato)" Le Règne Animal par Georges Cuvier; Paris: Fortin, Masson et Cie, Librairies; Pl. 133 Insectes Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de redacció / Secretaría de redacción / Editorial Office

Secretària de redacció / Secretaria de redacción / Managing Editor Montserrat Ferrer

Museu de Ciències Naturals Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail abc@bcn.cat

Consell assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Pere Abelló Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Javier Alba–Tercedor Univ. de Granada, Granada, Spain Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament–CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Michael J. Conroy Univ. of Georgia, Athens, USA Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain José Antonio Donazar Estación Biológica de Doñana–CSIC, Sevilla, Spain Gary D. Grossman Univ. of Georgia, Athens, USA Damià Jaume IMEDEA–CSIC, Univ. de les Illes Balears, Spain Jordi Lleonart Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Jorge M. Lobo Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pablo J. López–González Univ de Sevilla, Sevilla, Spain Juan José Negro Estación Biológica de Doñana–CSIC, Sevilla, Spain Vicente M. Ortuño Univ. de Alcalá de Henares, Alcalá de Henares, Spain Miquel Palmer IMEDEA–CSIC, Univ. de les Illes Balears, Spain Francisco Palomares Estación Biológica de Doñana–CSIC, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Montserrat Ramón Inst. de Ciències del Mar CMIMA­–CSIC, Barcelona, Spain Ignacio Ribera Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pedro Rincón Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Alfredo Salvador Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Ciències Naturals de Barcelona, Barcelona, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana–CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle–CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Jersey, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana–CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas–CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway Animal Biodiversity and Conservation 29.2, 2006 © 2006 Museu de Ciències Naturals, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58 The journal is freely available online at: http://www.bcn.cat/ABC

Animal Biodiversity and Conservation 29.2 (2006)

91

Morphometric analysis of population samples of soldier caste of Odontotermes obesus (Rambur) (Isoptera, Termitidae, Macrotermitinae) F. Manzoor & M. S. Akhtar

Manzoor, F. & Akhtar, M. S., 2006. Morphometric analysis of population samples of soldier caste of Odontotermes obesus (Rambur) (Isoptera, Termitidae, Macrotermitinae). Animal Biodiversity and Conservation, 29.2: 91–107.

Abstract Morphometric analysis of population samples of soldier caste of Odontotermes obesus (Rambur) (Isoptera, Termitidae, Macrotermitinae).— In order to study morphometric variations in Odontotermes obesus (Rambur), samples from nineteen nests were statistically analyzed for mean, standard deviation, standard error, coefficient of variability and confidence interval (95%) and analysis of variance (Model II ANOVA), The mean values of the different population samples were compared with the student t–test, following the Minitab version and Sokal & Rohlf (1973). In the study of external characters, measurements form a very important component, particularly for identification of species. However, the reliability of the measurements depends on the extent of variability which the structures show within and between colonies. For each individual soldier, the following nine parameters were measured: i) length of head; ii) width of head at mandibles; iii) width of head at the posterolateral ends of antennal carinae; iv) maximum width of head; v) length of left mandible; vi) tooth of left mandible from tip; vii) length of pronotum; viii) width of pronotum; ix) length of postmentum; and x) width of postmentum.

Key words: Termite, Soldier, Morphometric variability, Odontotermes obesus.

Resumen Análisis morfométrico de muestras de una población de la casta de las obreras de Odontotermes obesus (Rambur) (Isoptera, Termitidae, Macrotermitidae).— Con el objetivo de estudiar las variaciones morfométricas en Odontotermes obesus (Rambur), se analizaron estadísticamente muestras de diecinueve nidos, obteniéndose sus medias, desviaciones estándar, errores estándar, coeficientes de variabilidad e intervalos de confianza (95%) y análisis de varianza (Modelo II ANOVA). Los valores medios de las distintas muestras de las poblaciones se compararon mediante el test t de Student, según la versión Minitab y Sokal & Rohlf (1973).

En el estudio de los caracteres externos se midieron componentes muy importantes, particularmente para la identificación de la especie. Sin embargo, la fiabilidad de las mediciones depende de la cantidad de variabilidad de dichas estructuras dentro de cada colonia y entre colonias. En cada soldado se midieron los siguientes nueve parámetros: i) longitud de la cabeza, ii) ancho de la cabeza al nivel de las mandíbulas, iii) ancho de la cabeza en los extremos posterolaterales de las carinas antenales, iv) ancho máximo de la cabeza, v) longitud de la mandíbula izquierda, vi) diente de la mandíbula izquierda desde la punta, vii) longitud del pronoto, viii) ancho del pronoto, ix) longitud el postmentón, y x) ancho del postmentón.

Palabras clave: Termita, Soldado, Variabilidad morfométrica, Odontotermes obesus.

(Received: 29 III 05; Conditional acceptance: 19 X 05; Final acceptance: 13 XII 05) Farkhanda Manzoor, Dept. of Zoology, Lahore College for Women Univ., Lahore, Pakistan.– Muhammad Saeed Akhtar, Univ. of the Punjab, Q. A. Campus, Lahore, Pakistan.

Corresponding author: Farkhanda Manzoor. E–mail: doc_farkhanda@yahoo.com ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

92

Introduction Odontotermes obesus (Rambur) is widely distributed in Pakistan, Bangladesh and India (Akhtar, 1972, 1975; Chhotani, 1997). It is of great significance and feeds on wood, surface debris such as twigs, bark fragments, dry leaves and grasses. It is a common wood eater, damaging firewood, floor timber, wooden boxes, baskets and railway sleepers (Akhtar, 1991). In Pakistan this species has also been recorded to damage woodwork in buildings in various ecological areas. It attacks houses in villages more commonly than in urban areas (Akhtar, 1981, 1991).

The morphological features of termites are very important in termite taxonomy and classification and only a few studies on morphometric variations have been made (Ahmad, 1949; Roonwal, 1970; Chhotani & Das, 1979; Chhotani, 1981; Akhtar & Anwar, 1991; Akhtar & Ahmad, 1992; Coronel & Porcel (2002).

There are several forms of this species, and the relationship between the population samples is described here for the first time, using the Manhattan distance (Mayr & Ashlolck, 1991).

The morphometric analysis of O. obesus presented in this paper provides a standard of comparison for specimens from different localities in the range of this species and other species of the genus. The photographs of the specimens have also been prepared to present the exact morphological appearance of various taxonomic characters. Another aim of this study was to determine whether different populations can be differentiated statistically by measurements and indices calculated for the imago and soldier caste. Internest and intranest comparisons were made.

The objective of this work was to contribute to the taxonomic knowledge of this species by means of the study of intracolonial and intercolonial variations in the soldier caste.

Material and methods The study was based on material available in the collection of Prof. Dr. Muzaffar Ahmad, presently in the custody of Prof. Dr. M. Saeed Akhtar. Specimens from the samples were selected at random and measured under stereoscopic binocular microscope with a built–in magnification changer. Measurements were taken with the aid of a calibrated ocular micrometer. Diagrams of the mandible and postmentum were prepared with the help of Olympus Binoculars with attached camera.

Taxonomic terms and measurements used in the present study are as explained by Emerson (1945, 1952), Ahmad (1965) and Akhtar (1975). Population samples of the species collected from the geographic range of the species were compared using the Manhattan distance (Mayr & Ashlock, 1991) to highlight similarities and differences between population samples.

Manzoor & Akhtar

To determine the Manhattan distance, ranges were coded as three characters. The character range of the maximum number of individuals was coded as one, less than this range as zero and more than that range as two. Several absolute differences between the character state of each character for each possible pair of population samples collected from different localities were then determined.

Soldier: 1. The length of mandible is the distance from the condyle to the tip; 2. The tooth is measured from its tip to the base; 3. The length of the postmentum is the median length of the sclerotized portion.

Indices: 1. Mandibular tooth index (TLT/LLM) is the distance of tooth of left mandible from tip/length of left mandible; 2. Head mandibular index (LLM/ LHSBM) is the length of left mandible/length of head to side base of mandible; 3. Head width mandibular index (LLM/MWH) is the length of left mandible/maximum width of head.

Examined material Pakistan A. Lahore, soldiers and workers, collected by Ghani, 6 IV 1970, determined by M. S. Akhtar; B. Hangu, soldiers and workers, collected by M. S. Akhtar from ex–soil, 14 IX 1969; C. Lahore, i) soldiers and workers, collected by A. Aleem, 25 I 1968, from a mound, determined by M. S. Akhtar, ii) soldiers and workers, collected by A. Aleem, from a cow–dung, 24 II 1968, determined by M. S. Akhtar, iii) soldiers and workers, collected by A. Aleem, from roots of a tree, 24 II 1968, determined by M. S. Akhtar; E. Lahore, soldiers and workers, collected by A. Aleem, from mound, 25 I 1968; G. Dalwal Rukh forest, soldiers and workers, collected and determined by M. S. Akhtar, from dung, 23 III 1968; H. Rawalpindi, soldiers and workers, collected by N. K. Malik, from Shisham, 10 X 1968, determined by M. S. Akhtar; J. Chhanga Manga, i) soldiers and workers, collected by A. Aleem, in a log, 9 I 1968, determined

by M. S. Akhtar, ii) soldiers and workers, collected

by A. Aleem, from stump of a tree, 10–11 I 1968, determined by M. S. Akhtar, iii) soldiers and workers, collected by A. Aleem, from stump of a Mulberry tree, 9 I 1968, determined by M. S. Akhtar.

India F. Hoshiarpur (latitude 31° 30’ N, longitude 75° 59’ E), soldiers and workers, collected by T. Ahmad, in the ground, 4 IX 1980. I. Sujanpur (latitude 32° 19’ N, longitude 75° 38’ E), soldiers and workers, collected by T. Ahmad, 21 VI 1929, 23 XI 1929.

Bangladesh D. Chaumahani (latitude 22° 56’ N, longitude 91° 07’ E), soldiers and workers, collected by Fletcher, from a mound, 7 XII 1911; K. Noakhali (latitude 22° 45’ N, longitude 91° 08’ E), soldiers and workers, collected by N. K. Malik, in a mound, 20 I 1970, determined by M. S. Akhtar; L. Dinajpur,

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soldiers and workers, collected by N. K. Malik, 22 XII 1969, determined by M. S. Akhtar; M. Rasulpur (latitude 28° 42’ N, longitude 77°01’ E), soldiers and workers, collected by N. K. Malik, in a mound, 8 I 1970, determined by M. S. Akhtar; N. Singra (latitude 24° 30’ N, longitude 89° 12’ E), soldiers and workers, collected by N. K. Malik, in a mound, from a tree Bonia, 28 XII 1969, 25, 28 XII 1969, determined by M. S. Akhtar; O. Titalya (latitude 26° 30’ N, longitude 88° 20’ E), soldiers and workers, collected by N. K. Malik, in a mound, 3 XII 1969, determined by M. S. Akhtar; P. Chandpur (latitude 22° 07’ N, longitude 91° 54’ E), soldiers and workers, collected by N. K. Malik, in a mound, 19 I 1970, determined by M. S. Akhtar; Q. Sripur (latitude 24° 12’ N, longitude 90° 29’ E), soldiers and workers, collected by N. K. Malik, from cow– dung, 31 X 1968, determined by M. S. Akhtar; R. Rajshahi (latitude 24° 25’ N, longitude 88° 34’ E), soldiers and workers, collected by N. K. Malik, in a mound, 6 I 1970, determined by M. S. Akhtar; S. Barisal (latitude 22° 40’ N, longitude 90° 23’ E), soldiers and workers, collected by N. K. Malik, in a mound, determined by M. S. Akhtar.

Results Odontotermes obesus (Rambur) Termes obesus: Rambur, 1842 Odontotermes obesus: Krishna, 1965; Chatterjee & Thakur, 1967; Roonwal & Chhotani, 1967; Roonwal, 1970; Akhtar, 1974, 1975; Thakur, 1981 (considers O. assamensis Holmgren, O. bangalorensis Holmgren, O. flavonaculatus Holmgren et Holmgren, O. obesus var. oculatus Silvestri, O. vashino Bose as junior synonym of O. obesus); Verma & Thakur, 1982; Bose & Das, 1982, 1987; Bose, 1984; Bose & Roy, 1984; Verma, 1984; Akhtar & Anwar, 1991; Chhotani, 1997 [considers O. assamensis Holmgren, O. bangalorensis Holmgren, O. flavomaculatus Holmgren & Holmgren, O. obesus var. oculatus Silvestri and Termes (Cyclotermes) orissae Snyder as junior synonyms of O. obesus] Termes obesus (Cyclotermes) orissae: Snyder, 1934

Soldier (fig. 1, 2; tables 1–4) The soldier of O. obesus (Rambur) is characterized by an oval head capsule, weakly converging anteriorly. Mandibles long, slender, saber–shaped.

Left mandible with a sharp, prominent tooth at distal 1/3. Postmentum subrectangular.

Internest comparisons revealed significant differences between samples collected from different localities for the parameters: length of head to side base of mandible (F = 24.90; df = 18.134; P < 0.05); width of head at side base of mandible (F = 30.69; df = 18.134; P < 0.05); width of head at the posterolateral ends of antennal carinae (F = 22.67; df = 18.134 P < 0.05); maximum width of head (F = 11.69; df = 18.134; P < 0.05); length of left mandible (F = 15.65; df = 18.134; P < 0.05); tooth of left mandible from tip (F = 28.02; df = 18.134; P < 0.05); length of pronotum (F = 36.57; df = 18.134; P < 0.05); width of pronotum (F = 25.08; df = 18.134; P < 0.05);

length of postmentum (F = 44.69; df = 18.134; P < 0.05); width of postmentum (F = 18.21; df = 18.134; P < 0.05), (table 1).

More variations were recorded in tooth of left mandible from tip and length of postmentum. The coefficient of variability for tooth of left mandible from tip varied from 2.65–11.60 (table 2). However, for the pooled data, the coefficient of variability was 13.60 (table 2). The coefficient of variability for length of postmentum varied from 1.05–9.86 (table 3) and for the pooled data it was 12.70 (table 3).

The length of the postmentum is a very important character. Internest variations are shown in figure 2. For the pooled data, the lowest value of coefficient of variability (CV = 5.27) was recorded for a maximum width of head (table 2). As regards frequency distribution of specimens for length of postmentum based on 153 specimens, maximum number of specimens (39) measured 0.82–0.86 mm.

Similarly, other characters were measured for variability and are explained in tables 1 and 2.

On the basis of the Manhattan distance, population samples from locality A (Pakistan: Lahore) and G (Pakistan: Dalwal Rukh) form a primary cluster at value of 2; locality samples M (Bangladesh: Rasulpur) and S (Bangladesh: Barisal) form the second primary cluster at value of 2; locality samples Q (Bangladesh: Sripur) and L (Bangladesh: Dinajpur) form third primary cluster at value of 2; locality samples B (Pakistan: Hangu) and R (Bangladesh: Rajshahi) form fourth primary cluster at value of 2; locality samples P (Bangladesh: Chandpur) and O (Bangladesh: Titalya) form fifth primary cluster at value of 4; locality samples D (Bangladesh: Chaumahani) and H (Pakistan: Rawalpindi) form sixth primary cluster at value of 8 (table 5); locality sample F (India: Hoshiarpur) forms the secondary cluster with AG at value of 4; locality sample J (Pakistan: Chhanga Manga) forms the second secondary cluster with MS at value of 4; locality sample N (Bangladesh: Singra) forms the third secondary cluster with BR at value of 5; locality sample I (India: Sujanpur) joins another secondary cluster with PO at value of 6; locality sample K (Bangladesh: Noakhali) joins QL at value of 4; pairs AGF and MSJ are joined to form tertiary cluster at value of 6.24; pairs BRN and QLK again join to form another tertiary cluster at value of 5.88; pairs AGFMSJ and BRNQLK are joined at value of 8.61; pair DH join AGFMSJBRNQLK at value of 8.16; pair POI join AGFMSJBRNQLK at an average value of 9.21, the value at which last separate clusters are joined (fig. 3).

Discussion The length of the left mandible varied from 0.74– 1.17 mm in the pooled data (table 2). The tooth of the left mandible from the tip varied from 0.20– 0.40 mm (table 2), and most of the samples showed overlapping. The highest tooth distance was recorded for sample C (Lahore) (table 1).

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Manzoor & Akhtar

A

B

H

I

J

N

O

Q

C

Fig. 1. Variations in head capsule of soldiers of O. obesus (Rambur): A. Pakistan: Lahore (x 10); B. Pakistan: Hangu (x 10); C. Lahore (x 10); D. Bangladesh: Chaumahani (x 10); F. India: Hoshiarpur (x 10); G. Pakistan: Dalwal Rukh (x 10); H. Pakistan: Rawalpindi (x 10); I. India: Sujanpur (x 10); J. Pakistan: Chhanga Manga (x 10); K. Bangladesh: Noakadi (x 12); L. Bangladesh: Dinjapur (x 12); M. Bangladesh: Rasulpur (x 10); N. Bangladesh: Singra (x 12); O. Bangladesh: Titalya (x 12); Q. Bangladesh: Sripur (x 12); R. Bangladesh: Rajshashi (x 12); S. Bangladesh: Barisal (x 12).

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D

F

G

K

L

M

S R

S

Fig. 1. Variaciones de la capsula cefรกlica de las hormigas soldado of O. obesus (Rambur): A. Pakistan: Lahore (x 10); B. Pakistan: Hangu (x 10); C. Lahore (x 10); D. Bangladesh: Chaumahani (x 10); F. India: Hoshiarpur (x 10); G. Pakistan: Dalwal Rukh (x 10); H. Pakistan: Rawalpindi (x 10); I. India: Sujanpur (x 10); J. Pakistan: Chhanga Manga (x 10); K. Bangladesh: Noakadi (x 12); L. Bangladesh: Dinjapur (x 12); M. Bangladesh: Rasulpur (x 10); N. Bangladesh: Singra (x 12); O. Bangladesh: Titalya (x 12); Q. Bangladesh: Sripur (x 12); R. Bangladesh: Rajshashi (x 12); S. Bangladesh: Barisal (x 12).

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A

B

A

J

L

K

P

Q

Fig. 2. Variations in postmentum of soldiers of O. obesus (Rambur): A. Pakistan: Lahore (x 15); B. Pakistan: Hangu (x 15); E. Lahore (x 15); H. Pakistan: Rawalpindi (x 15); I. India: Sujanpur (x 15); J. Pakistan: Chhanga Manga (x 20); K. Bangladesh: Noakadi (x 20); L. Bangladesh: Dinjapur (x 20); M. Bangladesh: Rasulpur (x 20); N. Bangladesh: Singra (x 20); O. Bangladesh: Titalya (x 20); P. Bangladesh: Chandpur (x 20); Q. Bangladesh: Sripur (x 20); R. Bangladesh: Rajshashi (x 20).

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E

H

I

M

N

O

R

Fig. 2. Variaciones en el postmentum de las hormigas soldado de O. obesus (Rambur): A. Pakistan: Lahore (x 15); B. Pakistan: Hangu (x 15); E. Lahore (x 15); H. Pakistan: Rawalpindi (x 15); I. India: Sujanpur (x 15); J. Pakistan: Chhanga Manga (x 20); K. Bangladesh: Noakadi (x 20); L. Bangladesh: Dinjapur (x 20); M. Bangladesh: Rasulpur (x 20); N. Bangladesh: Singra (x 20); O. Bangladesh: Titalya (x 20); P. Bangladesh: Chandpur (x 20); Q. Bangladesh: Sripur (x 20); R. Bangladesh: Rajshashi (x 20).

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Table 1. Internest morphometric variations in taxonomic parameters of the soldier caste of O. obesus (Rambur). Samples followed by similar letters indicate non–significant differences in mean values by t–test (P > 0.05): Ns. Nest sample; N. Number of samples; OR. Observed range; X. Mean; SD. Standard deviation; SE. Standard error; CI. Confidence Interval; CV. Coefficient of variance.

Tabla 1. Variaciones morfométricas entre nidos de parámetros taxonómicos de la casta de los soldados de O. obesus (Rambur). Las muestras que van seguidas de letras indican diferencias no significativas de los valores medios según el test t (P > 0,05): Ns. Muestra nido; N. Número de muestras; OR. Rango observado; X. Media; SD. Desviación estándar; SE. Error estándar; CI. Intervalo de confianza; CV. Coeficiente de varianza.

Ns

N

OR

X

SD

SE

95% CI

CV

Length of head to side base of mandibles (F = 24.90; df = 18.134; P < 0.05) Aa

10

1.25–1.37

1.3120

0.0379

0.0120

1.2848–1.3392

2.88

Bb

2

1.55–1.57

1.5600

0.0141

0.0100

1.4329–1.6871

0.90

Cbc

10

1.42–1.60

1.5270

0.0523

0.0165

1.4896–1.5644

3.42

Dd

4

1.37–1.47

1.4300

0.0432

0.0216

1.3613–1.4987

3.02

Ebde

10

1.34–1.50

1.4510

0.0669

0.0212

1.4031–1.4989

4.61

adf

10

1.25–1.46

1.3590

0.0714

0.0226

1.3079–1.4101

5.25

3

1.37–1.55

1.4300

0.1039

0.0600

1.1718–1.6882

7.26

F

Gbdefg Hafgh

2

1.30–1.35

1.3250

0.0354

0.0250

1.0073–1.6427

2.67

Ibcghi

10

1.40–1.60

1.5190

0.0601

0.0215

1.4703–1.5677

4.48

J

10

1.19–1.33

1.2500

0.0481

0.0152

1.2156–1.2844

3.84

Kbcdegik

10

1.42–1.56

1.4920

0.0518

0.0164

1.4549–1.5291

3.47

bcdegikl

10

1.33–1.58

1.4830

0.0780

0.0247

1.4272–1.5388

5.25

L

afh

10

1.27–1.35

1.31800

0.02348

0.0072

Ncegikln

10

1.44–1.56

1.4900

0.0316

0.0100

1.4674–1.5126

2.12

M

1.30120–1.33480 1.78

bcio

4

1.50–1.64

1.5950

0.0661

0.0330

1.4899–1.7001

4.14

Pbcio

10

1.54–1.64

1.5480

0.0518

0.0164

1.5109–1.5851

3.34

1.4507–1.5193

2.76

O Q

cdegiklnq

8

1.40–1.52

1.4850

0.0411

0.0145

Regiklnq

10

1.46–1.52

1.48800

0.01932

0.00611

Sdeg

10

1.35–1.48

1.4180

0.0434

0.0137

1.47417–1.50183 1.29 1.3869–1.4491

3.06

0.0127

0.7473–0.8047

5.16

Width of head at sidebase of mandibles (F = 30.69; df = 18.134; P < 0.05) Aa

10

0.75–0.85

0.7760

0.0401

B

2

0.90

0.90000

0.00000

0.00000

0.90000–0.90000

Cc

10

0.82–0.90

0.85400

0.02716

0.00859

0.83456–0.87344 3.18 0.90744–0.96256 1.85

D

4

0.92–0.95

0.93500

0.01732

0.00866

Eae

10

0.75–0.87

0.7910

0.0567

0.0179

0.7505–0.8315

aef

F

–

7.16

10

0.75–0.85

0.7930

0.0359

0.0114

0.7673–0.8187

4.52

Gaefg

3

0.75–0.82

0.7800

0.0361

0.0208

0.6904–0.8696

4.62

H

2

0.75

0.75000

0.00000

0.00000

0.75000–0.75000

c

10

0.85–0.92

0.87600

0.01955

0.00618

0.86201–0.88999 2.23

Jj

10

0.67–0.76

0.7080

0.0319

0.0101

k

10

0.72–0.78

0.74000

0.01633

0.00516

0.72832–0.75168 2.20

Laefgl

10

0.76–0.82

0.78400

0.02951

0.00933

0.76288–0.80512 3.76

M

10

0.65–0.72

0.67100

0.01912

0.00605

0.65732–0.68468 2.84

Naefgln

10

0.76–0.82

0.80200

0.02201

0.00696

0.78625–0.81775 2.74

4

0.76–0.86

0.8100

0.0476

0.0238

I

K

O

aefglno

0.6852–0.7308

0.7342–0.8858

– 4.50

5.87

99

Animal Biodiversity and Conservation 29.2 (2006)

Table 1. (Cont.)

Ns P

aefglnop

Q

aegklp

N

OR

X

SD

SE

10

0.72–0.82

0.7800

0.0377

0.0119

95% CI

CV

0.7530–0.8070

4.83

8

0.72–0.78

0.75500

0.02777

0.00982

0.73177–0.77823 3.67

Reo

10

0.80–0.84

0.82000

0.01333

0.00422

0.81046–0.82954 1.62

jk

10

0.70–0.78

0.72200

0.02394

0.00757

0.70487–0.73913 3.31

S

Width of head at the posterolateral ends of antennal carinae (F = 22.67; df = 18.134; P < 0.05) Aa

10

0.97–1.10

1.0070

0.0340

0.0108

0.9827–1.0313

3.37

Bab

2

1.00–1.02

1.0100

0.0141

0.0100

0.8829–1.1371

1.39

Cc

10

1.05–1.12

1.08400

0.03026

0.00957

1.06235–1.10565 2.79

Dcd

4

1.10–1.12

1.11000

0.01155

0.00577

1.09163–1.12837 1.04

Ede

10

1.05–1.25

1.1670

0.0707

0.0224

abf

10

1.00–1.10

1.0340

0.0320

0.0101

1.0111–1.0569

3.09

3

1.00–1.10

1.0400

0.05129

0.0306

0.9086–1.1714

5.08

F

Gabcfg Hbgh

1.1164–1.2176

6.05

2

0.87–0.97

0.9200

0.0707

0.0500

0.2847–1.5553

7.68

Idei

10

1.07–1.20

1.1570

0.0427

0.0135

1.1264–1.1876

3.69

hj

J

10

0.94–0.96

0.95600

0.00843

0.00267

Kcdegk

10

1.03–1.19

1.1070

0.0589

0.0186

1.0649–1.1491

5.32

cdgkl

10

1.03–1.17

1.0990

0.0428

0.0135

1.0684–1.1296

3.89

bhj

10

0.92–1.03

0.9590

0.0390

0.0123

0.9311–0.9869

4.06

Ncdkln

10

1.05–1.15

1.10700

0.03129

0.00989

L

M

Oeiko Pdeiklnop Q

cdklnq

Rcdklnpq S

bfg

0.94997–0.96203 0.88

1.08461–1.12939 2.82

4

1.13–1.19

1.1550

0.0300

0.0150

1.1073–1.2027

2.59

10

1.05–1.17

1.1210

0.0463

0.0146

1.0879–1.1541

4.13

8

1.07–1.11

1.08875

0.01808

0.00639

1.07363–1.10387 1.66

10

1.07–1.15

1.10400

0.03134

0.00991

1.08157–1.12643 2.83

10

1.00–1.08

1.05000

0.02906

0.00919

1.02921–1.07079 2.76

Maximum width of head (F = 11.69; df = 18.134; P < 0.05) Aa

10

1.07–1.33

1.1850

0.0896

0.0283

ab

2

1.21–1.27

1.2400

0.0424

0.0300

Cbc

10

1.25–1.31

1.27600

0.02503

0.00792

B

1.1209–1.2491

7.56

0.8588–1.6212

3.41

1.25809–1.29391 1.96

Dabcd

4

1.17–1.38

1.2925

0.0881

0.0440

1.1523–1.4327

6.81

Ebcde

10

1.19–1.29

1.2520

0.0346

0.0109

1.2273–1.2767

2.76

abf

10

1.15–1.23

1.19600

0.03134

0.00991

3

1.19–1.23

1.2167

0.0231

0.0133

1.1593–1.2740

F

Gabfg

1.17357–1.21843 2.62 1.89

bgh

2

1.27

1.27000

0.00000

0.00000

1.27000–1.27000

Ibcde

10

1.23–1.29

1.26200

0.02150

0.00680

1.24662–1.27738 1.70

Jh

10

1.29–1.40

1.3310

0.0335

0.0106

H

K

abfghk

–

1.3070–1.3550

2.51

1.2192–1.2728

3.00

10

1.19–1.31

1.2460

0.0375

0.0119

Labfgkl

10

1.19–1.25

1.22800

0.02573

0.00814

1.20959–1.24641 2.09

Magklm

10

1.11–1.15

1.13200

0.01751

0.00554

1.11947–1.14453 1.54

Nabeln

10

1.13–1.25

1.1940

0.0460

0.0145

O

abcdefgklmno

Pabcgklmop Q R

abghklmo

abdeklno

Sagklmop

1.1611–1.2269

3.85

4

1.25–1.31

1.2800

0.0258

0.0129

1.2389–1.3211

2.01

10

1.19–1.35

1.2500

0.0422

0.0133

1.2198–1.2802

3.37

8

1.17–1.23

1.20000

0.02619

0.00926

10

1.15–1.29

1.2400

0.0455

0.0137

10

1.13–1.21

1.17600

0.02675

0.00846

1.17810–1.22190 2.18 1.2089–1.2711

3.50

1.15686–1.19514 2.27

100

Manzoor & Akhtar

Table 1. (Cont.)

Ns

N

OR

X

SD

SE

95% CI

CV

Length of left mandible (F = 15.65; df = 18.134; P < 0.05) Aa

10

0.97–1.00

0.99700

0.00949

0.00300

b

2

1.00–1.07

1.0350

0.0495

0.0350

10

1.05–1.12

1.08400

0.03026

0.00957

1.06235–1.10565 2.79 1.04909–1.08091 0.93

B

C

bc

D

bcd

0.99021–1.00379 0.95 0.5903–1.4797

4.78

4

1.05–1.07

1.06500

0.01000

0.00500

Ebcde

10

1.00–1.17

1.0550

0.0643

0.0203

af

10

0.95–1.00

0.98900

0.01853

0.00586

3

0.85–1.00

0.9400

0.0794

0.0458

0.7428–1.1372

8.44

F

G

bdefg

H

6.09

0.97574–1.00226 1.87

2

0.87–0.90

0.8850

0.0212

0.0150

0.6944–1.0756

2.39

10

1.00–1.10

1.0710

0.0398

0.0126

1.0425–1.0995

3.71

d

10

0.84–0.90

0.87000

0.01944

0.00615

abdegik

10

0.74–1.00

0.9480

0.0744

0.0235

0.8948–1.0012

abegkl

Ibcdei J

1.0090–1.1010

K L

0.85609–0.88391 2.23 7.84

10

0.86–1.03

0.9850

0.0504

0.0159

0.9489–1.0211

5.11

M

10

0.92–1.03

0.9590

0.0390

0.0123

0.9311–0.9869

4.06

Nabfgln

10

0.96–1.08

1.0210

0.0373

0.0118

0.9943–1.0477

3.65

abdeiko

4

0.94–1.07

1.0000

0.0606

0.0303

0.9036–1.0964

6.06

degiklop

10

0.94–1.00

0.96200

0.02573

0.00814

8

0.94–1.00

0.9475

0.0399

0.0141

0.9141–0.9809

4.21

bdegiklopq

10

0.96–1.07

1.0260

0.0375

0.0119

0.9992–1.0528

3.65

fn

10

0.90–0.98

0.95600

0.02633

0.00833

O P

Qfgnq R S

0.94359–0.98041 2.67

0.93716–0.97484 2.75

Tooth of left mandible from tip (F = 28.02; df = 18.134; P < 0.05) Aa B

ab

10

0.35

0.35000

0.00000

0.00000

0.35000–0.35000

–

2

0.35–0.37

0.3600

0.0141

0.0100

0.2329–0.4871

a

10

0.37

0.37000

0.00000

0.00000

0.37000–0.37000

–

Da

4

0.25

0.25000

0.00000

0.00000

0.25000–0.25000

–

Eabe

10

0.35–0.37

0.36400

0.00966

0.00306

0.35709–0.37091 2.65

abef

10

0.35–0.37

0.35600

0.00966

0.00306

0.34909–0.36291 2.71

befg

3

0.30–0.37

0.3467

0.0404

0.0233

0.2463–0.4471

2

0.32

0.32000

0.00000

0.00000

0.32000–0.32000

C

F

G

Heh I

abfgi

3.91

11.60 –

10

0.32–0.40

0.36600

0.02716

0.00859

0.34656–0.38544 7.42

bj

10

0.28–0.35

0.29500

0.02369

0.00749

0.27805–0.31195 8.03

jk

10

0.26–0.35

0.30300

0.02751

0.00870

0.28332–0.32268 9.07

Lbfgil

10

0.28–0.37

0.34000

0.02944

0.00931

0.31893–0.36107 8.65

m

10

0.20–0.28

0.26000

0.02494

0.00789

0.24215–0.27785 9.59

bgln

10

0.30–0.35

0.33400

0.02171

0.00686

0.31847–0.34953

6.5

0.2791–0.3709

8.89

J

K

M N

O

bgjklnoh

4

0.30–0.35

0.3250

0.0289

0.0144

Pmp

10

0.22–0.30

0.26200

0.02201

0.00696

0.24625–0.27775 8.40

Qjkq

0.01773

0.00627

0.27017–0.29983 6.22

8

0.26–0.30

0.28500

abefgilno

10

0.32–0.39

0.34900

0.02961

0.00936

0.32781–0.37019 8.48

Sefgijklmnopq

10

0.26–0.30

0.284

0.01578

0.00499

0.27271–0.29529 5.55

R

101

Animal Biodiversity and Conservation 29.2 (2006)

Table 1. (Cont.)

Ns

N

OR

X

SD

SE

95% CI

CV

Length of pronotum (F = 36.57; df = 18.134; P < 0.05) Aa B

ab

C

c

10

0.55–0.60

0.57400

0.02366

0.00748

2

0.57–0.60

0.5850

0.0212

0.0150

0.55707–0.59093 4.12 0.3944–0.7756

3.62

10

0.62–0.67

0.64700

0.02058

0.00651

0.63228–0.66172 3.18

Dcd

4

0.62–0.65

0.62750

0.01500

0.00750

0.60363–0.65137 2.39

Ecd

10

0.62–0.75

0.6800

0.0506

0.0160

bdf

10

0.57–0.65

0.60800

0.02781

0.00879

3

0.57–0.60

0.5800

0.0173

0.0100

0.5370–0.6230

2.98

2

0.57–0.60

0.5850

0.0212

0.0150

0.3944–0.7756

3.62

10

0.60–0.65

0.62000

0.01826

0.00577

0.60694–0.63306 2.94

F

Gabg H I

abfgh

df

0.6438–0.7162

7.44

0.58810–0.62790 4.57

J

10

0.47–0.51

0.48200

0.01398

0.00441

0.47199–0.49201 2.90

Kabghk

10

0.55–0.61

0.57200

0.02201

0.00696

0.55625–0.58775 3.84

L

l

10

0.55–0.57

0.55400

0.00843

0.00267

0.54797–0.56003 1.52

m

10

0.51–0.57

0.53000

0.02108

0.00667

0.51491–0.54509 3.93

ln

10

0.53–0.57

0.55000

0.01633

0.00516

0.53832–0.56168 2.96

4

0.57–0.59

0.57500

0.01000

0.00500

0.55909–0.59091 1.73

M N

Oabghko Pbfh

10

0.59–0.61

0.59800

0.01033

0.00327

0.59061–0.60539 1.72

abghkoq

8

0.57–0.59

0.57600

0.00966

0.00306

0.56909–0.58291 1.67

abghkoqr

10

0.55–0.59

0.57000

0.01333

0.00422

0.56046–0.57954 2.33

Sabghklmnor

10

0.53–0.59

0.55200

0.02573

0.00814

0.53359–0.57041 4.66

Q R

Width of pronotum (F = 25.08; df = 18.134; P < 0.05) Aa

10

0.90–1.00

0.9610

0.0373

0.0118

0.9343–0.9877

3.88

0.8829–1.1371

1.39

ab

2

1.00–1.02

1.0100

0.0141

0.0100

Cbc

10

1.02–1.07

1.03900

0.02132

0.00674

1.02375–1.05425 2.05

Dbcd

4

1.00–1.02

1.01500

0.01000

0.00500

0.99909–1.03091 0.98

B

E

10

1.00–1.07

1.03300

0.02830

0.00295

1.0275–1.05825

Fabdf

10

0.95–1.02

0.98700

0.02627

0.00831

0.96820–1.00580 2.66

Gag

3

0.92–0.95

0.9300

0.0173

0.0100

0.8870–0.9730

1.86

2

0.92–0.95

0.9350

0.0212

0.0150

0.7444–1.1256

2.26

H

agh

2.73

abfi

10

0.95–1.00

0.98500

0.02173

0.00687

Jghj

10

0.82–0.96

0.8900

0.0445

0.0141

0.8582–0.9218

5.00

bcdk

10

0.96–1.07

1.0160

0.0347

0.0110

0.9912–1.0408

3.41

bdfk

10

0.98–1.03

1.00700

0.01703

0.00539

0.99481–1.01919 1.69

10

0.88–0.96

0.91800

0.83048

0.00964

0.89619–0.93981 3.32

10

0.88–0.98

0.9140

0.0327

0.0103

0.8906–0.9374

3.57

4

1.03–1.08

1.0525

0.0263

0.0131

1.0107–1.0943

2.49

10

1.03–1.08

1.06800

0.02044

0.00646

1.05337–1.08263 1.91

I

K L

M

ghjm

Nghjn O P

bcko

o

Q

afi

Rabfhir S

abfghir

0.96945–1.00055 2.20

8

0.96–1.00

0.97500

0.01773

0.00627

0.96017–0.98983 1.81

10

0.92–1.00

0.97000

0.02539

0.00803

0.95184–0.98816 2.61

10

0.92–1.00

0.9640

0.0350

0.0111

0.9389–0.9891

3.63

102

Manzoor & Akhtar

Table 1. (Cont.)

Ns

N

OR

X

SD

SE

95% CI

CV

Length of postmentum (F = 44.69; df = 18.134; P < 0.05) Aa

10

0.67

0.67000

0.00000

0.00000

0.67000–0.67000

Bb

2

0.85–0.87

0.8600

0.0141

0.0100

0.7329–0.9871

Cbc

– 1.63

10

0.80–0.87

0.85700

0.02214

0.00700

d

4

0.75–0.80

0.7675

0.0236

0.0118

e

10

1.00–1.07

1.03500

0.02635

0.00833

Fbcdf

10

0.75–1.00

0.8190

0.0808

0.0255

0.7612–0.8768

9.86

bdfg

3

0.75–0.82

0.7967

0.0404

0.0233

0.6963–0.8971

5.07

bdfgh

D E

G H

0.84116–0.87284 2.58 0.7299–0.8051

3.07

1.01614–1.05386 2.54

2

0.75–0.82

0.7850

0.0495

0.0350

0.3403–1.2297

6.30

ei

10

0.95–1.12

1.0010

0.0689

0.0218

0.9517–1.0503

6.88

Ja

10

0.63–0.72

0.6660

0.0320

0.0101

0.6431–0.6889

4.80

dfghk

10

0.74–0.86

0.7880

0.0391

0.0124

0.7600–0.8160

4.96

bcfghl

10

0.72–0.92

0.8460

0.0633

0.0200

0.8007–0.8913

7.48

dfghk

10

0.67–0.80

0.7690

0.0384

0.0122

0.7415–0.7965

4.99

10

0.76–0.88

0.8180

0.0358

0.0113

0.7924–0.8436

4.37

0.94500

0.01000

0.00500

I

K L

M

Nbfghkln O

i

4

0.94–0.96

bcfghlnp

10

0.78–0.88

0.8460

0.0341

0.0108

Qbcfglnpq

8

0.80–0.86

0.84000

0.02390

0.00845

0.82001–0.85999 2.84

10

0.88–0.92

0.89600

0.01838

0.00581

0.88285–0.90915 2.16

10

0.74–0.88

0.8380

0.0426

0.0135

P

R S

bcfghlnpq

0.92909–0.96091 1.05 0.8216–0.8704

0.8075–0.8685

4.03

5.08

Width of postmentum (F = 18.21; df = 18.134; P < 0.05) Aa

10

0.47–0.50

0.47300

0.00949

0.00300

0.46621–0.47979 2.00

b

2

0.50

0.50000

0.00000

0.00000

0.50000–0.50000

10

0.47–0.50

0.49700

0.00949

0.00300

0.49021–0.50379 1.90

B

C

bc

D

–

4

0.40–0.42

0.40500

0.01000

0.00500

0.38909–0.42091 2.46

Ebce

10

0.50–0.55

0.50500

0.01581

0.00500

0.49369–0.51631 3.13

acf

10

0.47–0.52

0.48400

0.01897

0.00600

0.47042–0.49758 3.91

3

0.47

0.47000

0.00000

0.00000

0.47000–0.47000

– –

F

G H

a

bc

2

0.50

0.50000

0.00000

0.00000

0.50000–0.50000

Ibfi

10

0.47–0.50

0.48800

0.01549

0.00490

0.47691–0.49909 3.17

J

0.44799–0.46801 3.05

10

0.45–0.49

0.45800

0.01398

0.00442

bek

10

0.49–0.55

0.5140

0.0324

0.0102

bcekl

10

0.47–0.55

0.5140

0.0324

0.0102

Mbcefilm

10

0.47–0.51

0.49400

0.01265

0.00400

0.48495–0.50305 2.56

Nceiklmn

10

0.49–0.55

0.50200

0.01932

0.00611

0.48817–0.51583 3.84

K L

O

l

6.30

0.4908–0.5372

6.30

4

0.53–0.55

0.54500

0.01000

0.00500

0.52909–0.56091 3.84

10

0.49–0.53

0.52200

0.01398

0.00442

0.51199–0.53201 2.67

bceklnq

8

0.49–0.53

0.50750

0.01282

0.00453

0.49678–0.51822 2.52

bceklnqr

10

0.49–0.53

0.50600

0.01265

0.00400

0.49695–0.51505 2.50

bceklnqr

10

0.49–0.53

0.50800

0.01476

0.00467

0.49744–0.51856 2.90

Pkl Q R S

0.4908–0.5372

103

Animal Biodiversity and Conservation 29.2 (2006)

Table 2. Statistics for various parameters used in this study for O. obesus (Rambur), all localities combined: L(h–m). Length of head to sidebase of mandibles; W(h–m). Width of head at sidebase of mandibles; W(h–an). Width of head at the posterolateral ends of antennal carinae; Mhw. Maximum head width; Llm. Length of left mandible; T(lm–t). Tooth of left mandible from tip; Lp. Length of pronotum; Wpn. Width of pronotum; Lpm. Length of postmentum; W. Width of postmentum. (For other abbreviations see table 1.)

Tabla 2. Cálculos estadísticos de varios parámetros utilizados en este estudio de O. obesus (Rambur), combinándose todas las localidades: L(h–m). Longitud de la cabeza a la base lateral de las mandíbulas; W(h–m). Ancho de la cabeza a la base lateral de las mandíbulas; W(h–an). Ancho de la cabeza en los estremos de las carinas antenales; Mhw. Máxima anchura de la cabeza; Llm. Longitud de la mandíbula izquierda; T(lm–t). Dientes de la mandíbula izquierda desde la punta; Lp. Longitud del pronoto; Wpn. Ancho del pronoto; Lpm. Longitud del postmentum; W. Ancho del postmentum. (Para otras abreviaturas ver tabla 1.)

Parameters

OR

X

SD

SE

95% CI

CV

L(h–m)

153

N

1.19–1.64

1.44

0.1022741

0.008241484

1.42–1.45

7.10

W(h–m)

153

0.65–0.95

0.78

0.064866749

0.00522711

0.77–0.79

8.31

W(h–an)

153

0.87–1.25

1.06

0.069802265

0.005624826

1.05–1.07

6.58

Mhw

153

1.07–1.40

1.23

0.064924317

0.00523175

1.22–1.24

5.27

Llm

153

0.74–1.17

0.99

0.07917864

0.06380396

0.98–1.00

7.99

T(lm–t)

153

0.20–0.40

0.32

0.043712055

0.003522417

0.31–0.33

13.60

Lpn

153

0.47–0.75

0.58

0.050980477

0.004108123

0.57–0.59

8.78

Wpn

153

0.82–1.08

0.97

0.061157525

0.004928213

0.96–0.98

6.30

Lpm

153

0.63–1.12

0.84

0.107145218

0.008634007

0.82–0.86

12.70

Wpm

153

0.40–0.55

0.50

0.027658755

0.002228806

0.49–0.50

5.53

Table 3. Statistics of various indices used in this study for O. obesus (Rambur). (For abbreviations see table 1 and Examined material.)

Tabla 3. Cálculos estadísticos de varios índices utilizados en este estudio de O. obesus (Rambur).

(Para otras abreviaturas ver tabla 1 y Examined material.)

Ns

N

OR

X*

SD

SE

95% CI

CV

Mandibular tooth index (TLT/LLM) *(average mean value = 0.32) A

10

0.35–0.36

0.35

0.03

0.000948683

0.34–0.35

0.86

B

2

0.32–0.33

0.325

0.005

0.003535533

0.32–0.33

1.53

C

10

0.33–0.37

0.35

0.011874342

0.003754996

0.34–0.36

3.39

D

4

0.23–0.24

0.232

0.004330127

0.002165063

0.23–0.24

1.86

E

10

0.35–0.39

0.36

0.01248999

0.003949683

0.35–0.37

3.46

F

10

0.32–0.37

0.35

0.02002498

0.006332456

0.34–0.36

5.72

G

3

0.35–0.38

0.37

0.012472191

0.00720823

0.35–0.38

3.37

H

2

0.35–0.37

0.36

0.01

0.007071067

0.35–0.37

2.77

I

10

0.32–0.36

0.34

0.01264911

0.004

0.33–0.35

3.72

J

10

0.32–0.39

0.34

0.021540659

0.006811754

0.33–0.35

6.33

K

10

0.26–0.38

0.32

0.034351128

0.01086278

0.30–0.34

10.70

L

10

0.28–0.38

0.345

0.026551836

0.00839642

0.32–0.36

7.80

M

10

0.25–0.32

0.29

0.017578395

0.005558776

0.28–0.30

6.06

N

10

0.30–0.36

0.33

0.017349351

0.005486346

0.32–0.34

5.25

104

Manzoor & Akhtar

Table 3. (Cont.)

Ns

X*

SD

95% CI

CV

O

N 4

0.31–0.34

OR

0.32

0.011180339

0.003535533

SE

0.31–0.33

3.49

P

10

0.23–0.31

0.27

0.020712315

0.006549809

0.26–0.28

7.67

Q

8

0.28–0.35

0.30

0.024717149

0.008738832

0.28–0.31

8.23

R

10

0.31–0.38

0.34

0.022803508

0.007211102

0.32–0.35

6.70

S

10

0.26–0.32

0.30

0.02244994

0.007099295

0.29–0.31

7.48

0.75–0.78

2.93

Head mandibular index (LLM/LHSBM) (*average mean value = 0.68) A

10

0.73–0.80

0.765

0.022472205

0.07106335

B

2

0.64–0.69

0.665

0.025

0.07677669

0.63–0.70

3.78

C

10

0.64–0.74

0.682

0.029257477

0.09252025

0.66–0.70

4.30

D

4

0.71–0.78

0.74

0.025

0.0125

0.71–0.76

3.37

E

10

0.68–0.80

0.73

0.03522782

0.011140017

0.71–0.75

4.82

F

10

0.67–0.85

0.73

0.049487372

0.01564928

0.70–0.76

6.77

G

3

0.62–0.71

0.66

0.038586123

0.02227708

0.62–0.70

5.84

H

2

0.64–0.69

0.66

0.025

0.017677669

0.62–0.69

3.78

I

10

0.62–0.74

0.71

0.046518813

0.01471054

0.68–0.74

6.55

J

10

0.65–0.72

0.70

0.025317977

0.008006247

0.68–0.71

3.61

K

10

0.61–0.66

0.631

0.041097445

0.012996153

0.60–0.65

6.52

L

10

0.59–0.74

0.66

0.045431266

0.01436662

0.63–0.69

6.88

M

10

0.60–0.71

0.68

0.031368774

0.009919677

0.66–0.70

4.61

N

10

0.66–0.72

0.68

0.024576411

0.007771743

0.66–0.69

3.61

O

4

0.60–0.69

0.63

0.04602988

0.02301494

0.58–0.67

7.30

P

10

0.59–0.66

0.62

0.02491987

0.00788035

0.60–0.63

4.00

Q

8

0.58–0.68

0.63

0.029341736

0.0103787

0.61–0.65

4.65

R

10

0.68–0.73

0.69

0.023685438

0.007489993

0.67–0.70

3.43

S

10

0.65–0.70

0.67

0.01627882

0.005147815

0.66–0.68

2.40

0.79–0.82

3.45

Head width mandibular index (LLM/MWH) (*average mean value = 0.76) A

10

0.75–0.85

B

2

0.69–0.79

C

10

0.65–0.87

D

4

0.64–0.79

E

10

0.70–0.79

F

10

G

3

H I

0.81

0.027946377

0.00883742

0.74

0.05

0.035355339

0.67–0.81

6.75

0.80

0.0620

0.0196

0.75–0.84

7.75

0.71

0.053560713

0.026780356

0.66–0.76

7.54

0.74

0.025787593

0.008154753

0.72–0.75

3.48

0.70–0.82

0.75

0.032186953

0.010178408

0.73–0.77

4.29

0.76–0.80

0.78

0.016996731

0.009813067

0.76–0.80

2.17

10

0.64–0.80

0.72

0.040298883

0.012743625

0.69–0.74

5.59

10

0.74–0.83

0.79

0.024413111

0.007720103

0.77–0.80

3.09

J

10

0.72–0.82

0.75

0.032186953

0.010178408

0.73–0.77

4.29

K

10

0.72–0.80

0.75

0.023323807

0.007375635

0.73–0.76

3.10

L

10

0.72–0.81

0.75

0.033541019

0.010606601

0.73–0.77

4.47

M

10

0.72–0.82

0.77

0.037682887

0.011916375

0.75–0.79

4.89

N

10

0.70–0.91

0.79

0.062577951

0.019788885

0.75–0.83

7.92

O

4

0.70–0.79

0.76

0.0349106

0.011039701

0.72–0.79

4.59

P

10

0.71–0.80

0.75

0.025475478

0.008056053

0.73–0.76

3.39

Q

10

0.74–0.80

0.76

0.015620499

0.004939635

0.75–0.77

2.05

R

10

0.77–0.82

0.79

0.024576411

0.007771743

0.77–0.80

3.11

S

10

0.73–0.80

0.76

0.017776388

0.005621387

0.75–0.77

2.33

105

Animal Biodiversity and Conservation 29.2 (2006)

Table 4. Similarity matrix: Manhattan distance rearranged by similarity. (For abbreviations see Examined material.)

Tabla 4. Matriz de similitud: distancia de Manhattan reordenada por similitud. (Para las abreviaturas ver Examined material.)

A

G

F

M

S

H

B

D

Q

J

K

L

R

I

P

O

A

X

2

3

4

6

6

7

7

7

7

9

9

9

10

11

13

G

2

X

5

4

6

14

7

7

7

5

7

7

9

10

9

13

F

3

5

X

7

7

9

6

8

6

10

10

8

6

7

10

10

M

4

4

7

X

2

6

11

19

7

3

7

7

13

14

11

15

S

6

6

7

2

X

6

9

11

5

5

7

5

11

14

9

13

H

6

14

9

6

6

X

9

8

7

3

7

7

8

14

9

11

B

7

7

6

11

9

9

X

8

6

12

6

6

2

5

6

6

D

7

7

8

9

11

8

8

X

8

8

18

8

8

7

10

8

Q

7

7

6

7

5

7

6

8

X

10

4

2

6

9

4

8

J

7

5

10

3

5

3

12

8

10

X

8

8

14

15

12

14

N

8

10

9

8

6

10

5

10

5

11

7

5

5

18

7

7

K

9

7

10

7

7

7

6

18

4

8

X

4

6

9

4

8

L

9

7

8

7

5

7

6

8

12

8

4

X

6

9

4

8

R

9

9

6

13

11

8

2

8

6

14

6

6

X

8

4

8

I

10

10

7

14

14

14

5

7

9

15

9

9

8

X

7

5

P

11

9

10

11

9

9

6

10

4

12

4

4

4

7

X

4

O

13

13

10

15

13

11

6

8

8

14

8

8

8

5

4

X

For the pooled data, the highest value of coefficient of variability (CV = 13.60) was recorded for the tooth of the left mandible from the tip (table 2).

This is a highly variable character, as is the length of the postmentum (CV = 12.70).

The smallest sample (J) belonging to Chhanga Manga was collected by A. Aleem and was determined by M. S. Akhtar. Cluster analysis revealed that specimens from locality D (Bangladesh: Chaumahani) and H (Pakistan: Rawalpindi) are distantly related (fig. 3).

Thakur (1981) considers O. assamensis Holmgren, O. banglorensis Holmgren, O. flavomaculatus Holmgren et Holmgren, O. obesus var. oculatus Silvestri and O. vaishno Bose as junior synonym of O. obesus. Chhotani (1997) also treats O. assamensis Holmgren, O. banglorensis Holmgren, O. flavomaculatus Holmgren and Holmgren, O. obesus var. oculatus Silvestri and Termes (Cyclotermes) orissae Snyder, all these species as junior synonym of O. obesus. Ahmad (1958), Roonwal & Chhotani (1962) and Akhtar & Ahmad (1992) considered O. assamensis as a valid species. In the present study, internest variation was studied for the soldier caste. As these morphometric variations show many kinds of overlappings, further biochemical and karyotype studies are required to

decide whether O. obesus. is a sibling complex or not. The present studies however, show that O. obesus is a species which consists of a highly variable population.

Indices Mandibular tooth index (TLT/LLM) The index value varied from 0.23â&#x20AC;&#x201C;0.39. The mean values were 0.35, 0.325, 0.35, 0.23, 0.36, 0.35, 0.37, 0.36, 0.34,0.34, 0.32, 0.345, 0.29, 0.33, 0.32, 0.27, 0.30, 0.34 and 0.30 for locality samples A, B, C, D, E, F, G, H, I, J, K, L, M, N, O, P, Q, R and S, respectively (fig. 3). The sample from locality K (Noakhali) showed the highest value of coefficient of variability (CV = 10.70) (table 3).

Head mandibular index (LLM/LHSBM) The index values varied from 0.58â&#x20AC;&#x201C;0.85. The mean values were 0.76, 0.66, 0.68, 0.74, 0.73, 0.73, 0.66, 0.66, 0.71, 0.70, 0.63, 0.66, 0.68, 0.68, 0.63, 0.62, 0.63, 0.69 and 0.67 for locality samples A, B, C, D, E, F, G, H, I, J, K, L, M, N, O, P, Q, R and S, respectively (fig. 3). The sample from locality O (Bangladesh: Titalya) had the highest value of coefficient of variability (CV = 7.30) (table 3).

106

Manzoor & Akhtar

0 A 2

4

2

G F M 2 SJ B R 2

4

N

Q 2 L K

4

P 4 O

4

I

5 5.88

6

6

6.24

D

8

8.14 8.61

8

H

9.21

10

Fig. 3. Phenogram: Manhattan distance of the soldier samples of O. obesus (Rambur). Primary clusters are indicated by solid lines, secondary clusters by dotted lines and tertiary clusters by dashed lines and quaternary clusters by dashed–dotted lines. The scale on the left is a distance measure.

Fig. 3. Fenograma: distancia de Manhattan de las muestras de hormiga soldado de O. obesus (Rambur). Los grupos primarios se indican mediante líneas contínuas, los secundarios con líneas de puntos, los terciarios con líneas discontinuas y los cuaternarios con líneas discontínuas punteadas.

Head width mandibular index (LLM/MWH) The index values varied from 0.64–0.87. The mean values were 0.81, 0.74, 0.80, 0.71, 0.74, 0.75, 0.78, 0.72, 0.79, 0.75, 0.75, 0.75, 0.77, 0.79, 0.76, 0.75, 0.76, 0.79 and 0.76 for samples A, B, C, D, E, F, G, H, I, J, K, L, M, N, O, P, Q, R and S, respectively (fig. 3). The sample from locality N (Bangladesh: Singra) had the highest value of coefficient of variability (CV = 7.92) (table 3).

Acknowledgements This study was carried out in the Department of Zoology, University of Punjab, Lahore, Pakistan.

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Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 29.2 (2006)

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A preliminary examination of genetic diversity in the Indian false vampire bat Megaderma lyra K. Emmanuvel Rajan & G. Marimuthu

Emmanuvel Rajan, K. & Marimuthu, G., 2006. A Preliminary examination of genetic diversity in the Indian false vampire bat Megaderma lyra. Animal Biodiversity and Conservation, 29.2: 109–115.

Abstract A preliminary examination of genetic diversity in the Indian false vampire bat Megaderma lyra.— Habitat loss and fragmentation have serious consequences for species extinction as well as genetic diversity within a species. Random Amplified Polymorphic DNA (RAPD) analysis was employed to assess the genetic diversity within and between four natural populations of M. lyra. Our results suggest that the genetic diversity varied from 0.21 to 0.26 with a mean of 0.11 to 0.13 (± SD). The mean Gst value of 0.15 was obtained from all four populations and estimated average Nm (1.41) showing gene flow between the populations. AMOVA analysis showed 88.96% within and 11.04% among the studied populations. Cluster analyses of RAPD phenotypes showed that specimens were not grouped by geographical origin. The genetic diversity found in the M. lyra population may be explained by its breeding behaviors. Though preliminary, the results indicate that all four populations should be considered to maintain the genetic diversity.

Key words: Genetic diversity, Genetic structure, Megaderma lyra, Microchiroptera, PCR–RAPD. Resumen Examen preliminar de la diversidad genética del falso vampiro mayor Megaderma lyra.— La fragmentación y la pérdida del hábitat tienen graves consecuencias para la extinción de las especies y su diversidad genética. Se empleó el análisis del DNA polimórfico amplificado aleatorio (RADP) para evaluar la diversidad genética dentro de cada población y entre poblaciones naturales de M. lyra. Nuestros resultados sugieren que la diversidad genética varía de 0,21 a 0,26, con una media de 0,11 a 0,13 (± DE).

El valor Gst medio de 0,15 se obtuvo de las cuatro poblaciones y el promedio estimado Nm (1,41) indicador del flujo genético entre las poblaciones. El análisis AMOVA dio como resultados un 88,96% dentro de las poblaciones, y un 11,04% entre las poblaciones estudiadas. Los análisis de grupos de los fenotipos RAPD pusieron de manifiesto que los especímenes no estaban agrupados según su origen geográfico. La diversidad genética hallada en la población de M. lyra puede explicarse por sus conductas reproductoras. Aunque preliminares, los resultados indican que debería considerarse que las cuatro poblaciones mantienen su diversidad genética.

Palabras clave: Diversidad genética, Estructura genética, Megaderma lyra, Microchiroptera, RAPD–PCR. (Received: 29 XI 05; Conditional acceptance: 2 II 06; Final acceptance: 1 VI 06) K. Emmanuvel Rajan & G. Marimuthu, Dept. of Animal Behaviour and Physiology, School of Biological Sciences, Madurai Kamaraj Univ., Madurai–625 021, India.

Corresponding author: K. Emmanuvel Rajan, Dept. of Animal Science, School of Life Sciences, Bharathidasan Univ., Tiruchirappalli–620 024, India. E–mail: emmanuvel1972@yahoo.com

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Emmanuvel Rajan & Marimuthu

Introduction

Material and methods

Molecular genetic techniques nowadays are valuable tools in the studies on fields of population, behavioural and evolutionary biology where the use of traditional methods such as direct observation of individuals or a population is greatly restricted (Burland & Wilmer, 2001). Most of the temperate bats move between roosts over the course of a year and the sexes often use different roosts. In many species, females raise their offspring in maternal colonies and occasionally share their roost with males (Burland et al., 2001). In this context, the application of molecular genetic techniques extracts valuable biological and behavioural information to document population dynamics of the species.

Studies on different bat species using the molecular genetic approach have shown genetic diversity among distant populations (Mahardtunkamsi et al., 2000; Rossiter et al., 2000; Emmanuvel Rajan & Marimuthu, 2000), paternity (Petri et al., 1997), extra harem paternity (Heckel & Helversen, 2003), sex–biased dispersal (Dallimer et al., 2002) and suckling behaviour (Watt & Fenton, 1995).

The Indian false vampire bat Megaderma lyra lives in small colonies (30–50 bats) comprising both males and females. It roosts in temples, old buildings, caves and artificial underground tunnels (Brosset, 1962). It belongs to a heterogeneous group of echolocating bats called gleaners. Gleaning bats prefer to capture prey from ground and water surfaces. They consume large arthropods and small vertebrates such as frogs, geckoes, lizards, fish, mice, birds and even smaller bat species (Advani, 1981). The roosting ecology of M. lyra provides a unique opportunity to analyse the genetic structure of the natural population.

Like many tropical bats, individuals of M. lyra use their roost constantly for several years and exhibit no seasonal migration or hibernation. A recent study on M. lyra suggests that its reproductive success as well as the population size gradually decreased from 1995 to 2003 (Sripathi et al., 2004).

It is important to understand the genetic structure of declining population of M. lyra to identify priorities for its conservation. We chose Randomly Amplified Polymorphic DNA (RAPD) markers to estimate the genetic diversity, because (a) it reveals even minimal genetic differences by means of assessing polymorphism from large part of nuclear genome (Borowsky, 2000) and (b) RAPD–PCR is effectively employed to detect genetic variation in species listed as endangered, with scarce genetic variability or population sizes as a limiting factor (Haig et al., 1996; Kimberling et al., 1996; Kim et al., 1998; Vandwoestijne & Baguette, 2004). So far, very little is known about the mating behaviour and population dynamics and this is the first report of the genetic diversity in the Indian false vampire bat M. lyra.

Bats were captured by mist net from four different populations (I to IV) of M. lyra at four different locations, Population I (n = 9) from Pannian cave 15 km away from Madurai Kamaraj University campus, Madurai (9º 58' N, 78º 10' E); Population II (n = 11), 180 km away from population I towards the south, near Tirunelveli (8º 44' N, 77º 42' E); Population III (n = 15) 20 km away from population II towards the southeast; Population IV (n = 15) 60 km away from population II towards the southwest (fig. 1). We collected 0.25 ml of blood samples from each individual. Samples were stored (Emmanuvel Rajan & Marimuthu, 2000) until the genomic DNA was isolated. Along with blood sampling, the sex, reproductive status and body mass of each individual were recorded.

Total genomic DNA was extracted from the blood by Sambrook et al’s method (1989). The concentration of DNA samples was quantified spectrophotometrically and diluted to 10 ng/µl for further experimental use. The PCR reaction was carried out using a modified protocol of Williams et al. (1990). Each RAPD reaction (20 ml) contained 10 x buffer; 2.5 mM each of dNTP; 5 pM primers, 10 ng of template DNA and 0.5 unit of Taq DNA polymerase (Pharmacia, Uppsala, Sweden). Amplification was done using a Perkin Elmer Gene Amp PCR system 2400. The samples were subjected to the following PCR profiles: 5 minutes denaturation at 94°C followed by 40 cycles of 90 sec denaturation at 94°C, 90 sec annealing at 32°C, 2 min extension at 72°C and an additional one cycle for 7 min at 72°C as the final extension.

Negative reactions with no DNA template were used to check for contamination.

The following primers were chosen based on their reproducibility, banding pattern and polymorphism OPA3–5’AGTCGCCACT3’,OPA4– 5’AATCGGGCTG3’, OPA10–5’GTGATCGCAG3’, OPB1–5’GTTTCGCTG3’, OPB3–5’CATCCCCCTG 3’and OPB5–5’TGCGCCCTTC3’ (Bangalore Genei Pvt. Ltd., India). The consistency of the RAPD reaction was examined through a series of repeatability test for each individual from all four populations tested within and between PCR runs.

Finally, successfully repeatable samples only were included for subsequent genetic analysis and considered as a sample size for each population.

For analysis, the amplified products were electrophoresed in 6.0% polyacrylamide gel, at 100 V for 12 h in 1 x TAE buffer. Gels were silverstained (Sanguinetti et al., 1994) and photographed for subsequent analysis. Based on the known marker size (mixture of 1018 bp fragment and its multimer with pBR322 fragment), different polymorphic band sizes were calculated using Kodak Digital Science (ver 2.01, Kodak Scientific Imaging System, Eastman Kodak Company). Amplified polymorphic bands were scoredas dicerte, binary data was created for each individual’s presence (1) / absence (0) and analyzed as allelic variants hav-

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Animal Biodiversity and Conservation 29.2 (2006)

ing a dominant inheritance. One individual variable was chosen as the minimum criterion for band polymorphism (Haig et al., 1994).

A data matrix of the individual X marker containing the band scoring information was transformed to allele frequencies under the assumption that each amplified band corresponds to a different RAPD locus. This data set was used to calculate Nei’s genetic diversity (h) (Nei, 1973) and Shannon’s Index (S) (Allnutt et al., 1999). The gene flow between the populations was estimated from the Gst for each locus:

N

India Chennai

Nm = 0.25 (1 – Gst) / Gst (Slatkin & Barton, 1989). In addition, gene frequencies across the population were tested by the homogeneity test (G–square statistics) using Popgene version 1.31. AMOVA–PREP version 1.01 (Miller, 1998) was used to construct a data matrix for AMOVA version 1.55 (Excoffier et al., 1992), which is used to examine genetic difference among populations. An analysis of molecular variation (AMOVA) was performed on total molecular variation divided into two separate components (i) inter– individual difference within each population and (ii) inter–population difference by means of the Best Cut Test on 1000 permutation. An Unweighted Pair Group Method with Arithmetic Average (UPGMA) dendrogram was constructed using genetic distance based on Sneath & Sokal (1973).

Results A total of 14 markers generated from the primer were used in this study. RAPD band frequencies varied within and among all estimated populations, and the PCR fragment sizes ranged from 154 bp to 1636 bp (fig. 2). In no case did any two individuals share all the scored bands, and therefore no individuals of 100% similarity were found. The lowest genetic diversity estimated by Nei’s genetic diversity index and Shannon’s index was observed in population IV (h = 0.21 ± 0.11; S = 0.22 ± 0.14), while the highest value was observed in population I (h = 0.26 ± 0.13; S = 0.28 ± 0.16). Pairwise Gst value was calculated against each of them, and showed that population IV contributed less than other populations (excluding population IV the Gst value 0.11) and population I contributed more than other populations (excluding population I the Gst value 0.27). The mean Gst value of 0.15 was obtained. This resulted in an average estimate Nm of 1.41 indicating a large amount of gene flow between populations. Gene frequencies among different populations from different geographical regions were compared using the G2 test. All population pairs were significantly heterogeneous (G2 = 10.85, df = 3, P < 0.001). The pair wise value derived from AMOVA indicated a large number of significant differences between populations (P < 0.05) when population IV was excluded from the analysis. The result showed a

I Madurai

Bay of Bengal

II III

100 km

Indian Ocean

IV

Fig. 1. Locations of four populations (I to IV) of M. lyra in and around Madurai in Southern India.

Fig. 1. Localización de las cuatro poblaciones (I a IV) de M. lyra en y alrededor de Madurai, en el sur de la India.

genetic variation at 0.05% significant level of 88.96 % within populations and 11.04 % between populations (table 1).

When genetic distances between the populations were used to construct a cluster diagram in order to examine the relationship between the populations, no consistent geographical structure of the RAPD variation in M. lyra was compatible with restricted gene flow and long–term isolation (fig. 3).

Discussion A recent study on population I of M. lyra at Madurai (South India) indicates that the size of the population is dwindling (Sripathi et al., 2004). A decrease in population size is usually due to (a) habitat destruction (b) human poaching or (c) loss of genetic variation (i.e. only a small number of individuals that actually contribute to a gene pool; this may increase the probability of population extinction through a decline in fecundity and viability) (Pusey & Wolf, 1996). The development of RAPD (Welsh & McClelland, 1990) has been useful to demonstrate the genetic status of endangered species and the technique is also useful in

Emmanuvel Rajan & Marimuthu

112

D

1 2

3

4

5 6 7

8

9 10 11 12 13 14 M 12216 10636 1018

517/506 396 344 298

220

134

Fig. 2. Examples of RAPD amplifications with primer OPB 5. Lane 2–3, 4–5, 6–7, 8–9, 10–11 are mother–young pairs of M. lyra and lane 1, 12, 13, 14 are male samples: D. Negative control without template DNA; M. Indicated marker.

Fig. 2. Ejemplos de amplificaciones RAPD con el cebador genético OPB 5. Las pistas 2–3, 4–5, 6–7, 8–9, 10–11 son parejas madre–hijo de M. lyra, y las pistas 1, 12, 13, 14 proceden de muestras de machos: D. Control negativo sin plantilla de DNA; M. Marcador indicado.

conservation efforts in desert fishes (Vrijenhoek, 1995), sea turtles (Bowen & Avise, 1995) and Blanding’s turtle (Rubin et al., 2001).

In the present study, we used three different approaches for data analysis, genetic diversity, het-

erozygosity and genetic differentiation. The analysis of genetic diversity in M. lyra shows that no population has a higher degree of diversity. The genetic diversity found in this study is related to other bat species such as Tadarida brasiliensis

Table 1. Analysis of Molecular Variation (AMOVA) for 35 individuals of M. lyra. The total data set contains individuals from three populations. Statistics include the sum of squared deviations (SSD), mean squared deviations (MSD), variance component estimates (VCE), the percentages of total variance contributed by each component (%TV) and the probability (P) of obtaining a more extreme component estimated by chance alone: *** After 1,000 permutation.

Tabla 1. Análisis de variación molecular (AMOVA) para 35 individuos de M. lyra. La serie completa de datos contiene individuos procedentes de tres poblaciones. Las estadísticas incluyen la suma de las desviaciones elevadas al cuadrado (SSD), las desviaciones medias elevadas al cuadrado (MSD), las estimaciones de los componentes de varianza, los porcentajes de la varianza total aportada por cada componente, y la probabilidad (P) de obtener un componente más extremo estimado únicamente al azar.

Source of variation

df

SSD

MSD

VCE

% TV

P ***

Between populations

2

170.40

21.3

0.81

11.04

< 0.001

Individuals within population

34

1017.84

6.5

6.56

88.96

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Animal Biodiversity and Conservation 29.2 (2006)

Populations I

III

II

IV

0.00

0.05

0.10

0.15 0.20 0.25 Linkage distance

0.30

0.35

Fig. 3. Dendrogram showing the genetic relationship of the four populations of M. lyra based on the inter–population distance and cluster analysis by UPGMA Fig. 3. Dendrograma que muestra las relaciones genéticas de cuatro poblaciones de M. lyra, basándose en la distancia entre poblaciones y el análisis de grupos mediante UPGMA.

(McCracken et al., 1994), the Australian flying–fox Pteropus spp (Webb & Tideman, 1996) —using conventional protein (allozymes) markers—, Myotis myotis (Petri et al., 1997) —using DNA markers, mtDNA and Simple Sequence Repeats—, and a gleaning bat Plecotus auritus (Burland et al., 1999).

The high values of Nm (1.41) and low values of Gst (0.15) indicate a large amount of gene flow between populations. Slatkin (1985) suggested that significant differentiation between populations would be expected only if the Nm value was < 1.0. It is worth mentioning that despite the relatively high level of gene flow in these four populations, there were significant genetic differences among M. lyra in different regions. Similarly, there are a few other studies on genetic variation in megachiropterans in the Philippine islands (Peterson & Heaney, 1993) in which allozymes were used to estimate the level of gene flow for small fruit bats. Allele estimation of Nm was low at 0.05 for Haplonycteris fischeri, a species known to have low vagility compared with an Nm of 7.5 for Cynopterus brachyotis, which is an effective seed disperser and long distance forager (Peterson & Heaney, 1993). The level of genetic differentiation that we observed within and between populations of M. lyra compares favorably with other bat species such as the little red flying–fox Pteropus scapulatus (Sinclair et al., 1996) and the Indian leaf–nosed bat Hipposideros speoris (Emmanuvel Rajan & Marimuthu, 2000).

Gene flow between the colonies probably occurs mainly via extra–colony copulations without

permanent dispersal from the natal colony, but it may be limited by distance as well as availability of suitable mating sites or recently fragmented populations. Extra–colony copulation has been detected in most animal species, where interestingly no natal dispersal occurred in either sex (Amos et al., 1993). The recent mark–and–recapture studies at the roosting place show the fluctuation in population size of M. lyra during the breeding season (Sripathi et al., 2004). These observations support the extra–colony copulation and inbreeding avoidance behaviour, factors that may drive the maternity roost and determine the immigration/emigration dynamics of a particular colony.

However, population 1 and 3 are genetically more related than the other populations estimated in the present study. Future studies using advanced molecular markers in a greater number of samples (especially samples from populations 1 and 3) and distant populations will add additional insights to our understanding of the genetic diversity and contribute to conservation assessment of M. lyra in the Indian subcontinent.

Acknowledgements We thank Prof. G. Shanmugam for providing laboratory facilities and Dr. K. Kannan for helping in the experiments. Thanks also go to Francis C. Yeh and Rong–Cai Yang for providing the Popgene Genetic Analysis software program and to the Bioinformatics Centre, MKU for providing facilities to analyse the data.

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"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

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El género Antoinella Jeannel, 1937 (Coleoptera, Carabidae, Trechinae) tres especies nuevas de Marruecos: A. espanyoli sp. n., A. iblanensis sp. n. y A. fadriquei sp. n.

J. Mateu & O. Escolà

Mateu, J. & Escolà, O., 2006. El género Antoinella Jeannel, 1937 (Coleoptera, Carabidae, Trechinae) tres especies nuevas de Marruecos: A. espanyoli sp. n., A. iblanensis sp. n. y A. fadriquei sp. n. Animal Biodiversity and Conservation, 29.2: 117–121.

Abstract Genera Antoinella Jeannel, 1937 (Coleoptera, Carabidae, Trechinae) three new species from Morocco: A. espanyoli n. sp., A. iblanensis n. sp. y A. fadriquei n. sp.— Three new species of the genus Antoinella Jeannel (Carabidae, Trechinae) are described from the region of Taza in Morocco: A. espanyoli n. sp. (the smallest of all Antoinella), A. iblanensis n. sp. (with the end of aedeagus truncate) and A. fadriquei n. sp. (with the aedeagus rather similar to that of A. iblanensis n. sp. but end not truncate). A brief summary on the geographical dispersion of the genus is given. The most distinctive taxonomic characteristics concern the male genitalia; the accompanying drawings contribute further to the identification of the new taxa.

Key words: Antoinella, Coleoptera, Carabidae, Trechinae, Morocco, Description.

Resumen El género Antoinella Jeannel, 1937 (Coleoptera, Carabidae, Trechinae) tres especies nuevas de Marruecos: A. espanyoli sp. n., A. iblanensis sp. n. and A. fadriquei sp. n.— Se describen tres especies nuevas del género Antoinella Jeannel: A. espanyoli sp. n. (más pequeña que todas las demás Antoinella), A. iblanensis sp. n. (con la extremidad apical del edeago truncada por delante) y A. fadriquei sp. n. (edeago con un cierto parecido a A. iblanensis sp. n. pero con la extremidad apical no truncada por delante), recolectadas en cavidades del macizo del Atlas marroquí. Se presenta la dispersión geográfica del género. La característica taxonómica más importante concierne a la genitalia masculina; las figuras contribuyen además a la identificación de los nuevos taxones.

Palabras clave: Antoinella, Coleoptera, Carabidae, Trechinae, Marruecos, Descripción.

(Received: 29 XI 05; Conditional acceptance: 2 II 05; Final acceptance: 6 VI 06) J. Mateu & O. Escolà, Museu de Ciències Naturals de la Ciutadella (Edifici de Zoologia), Passeig Picasso s/n., 08003 Barcelona, España (Spain).

Corresponding autor: O. Escolà. E–mail: oescola@bcn.cat

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introducción Anteriormente, el género Antoinella estaba compuesto por la especie tipo groubei, descrita por Antoine (1935), como especie del género Duvalius, por la subespecie groubei salibai Antoine (1953), y por la especie gigoni Casale (1982). Un análisis más detallado de la especie tipo dio lugar a que, en el año 1937, el Prof. R. Jeannel estableciera para ella un género independiente (Antoinella), basándose principalmente en la posición de la pieza copulatriz del saco interno del edeago, siendo plana y simétrica en Duvalius, e inclinada y asimétrica (de champ, en francés), en Antoinella. Éste y el carácter de las protibias pubescentes en su porción apical en la cara interna, definen el género Duvalius, el cual se diferencia con cierta dificultad de Antoinella. A la espera de la futura y deseada monografía de los Duvalius y géneros afines, respetamos los caracteres un tanto cambiantes invocados por Jeannel (1937) y aceptados por Casale & Laneyrie (1982) para este género.

Material y métodos El material objeto de este estudio se ha recolectado integramente en cavidades situadas en el Atlas Medio Occidental, en una zona comprendida, aproximadamente entre los mil y tres mil metros de altitud. La citada recolección se ha efectuado en la zona isotérmica de las cavidades, siempre con un elevado grado de humedad próximo a la saturación y una relativa baja temperatura. Algunos ejemplares, como Antoinella fadriquei se han capturado en zonas muy profundas a más de 200 m de profundidad en el "Gouffre du Friouato" (al que mejor le correspondería el nombre de Ifri ou Addo según nuestros colegas de Agadir). Otros, como Antoinella iblanensis, se capturaron en cavidades de tan solo veinte o treinta metros de profundidad, pero con las condiciones climaticas citadas.

El material estudiado se encuentra montado en seco sobre cartulina, con las preparaciones de sus edeagos en láminas de celuloide, utilizando como fijador bálsamo de Canadá. Los ejemplares están depositados en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoologia– col. MZB) y han sido estudiados con un microscopio Olimpus BX40 y dibujados con un microscopio Nikon a 100 x y 200 x, fijando los detalles a 400 x.

Resultados y discusión Antoinella groubei (Antoine, 1935) Se trata de la especie descrita en 1935 por Antoine como perteneciente al género Duvalius Delarouzeé, 1859, para la cual, dos años más tarde, el Prof.

Jeannel, promovió como especie tipo del nuevo género Antoinella, próximo, eso sí, a Duvalius.

Desde entonces se ha añadido a groubei una nueva subespecie, la s. sp. salibai, también de Antoine (1953).

En 2001 fueron descubiertos tres ejemplares de una nueva especie de Antoinella que se separaba de las dos conocidas por el tamaño mucho más pequeño. En 2002 se hallaron otras dos especies nuevas pertenecientes al género Antoinella tal como está definido hasta hoy.

El género se compone de la especie tipo A. groubei descrita por Antoine en 1935 (como Duvalius). La misma especie dio lugar a que Jeannel en 1937 la separara de Duvalius (Jeannel, 1937) y estableciera el género independiente Antoinella basándose especialmente en la posición de la pieza copulatriz en el interior del saco interno: plana y simétrica para Duvalius y inclinada y asimétrica (de champ en francés) en Antoinella. Éste y el carácter de las protibias pubescentes en su porción apical por la cara interna definen el género Duvalius que se diferencia con dificultades de Antoinella. La duda desaparecerá el día en que el género Duvalius sea estudiado en profundidad y en su totalidad; en lo que se refiere a la genitalia del macho en las Antoinella los edeagos de las especies difieren notablemente entre si. En la espera de la futura monografía de los Duvalius y géneros afines respetamos los caracteres un tanto cambiantes invocados por Jeannel en 1937 (Jeannel, 1937) y aceptados por (Casale & Laneyrie, 1982) y (Casale, 1982) para el género.

Antoinella espanyoli sp. n.

Material estudiado Holotipo: 1 {, Marruecos occidental, Ifri Mkhrouga, Ain Leúh, Azrou, 24 V 01, M. Messouli, F. Fadrique & O. Escolà leg. (col. MZB, nº reg. 2001–0366).

Situación: coordenadas Lambert: X = 513,9 Y = 288,1 Z = 1.960 m.

Paratipos: 1 }, Ifri Nakhraman, Ain Leúh, Azrou, cavidad muy cercana a Ifri Mkrouga, 23 V 01 M. Messouli, F. Fadrique & O. Escolà leg. (col. MZB, nº reg. 2001–1046); 1 {, Ifri Mkhrouga, Ain Leúh, Azrou, 24 V 01, M. Messouli, F. Fadrique & O. Escolà leg. (col. MZB, nº reg. 2001–1047) (a esta cavidad de Mkrouga también se le da el nombre de "grotte de l’Aztèque Tartare" en el catálogo de cavidades de Marruecos "Inventaire Spéléologique du Maroc" de 1981).

Descripción Longitud 4,5 mm desde el ápice de las mandíbulas hasta el ápice elitral. Cabeza obtusa con las sienes poco convexas algo abultadas por detrás, los ojos completamente blancos, planos sin sobresalir del perfil, con los omatidios apenas visibles. Surcos interoculares borrosos y relativamente poco profundos por detrás. Pronoto transverso 1,34 veces más ancho que largo, de lados moderadamente redondeados, su máxima anchura a la

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altura de la primera seda lateral, brevemente sinuados por delante de los ángulos posteriores, éstos ligeramente agudos. Base pronotal casi rectilínea, surco mediano bien inciso; superficie ligeramente convexa. Élitros alargados casi subparalelos, apenas arqueados sobre los laterales, estrías incisas ligeramente punteadas, los intervalos ligeramente planos. Ángulos lateroposteriores internos ligeramente redondeados y algo separados, los exteriores totalmente redondeados, estría escutelar bien visible.

Derivatio nominis Dedicamos esta nueva especie al Dr. Francesc Español Coll, maestro común de los dos autores que publicó el primer trabajo con el Dr. Mateu en 1942 (Español & Mateu, 1942) y el primer trabajo con el segundo autor en 1969 (Español & Escolà, 1969). Español tuvo una presencia activa en cuanto a los coleópteros en Marruecos durante su servicio militar (1926–1929) pero a partir de 1966 representó un catalizador importante de las expediciones espeleológicas en Marruecos, iniciando sus trabajos con la descripción de uno de sus dos cavernícolas preferidos: Subilsia senenti gen. nov y sp. n. de la zona de Ait M’Hamed (Español, 1967).

Observaciones Esta nueva especie difiere de las ya descritas y las que se describen en el presente artículo por un carácter bien manifiesto: su tamaño notablemente menor del de los otros cuatro taxones: 4,5 mm.

Sobre los otros caracteres no hay ninguno que caracterice la especie de manera notable, todos son caracteres morfológicos cuantitativos. Otra diferencia evidente se encuentra en el edeago, como puede verse en las figuras 2–4.

1.0 mm

Fig. 1. Antoinella espanyoli sp. n., habitus del holotipo.

Fig. 1. Antoinella espanyoli n. sp., habitus of holotype.

Antoinella groubei (Antoine, 1935) Se trata de la especie descrita por Antoine en 1935 como perteneciente al género Duvalius Delarouzée, 1859. Dos años más tarde, en 1937, el Dr. Jeannel promovió la especie de Antoine a género independiente, próximo, eso sí, a Duvalius.

Desde entonces se añadió a groubei una subespecie, la s. sp. salibai también de Antoine (Antoine, 1953) que tiene una longitud de 5,8 mm según Antoine. Luego tenemos que llegar al año 1982 para que A. Casale enriqueciera el género que nos ocupa con un nuevo taxon: A. gigoni, de la cueva de Châra en el Atlas medio.

Antoinella gigoni Casale, 1982 Como señala el autor en su descripción la especie parece bastante distinta de groubei por su pronoto más transverso y sobre todo por la conformación de los ángulos posteriores más desarrollados y salientes.

El principal carácter distintivo de gigoni es asimismo la conformación del edeago, robusto caracterizado por su ápice levantado en lugar del gancho encorvado de A. groubei (Casale, 1982, p. 232) (Jeannel, 1937, p. 83). Longitud del holotipo 7,4 mm según Casale (Mathieu & Châtelain, 1966).

Antoinella iblanensis sp. n.

Material estudiado Holotipo: 1 {, de Tlat Izra, en Bou Iblane, Atlas medio, Marruecos 20 V 2002 (Fadrique y Escolà leg.). Tipo depositado en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoología, col.

MZB, nº reg. 2002–0569).

Situación: al pié de la vertiente septentrional de la cadena de Bou Iblane a un centenar de metros de altura respecto al fondo del valle por el que corre la carretera. No se halla situado en el "Inventaire spéléologique du Maroc" de 1981 y en la única visita de 2001 no se pudieron obtener las

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2

3

0.2 mm 1.0 mm

4

1.0 mm

Figs. 2–4. Edeagos de los holotipos en visión lateral: 2. Antoinella espanyoli sp. n..; 3. Antoinella iblanensis sp. n.; 4. Antoinella fadriquei sp. n.

Figs. 2–4. Aedeagus of the holotypes in lateral view: 2. Antoinella espanyoli n. sp.; 3. Antoinella iblanensis n. sp.; 4. Antoinella fadriquei n. sp.

coordenadas con G. P. S. Éstas se obtuvieron en la campaña de Marruecos de julio de 2006: 33º 42' 30,22'' N 04º 06' 27,1'' W; 2.136 m s.n.m.

Descripción Longitud 5,8 mm. Difiere de groubei por su talla menor, por sus élitros con todos los intervalos punteado–pubescentes, la pubescencia densa y bastante corta algo reclinada y la serie dorsal compuesta de tres poros setiformes casi equidistantes, la tercera seda más alejada hacia el ápice. Estrías finas y los intervalos planos.

Edeago (fig. 3) con el borde superior convexo y ventralmente casi subrectilíneo: el bulbo provisto de un fuerte y largo alerón sagital. Ápice largo, estrecho y sinuoso, levantado en su extremidad truncada por delante, convexa dorsalmente y ventralmente dentiforme formando un diente ventral agudo.

El saco interno conlleva dos piezas lameliformes dispares parcialmente recubiertas por un haz de escamas más o menos quitinizadas.

Parámeros robustos moderadamente alargados y con cuatro o cinco largas sedas terminales.

Derivatio nominis Especie dedicada a la zona orográfica donde se

ha hallado el primer ejemplar conocido: Jbel Bou Iblane, larga crestería de una sierra con nieve durante seis meses al año, que alcanza una cota máxima de 3.190 m, a unos 50 km al S de Taza.

Antoinella fadriquei sp. n.

Material estudiado Holotipo: 1 { de Ifri Ou Ado, Atlas medio, Taza, Marruecos 11 V 2002 (Fadrique y Escolà leg.); tipo depositado en el Museu de Ciències Naturals de la Ciutadella (edificio de Zoología, col. MZB, nº reg. 2004–0881).

Longitud 5,9 mm. Coordenadas Lambert: X = 622,35 Y = 390,25 Z = 1.450 m Descripción Por su longitud esta nueva especie es parecida a groubei. Se diferencia de A. iblanensis por su talla menor y especialmente por sus élitros completamente glabros, a parte de las sedas dorsales, tegumento liso, brillante y desprovisto de microescultura, estrías fuertes con los intervalos algo convexos, provistos de 4 sedas dorsales sobre la cuarta estría, la delantera más alejada de las

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tres siguientes equidistantes y un poro apical sobre el tercer intervalo.

El edeago del único ejemplar recolectado es bien distinto de las otras cuatro especies del género, como acabamos de constatar (fig. 4). En A. fadriquei el lóbulo mediano se presenta más sinuoso, grueso en el centro y estrangulado posteriormente por delante del lóbulo basal. Este último es robusto, sinuoso, con el alerón sagital largo, subparalelo y encorvado hacia adentro. El ápice guarda un cierto parecido con el de A. iblanensis en cuanto a su conformación general, con su extremidad alargada, sinuosa, paralela y levantada pero no truncada por delante, sino escotada y con sus puntas dorsal y ventralmente aguzadas.

Parámeros con cuatro sedas terminales.

Derivatio nominis Dedicada a nuestro amigo y colega D. Florentino Fadrique, por ser el "alma mater" de las últimas expediciones a Marruecos y por su gran actividad en la Bioespeleología, como ya es sabido.

Observaciones y conclusiones Las nuevas capturas de Antoinella vienen a suscitar ciertas reflexiones.

Primero la distribución del género que cubre un área bastante importante en el Atlas medio con una longitud en línea de aire de unos 120 x 60 km. La especie de mayor distribución es A. groubei que se encuentra en los alrededores de Taza y por el Sur hasta Bou Iblane. Ahora bien, si pensamos en A. espanyoli sp. n. se trata del taxón más excéntrico y especie única en las cavidades donde fue recolectada: Ifri Mkrouga y Kef Nkraman. En revancha A. groubei es la especie más extendida y que al mismo tiempo convive con otras dos especies: A. iblanensis sp. n. en el Djebel Bou Iblane, y A. fadriquei sp. n. en el Ifri ou Ado. Las dos nuevas especies A. iblanensis y A. fadriquei han sido descubiertas ahora, mientras que A. groubei se conoce desde 1935, sin que nunca se hubieran recolectado hasta el año 2002 conviviendo en una misma cavidad común.

Por lo que respecta a A. gigoni Casale, de la cueva de Chara sería muy parecida a A. groubei según el autor, separadas una de otra por su

conformación pronotal y especialmente por su edeago. Al parecer no convive con groubei en la cueva de Chara que se encuentra a unos 37 km al SW de Taza.

Agradecimientos Agradecemos sinceramente la realización de la parte iconográfica de esta nota, efectuada con un interés y tesón dignos de loar del Sr. Miguel Prieto Manzanares, doctor en ciencias químicas y excelente colaborador del Museo de Ciencias Naturales de la Ciutadella de Barcelona.

Referencias Antoine, M., 1935. Notes d’Entomologie Marocaine. XXI. Description d’ un Duvalius cavernicole microphthalme de la grotte de la daya Chiker (Coléoptères Carabidae). Bull. Soc. Scienc. Nat. Phis. Maroc, 15: 234–237.

– 1953. Notes d’Entomologie Marocaine, LVI. Melanges coléoptérologiques. A–Caraboidea.

Rev. fr. Ent., 20: 202–223.

Casale, A., 1982. Nuovi Carabidi del Marocco, di Grecia e di Papua–Nuova Guinea (Coleoptera).

Rev. Suisse Zool., 89(1): 229–244.

Casale, A. & Laneyrie, R., 1982. Trechodinae et Trechinae du Monde. Tableau des sous– familles, Tribus, Séries phylétiques, genres et catalogue général des espèces. Mém. Biosp., 9: 1–226.

Español, F., 1967. Resultados de una campaña bioespeleológica en el Gran Atlas Central.

Coleópteros. Misc. Zool., 2(2): 47–52.

Español, F. & Escolà, O., 1969. La biospeleología en España.Resumen histórico. V Internationaler Kongress für Speläeologie, Stuttgart, 4: B–15, 1–4.

Español, F. & Mateu, J., 1942. Revisión de los Steropus ibéricos (Col. Carabidae). An. Fac. Cien.

Porto, 27(2): 1–15.

Jeannel, R., 1937. Nouveaux Trechinae paléartiques (Col. Carabidae). Bull. Soc. ent. Fr., 42: 82–88.

Mathieu, L. & Châtelain, R., 1966. La grotte de Châra (Maroc). Rass. Spel. ital., 18: 60–65.

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

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Aspectos taxonómicos de Cetopsorhamdia boquillae y C. nasus (Pisces, Heptapteridae), con anotaciones sobre su ecología en la cuenca alta de los ríos Magdalena y Cauca, Colombia R. I. Ruiz–C. & C. Román–Valencia

Ruiz–C., R. I. Román–Valencia, C., 2006. Aspectos taxonómicos de Cetopsorhamdia boquillae y C. nasus (Pisces, Heptapteridae), con anotaciones sobre su ecología en la cuenca alta de los ríos Magdalena y Cauca, Colombia. Animal Biodiversity and Conservation, 29.2: 123–131.

Abstract Taxonomic aspects of Cetopsorhamdia boquillae and C. nasus (Pisces, Heptapteridae), with annotations on their ecology from Magdalena and Cauca rivers upper basin, Colombia.— A taxonomic analysis of Cetopsorhamdia boquillae and Cetopsorhamdia nasus from the Magdalena and Cauca river basin in Colombia is reported here based on fresh topotypical materials. Cetopsorhamdia boquillae can be differentiated from its congener by the color pattern, mainly concerning three dark lines: one on the supraoccipital bone, another at the dorsal fin base and a third at the caudal fin base. The pterygiophore of the dorsal fin first ray is inserted anterior to the ninth vertebra. C. nasus is readily distinguished from its congener by its lack of supraneural spines, fewer than 60 premaxilla teeth, the posterior edge of mesethmoid, and orbitonasal lamina joined by a cartilage band, and the shape of the frontal canal. Cetopsorhamdia boquillae can be distinguished from C. nasus by the length of the adipose-dorsal fin base(statistically significant) (F = 21, P = 0.05), the number of principal unbranched anal rays (5–6 in C. boquillae, 4 in C. nasus), and fewer vertebrae (36 in C. boquillae, 39 in C. nasus). Chemical, physical and ecological data are included to characterize the species habitats.

Key words: Taxonomy, Cetopsorhamdia, Siluriformes, Tropical fish.

Resumen Aspectos taxonómicos de Cetopsorhamdia boquillae y C. nasus (Pisces, Heptapteridae), con anotaciones sobre su ecología en la cuenca alta de los ríos Magdalena y Cauca, Colombia.— Se efectuó un análisis taxonómico de Cetopsorhamdia boquillae y Cetopsorhamdia nasus de la cuenca alta de los ríos Magdalena y Cauca, basado en material fresco y topotípico. Cetopsorhamdia boquillae se distingue de las demás especies conocidas por la coloración (principalmente en presentar una banda vertical oscura a nivel de la base de la aleta caudal, otra banda oscura a nivel del supraoccipital que cubre todo el dorso, otra a nivel del origen de la aleta dorsal). El pterigióforo del primer radio de la aleta dorsal insertado anterior a la novena vértebra. C. nasus se distingue de sus congeneres por la ausencia de supraneurales, menos de 60 dientes en el premaxilar, por el borde posterior del mesetmóides, la lámina orbitonasal unidos al frontal por una banda de cartílago, y la forma de la fontanela craneal. Cetopsorhamdia boquillae se distingue de C. nasus por la distancia aleta adiposa–aleta dorsal y es estadísticamente significativa (F = 21, P = 0,05), por el número de radios simples principales de la aleta anal (5– 6 en C. boquillae, 4 en C. nasus), y por el número menor de vértebras (36 en C. boquillae, 39 en C. nasus). Se incluyen datos ecológicos, físicos y químicos sobre las características de hábitat de las dos especies válidas.

Palabras claves: Taxonomía, Cetopsorhamdia, Siluriformes, Pez tropical.

(Received: 26 I 06; Conditional acceptance: 15 V 06; Final acceptance: 30 VI 06) R. I. Ruiz–C. & C. Román–Valencia, Lab. de Ictiología, Univ. del Quindío, A.A. 460, Armenia, Quindío, Colombia.

Corresponding author: C. Román–Valencia. E–mail: ceroman@uniquindio.edu.co ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introducción El género Cetopsorhamdia (Eigenmann & Fisher, 1916) incluye a un pequeño grupo de bagres, conformado por 12 especies (Eigenmann, 1922; Schultz, 1944; Schubart & Gomes, 1959; Miles, 1971, 1973; Stewart, 1985; Eschmeyer, 2003) distribuidas en el norte de Suramérica. Su taxonomía no está completamente estudiada. Además, las relaciones de Cetopsorhamdia con varios grupos no están resueltas (Lundberg & Mcdade, 1986; Stewart, 1985, 1986; Ferraris, 1988; Lundberg et al., 1991; Silfvergrip, 1996; Bockmann & Ferraris, 2005). Tres especies de Cetopsorhamdia se citan para Colombia: C. boquillae y C. molinae del alto Cauca (Eigenmann, 1922; Schultz, 1944; Dahl, 1971; Miles, 1971, 1973; Román–Valencia, 1988, 1995; Eschmeyer, 2003; Maldonado–Ocampo et al., 2005) y C. nasus del Alto Magdalena (Eigenmann & Fisher, 1916; Dahl, 1971; Miles, 1971, 1973; Eschmeyer, 2003; Maldonado–Ocampo et al., 2005).

El propósito de este trabajo es redefinir las especies Cetopsorhamdia boquillae y C. nasus de Colombia basándose en material fresco y topotipico; además, se incluyen observaciones ecológicas.

Material y métodos Las medidas se tomaron con un calibrador digital hasta centésimas de mm y se expresaron como porcentajes de la longitud estándar. Medidas y conteos de los ejemplares se realizaron sobre el lado izquierdo, excepto cuando estaban deteriorados en este lado. Conteos, medidas y descripción de caracteres siguen las generalidades a Stewart (1985), Lundberg et al. (1991) y Román–Valencia et al. (1999). Se realizó un análisis de varianza para determinar diferencias significativas de los caracteres con los taxones. En este caso se utilizó el programa Statgraphics V. 2.6.

Las observaciones de estructuras óseas se hicieron sobre ejemplares transparentados y teñidos (T&C) de acuerdo a modificaciones al método descrito por Taylor & Van Dyke (1985), Song & Parenti (1995). La nomenclatura de huesos se basó en la utilizada por Fink & Fink (1981), Adriaens & Verraes (1997) y Diogo et al. (2001, 2004). Se examinó material depositado en el laboratorio de Ictiología, Departamento de Biología, Universidad del Quindío, Armenia, Colombia (IUQ) y ejemplares de C. iheringi de la Coleção de Peixes, Departamento de Zoologia e Botânica, Instituto de Biociencias, Letras e Ciências Exactas, Universidade Estadual Paulista– UNESP, Brasil (DZSJRP) con fines comparativos.

Se realizaron los siguientes registros diurnos de variables físicas y químicas hidrográficas en los sitios de muestreo: In situ se determinaron: oxígeno disuelto y temperatura obtenido con oxímetro.

El pH se determinó con pHmetro portátil. Ancho y profundidad del río medidos con un decámetro y una vareta graduada en cm. Tipo de sustrato y color del agua, por observación directa. Las demás

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variables se determinaron en el laboratorio de aguas de la Universidad del Quindío con espectrofotómetro Hach modelo DRL/5. Coordenadas geográficas y altura, con un sistema de posicionamiento global marca Magellan 4000 XL. Material examinado Cetopsorhamdia boquillae: IUQ 231, 16 ejemplares, Colombia, Departamento del Quindío, Municipio de Armenia, Vereda San Juan, Alto Cauca, afluente río Quindío, quebrada San Pedro. IUQ 474, 2 ejemplares (T&C), Colombia, Departamento del Quindío, Municipio de Armenia, Vereda San Juan, Alto Cauca, afluente río Quindío, quebrada San Pedro. IUQ 151, 1 ejemplar, Colombia, Departamento del Quindío, Municipio de Armenia, Vereda San Juan; Alto Cauca, afluente río Quindío, quebrada El Descanso. IUQ 464, 1 ejemplar, Colombia, Departamento del Quindío, corregimiento de Pueblo Tapao, Municipio de Montenegro, Alto Cauca, afluente río La Vieja, quebrada La Maria (4° 30' 38'' N y 75° 52' 52'' O) 1.030 m. IUQ 465, 6 ejemplares, Colombia, Departamento del Quindío, Municipio de Quimbaya, Alto Cauca, afluente río La Vieja, quebrada Villa Leonor (4° 36' 29'' N y 75° 48' 30'' O) 1.230 m. IUQ 466, 7 ejemplares, Colombia, Departamento del Quindío, Municipio de Quimbaya, Alto Cauca, afluente río La Vieja, quebrada Villa Leonor. IUQ 467, 3 ejemplares, Colombia, Departamento del Quindío, Municipio de Montenegro, Vereda La Española, Alto Cauca, afluente río Roble, quebrada La Española (4° 34' 39'' N y 75° 51' 01'' O) 1.009 m. IUQ 468, 11 ejemplares, Colombia, Departamento del Quindío, Municipio de Montenegro, Alto Cauca, afluente río La Vieja, Quebrada La Isla (4° 32' 49'' N y 75° 49' 31'' O) 995 m, 27 VI 2001. IUQ 472, 8 ejemplares, Colombia, Departamento del Quindío, Municipio de Quimbaya, Vereda Calle larga, Alto Cauca, afluente río La Vieja, quebrada Canceles (4° 32' 42'' N y 75° 49' 33'' O) 1.288 m.

IUQ 478, 4 ejemplares, Colombia, Departamento del Valle, Municipio de Sevilla, Vereda Purnio, Alto Cauca, sistema del río La Paila, quebrada Saldaña (4º 15’ 24'' N y 75º 57' 19'' O) 1.031 m. IUQ 479, 2 ejemplares, Colombia, Departamento del Valle, Municipio de Bugalagrande, Vereda el Raicero, Alto Cauca, sistema del río Bugalagrande, Zanjón Venecia (4º 09' 47'' N y 76º 05' 19'' O) 1.110 m. IUQ 480, 1 ejemplar, Colombia, Departamento del Valle, Municipio de Bugalagrande, Vereda el Raicero, Alto Cauca, sistema del río Bugalagrande, quebrada San Miguel (4º 10' 04'' N y 76º 06' 46'' O) 1.063 m.

Cetopsorhamdia iheringi: DZSJRP 1146, 2 ejemplares, Brasil, Córrego da Barra Funda, "desembocadura", afluente río Preto, río Grande.

DZSJRP 001147, 4 ejemplares de siete, Brasil, SP, Brotas, bacia do Rio Jacaré–Pepira, afluente do rio Tietê (22° 16' 45'' S y 48° 6' 59'' O).

Cetopsorhamdia nasus: IUQ 469, 1 ejemplar, Colombia, Departamento del Huila, Municipio de

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Pitalito, Alto Magdalena, Quebrada La Criolla (1° 51' 23'' N y 76° 08' 3'' O) 1.264 m. IUQ 482, 11 ejemplares, Colombia, Departamento del Huila, Municipio de Pitalito, Alto Magdalena, Quebrada La Criolla (1° 51' 23'' N y 76° 08' 23'' O) 1.264 m.

IUQ 470, 4 ejemplares, Colombia, Departamento del Huila, Municipio de Pitalito, Alto Magdalena, quebrada Cabuche (1° 53' 23'' N y 76° 00' 02'' O) 1.307 m. IUQ 475, 1 ejemplar (T&C), Colombia, Departamento del Huila, Municipio de Pitalito, Alto Magdalena, quebrada Cabuche (1° 53' 23'' N y 76° 00' 02'' O) 1.307 m.

Cetopsorhamdia sp.: IUQ 241, 1 ejemplar, Departamento del Valle, Municipio de Sevilla, Alto Cauca, río La Paila. IUQ 471, 1 ejemplar, Colombia, Departamento del Quindío, Alto Cauca, río La Vieja.

Resultados Cetopsorhamdia boquillae Eigenmann 1922 (tabla 1, figs. 1, 3A, 4A) Cetopsorhamdia boquillae Eigenmann, 1922 p. 37 (descripción, localidad típica: Boquilla); Schultz, 1944 p. 218 (registro en clave: para la cuenca del Magdalena cerca de Honda); Miles, 1947, 1971 p. 66; 1943, 1973 p. 25 (registro: quebrada Boquía); Román–Valencia, 1988 p. 111; 1995 p. 14 (registro: quebrada Boquía en el río Quindío, Alto Cauca); Bockmann & Ferraris, 2005 (registro); Maldonado–Ocampo et al., 2005 p. 160 (registro).

Diagnosis El diseño de coloración descrito posteriormente diferencia a esta especie de las demás conocidas, la ausencia de la barra epifiseal y la presencia de forámenes simétricos sobre la superficie de las ramificaciones en el aparato de weber.

Descripción Forma del cuerpo Los datos morfométricos y merísticos se registran en la tabla 1. Cuerpo alargado y comprimido progresivamente hacia la aleta caudal. Desde el hocico hasta el inicio de la aleta dorsal se observa un perfil del cuerpo ligeramente convexo. Hocico achatado tanto en vista dorsal como lateral. Boca inferior. Las barbillas maxilares sobrepasan el extremo de las aletas pectorales y alcanzan el inicio de la aleta dorsal. Las barbillas mentonianas externas llegan hasta la base de las aletas pectorales. La barbilla mentoniana interna apenas llega hasta las abertura branquial. Ojos pequeños, ubicados dorso–lateralmente. Origen de la aleta dorsal ubicado en posición anterior al origen de las aletas pélvicas.

Primer radio ramificado de la aleta dorsal más largo que los demás. No presenta espinas punzantes en la aleta dorsal y pectoral; el primer radio ramificado en éstas últimas es más largo que el resto, sin alcanzar el origen de las pélvicas, las cuales tampoco llegan hasta el origen de la anal.

Aleta anal con el borde posterior convexo. Aleta caudal con lóbulos cortos y redondeados.

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Osteología (figs. 3A, 4A) Más de 60 dientes en el premaxilar rectos y puntiagudos dispuestos en parches. Rastrillos branquiales en todos los arcos branquiales, filamentos no bífidos. Veinticuatro a veintiséis filamentos en dos series presentes en los cuatro arcos. La cápsula ótica está reducida.

Dientes vómero–palatinos ausentes y extremo anterior de los palatinos es óseo. La lámina orbitonasal se extiende de forma ondulada desde la parte posterior del proceso ventral del mesetmóides bordeado por cartílago, hasta el extremo anterolateral del frontal en ausencia de cartílago. Apófisis posteriores del mesetmóides alargadas y se prolongan sobre el frontal. La parte dorsal de la lámina orbitonasal presenta forámenes en el parte lateral y sobresale lateralmente en relación al frontal y al parietal. Fontanela craneal anterior y posterior alargada y estrecha. Ausencia de cartílago sobre el pterótico. Extremo posterior del proceso parieto–supraoccipital delgado y en forma de "v". Procesos laterales del complejo Weberiano de proyecciones ramificadas en sus extremos, se observan entre 5 y 7 ramificaciones.

La parte láminar posterior a estas ramificaciones es rectangular. La rama posterior del cuarto proceso transversal es corta y gruesa. Forámenes simétricos presentes sobre la superficie de las ramificaciones en el aparato de weber. Se observa un solo supraneural corto pequeño, anterior al primer pterigióforo de la aleta dorsal. Proceso cleitral posterior delgado y puntiagudo. Primer pterigióforo de la aleta dorsal insertado anterior de la novena vértebra. Número total de vértebras: 36.

Dimorfismo sexual Los machos se distinguen de las hembras por la papila urogenital prolongada en forma de gonopodio (1,5 mm ó más), mientras que en las hembras sólo se observa el poro urogenital.

Color en vida Área dorso lateral del cuerpo oscura, más pronunciado en la parte dorsal. Área ventral a nivel de la cabeza y cintura pectoral, rosado–oscuro. Aletas dorsal, pectorales y caudal, oscuras; las aletas pélvicas amarillo–claro. Una banda vertical oscura a nivel de la base de la aleta caudal. Otra banda oscura a nivel del supraoccipital que cubre todo el dorso, otra a nivel del origen de la aleta dorsal.

Ecología y distribución La especie es poco abundante y se distribuye entre los 1.000 y los 1.790 m s.n.m. se ubican en drenajes o quebradas de tipo primario y secundario. Agua típicamente cristalina, sustrato conformado por piedras y material de origen vegetal y animal en descomposición. Temperatura del agua oscila entre 15 y 21°C; el oxígeno, el sulfato y la humedad relativa son altos; mientras que la conductividad, los nitratos, los nitritos, el N amoniacal, los fosfatos, el hierro, la turbidez, la dureza, la alcalinidad, DQO y DBO son bajos. El pH casi neutro. En general,

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son valores propios de ambientes acuáticos de alta montaña neotropical.

En el único trabajo (Román–Valencia & Giraldo, 2006) se reporta que "el hábitat característico de la especie está conformado principalmente por pasto kikuyo (Poaceae), Guadua angustifolia y Hedychium coronarium". Drenajes característicos para la especie son de promedio: ancho de 2 m y profundidad de 0,5 m; C. boquillae ocupa las cuevas formadas por raíces de árboles y plantas de zona litoral. El pH registró valores alrededor de 7,0 (promedio 7,8), temperatura superficial 20,8ºC, temperatura ambiente 21,3ºC, oxigeno disuelto alto (6,4 ppm). La actividad agropecuaria y ganadera es común en todos los sitios de muestreo y amenaza la sobrevivencia de la especie. Convive sintópicamente con Astyanax aurocaudatus (vide Román–Valencia & Ruiz–C., 2005). Astroblepus cyclopus, Bryconamericus caucanus, Chaetostoma fischeri, Creagrutus brevipinnis, Hemibrycon boquiae, Trichomycterus caliense, T. retropine, Poecilia caucana, Rhamdia quelen. C. boquillae es una especie con actividad en el crepúsculo–noche, momento durante el cual obtiene el alimento. La dieta está conformada, en su mayoría, por insectos los cuales representan el 70,5%, seguido de Acari (3,6%) y Gastropoda (1,4%). Dos desoves fueron encontrados para la población (julio–agosto y noviembre–diciembre); durante los periodos de desove la especie consumió poco alimento. La fecundidad osciló entre 10 y 2.277 (media 653 ovocitos), el diámetro del ovocito es pequeño (0,57 mm promedio). El tamaño promedio de madurez fue de 40 mm de longitud estándar para hembras y machos. La proporción entre sexos fue de 1:1 (( 2 = 2.706, p = 0,9, gl = 1). Correlación positiva entre longitud estándar–longitud intestino (r = 0,6), longitud total–peso total (r = 0,9), peso total–peso estómago (r = 0,6).

Cetopsorhamdia nasus Eigenmann & Fisher 1916 (tabla 1, figs. 2, 3B, 4B) Cetopsorhamdia nasus, Eigenmann & Fisher, 1916 p. 83 (descripción, localidad típica: Honda); Schultz, 1944 p.

220 (diagnosis en clave); Miles, 1971 p. 58 (registro); Dahl, 1971 p. 61 (registro); Maldonado–Ocampo, 2005 p.162 (registro).

Diagnosis La especie se distingue de sus congeneres por la ausencia de supraneurales, menos de 60 dientes en el premaxilar, por el borde posterior del mesetmóides y la lámina orbitonasal unidos al frontal por una banda de cartílago, y la forma de la fontanela craneal (fig. 4B).

Descripción Forma del cuerpo Los datos morfométricos y merísticos se registran en la tabla 1. Cuerpo alargado y comprimido progresivamente hacia la aleta caudal. Desde el

Ruiz–C. & Román–Valencia

hocico hasta el inicio de la aleta dorsal se observa un perfil del cuerpo ligeramente convexo. Hocico achatado tanto en vista dorsal como lateral. Boca inferior. Las barbillas maxilares sobrepasan el extremo de las aletas pectorales y el origen de la aleta dorsal. Las barbillas mentonianas externas llegan hasta la base de las aletas pectorales. Las barbillas mentonianas internas llegan hasta las aberturas branquiales. Ojos grandes, ubicados dorso–lateralmente.

Origen de la aleta dorsal ubicado en posición anterior al origen de las aletas pélvicas. Tercer radio ramificado de la aleta dorsal más largo que los demás. Sin espinas punzantes en aleta dorsal y pectoral; en éstas últimas, el primer radio ramificado es más largo que el resto; sin alcanzar el origen de las pélvicas, las cuales tampoco llegan hasta el origen de la anal. Aleta anal con el borde posterior convexo. Aleta caudal con lóbulos cortos y redondeados.

Osteología (figs. 3B, 4B) Menos de 60 dientes en el premaxilar rectos y puntiagudos dispuestos en parches. Rastrillos branquiales en todos los arcos branquiales, filamentos no bífidos. Veinticuatro a veintiséis filamentos en dos series presentes en los cuatro arcos.

Dientes vómero–palatinos ausentes y extremo anterior de los palatinos cartilaginoso. La lámina orbitonasal en posición oblicua, unida a los extremos antero laterales del frontal por una banda de cartílago; unida al borde posterior del mesetmóides por una banda de cartílago que lo cubre anterolateralmente; apófisis posteriores del mesetmóides reducidas. Longitud y forma de la fontanela craneal anterior y posterior es ancha y se bifurca en su extremo anterior. Banda de cartílago presente sobre la unión superficial del pterótico y parietal. Extremo posterior del proceso parieto– supraoccipital delgado y en forma de "v". La cápsula ótica pronunciada. Procesos laterales del complejo Weberiano con proyecciones ramificadas en sus extremos, se observan entre 4 y 5 ramificaciones. La parte laminar posterior a éstas ramificaciones es rectangular. La rama posterior del cuarto proceso transversal es corta y puntiaguda. No se observa supraneural. El pterigióforo del primer radio de la aleta dorsal insertado anterior a la octava vértebra. Proceso cleitral posterior delgado y puntiagudo. Número total de vértebras: 39.

Color en vida Área dorsal café o gris–oscuro, más claro en la parte lateral del cuerpo. Área ventral posterior a las aletas pélvicas, de color gris–oscuro o blanco– plateado y amarillo brillante con tonos grises a nivel de las branquias. Una banda lateral oscura se extiende desde la parte posterior del opérculo y alcanza la base de aleta caudal. Hocico con una banda oscura que atraviesa esta parte de la cabeza de lado a lado. Área dorsal a nivel de la cabeza presenta dos bandas anchas oscuras, alternada

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Animal Biodiversity and Conservation 29.2 (2006)

Tabla 1. Datos morfométricos y merísticos de Cetopsorhamdia boquillae, Cetopsorhamdia nasus y Cetopsorhamdia iheringii. Longitudes estándar y total en mm, el resto de longitudes son porcentajes de la longitud estándar. Todas las medidas con los promedios entre paréntesis.

Table 1. Morphometric and meristic data of Cetopsorhamdia boquillae, Cetopsorhamdia nasus y Cetopsorhamdia iheringii. Standard and total length given in mm, other lengths are percentages of the standard length. All measures with means into parenthesis.

C. boquillae n = 55

C. boquillae n=3

C. nasus n = 16

C. iheringii n=6

Datos morfométricos Longitud estándar

27,8–75,6 (44,0)

26,4–36,9 (31,7)

29,7–88,7 (46,0)

32,6–63,9 (43,5)

Longitud total

34,7–86,0 (53,4)

32,0–44,2 (38,1) 35,9–113,1 (56,5)

40,7–81,1 (61,5)

Longitud cabeza

19,4–24,9 (22,6)

21,5–25,7 (23,6)

22,9–29,3 (26,0)

19,1–24,8 (21,4)

Profundidad cabeza

12,4–17,8 (14,7)

12,1–15,5 (13,8)

12,7–16,7 (15,3)

15,4–16,3 (15,3)

Profundidad cuerpo

13,0–19,5 (16,1)

15,1–16,1 (15,6)

12,7–16,7 (15,8)

14,8–17,8 (15,7)

Distancia predorsal

34,5–56,2 (39,8)

35,9–41,0 (38,4)

31,1–36,8 (34,2)

36,7–42,2 (38,2)

Distancia prepélvica

41,7–47,6 (44,5)

44,9–45,7 (45,3)

39,8–44,9 (42,1)

44,4–51,5 (47,6)

Distancia preanal

61,4–72,7 (67,8)

66,6–68,6 (65,6)

64,0–66,2 (68,2)

65,7–74,5 (69,5)

Distancia preadiposa

55,0–67,5 (60,1)

63,9–65,7 (64,8)

58,7–70,3 (64,2)

63,3–71,0 (67,9)

6,9–11,5 (9,5)

9,3–11,0 (10,1)

6,7–9,1 (7,8)

8,1–9,9 (9,2)

Long pedúnculo caudal Distancia aleta dorsal–aleta adiposa

18,8–24,9 (22,1)

23,4–26,8 (25,1)

26,4–35,2 (30,2)

24,5–32,0 (28,7)

Long. base aleta dorsal 10,3–11,6 (11,1)

16,2–17,6 (16,9)

9,9–19,4 (12,9)

9,4–11,8 (10,6)

Long. base aleta adiposa 20,1–34,4 (28,6)

25,7–29,7 (27,7)

23,2–27,6 (25,4)

13,9–18,3 (16,5)

Altura aleta adiposa

22,3–25,9 (24,1)

21,3–28,1 (24,7)

16,4–25,9 (20,7)

9,4–16,1 (13,0)

Long. base aleta anal

10,9–15,7 (13,7)

10,8–14,3 (12,6)

10,8–18,9 (14,3)

10,7–17,9 (14,4)

Long. aletas pectorales 14,1–20,2 (17,8)

15,9–16,2 (16,1)

12,5–21,5 (14,8)

15,7–19,3 (17,8)

Long. aletas pélvicas

12,4–16,6 (14,0)

13,4–14,2 (13,8)

10,8–18,9 (15,8)

14,9–17,3 (16,2)

Ancho cleitral

13,5–19,3 (16,2)

16,0–16,7 (16,3)

13,5–18,7 (15,6)

13,8–17,5 (13,3)

9,89–46,13 (35,17) 31,2–35,7 (33,5)

31,6–46,1 (37,7)

19,3–25,9 (22,3)

lateral mentonianas 4,06–25,16 (18,79) 12,1–14,8 (13,5)

12,9–19,7 (17,9)

8,5–9,9 (9,2)

medial mentonianas 7,84–17,42 (12,89) 8,2–17,4 (11,8)

Longitudes barbillas maxilares

8,1–18,3 (12,8)

7,8–13,4 (10,4)

Anchura bucal

7,58–10,29 (8,91) 10,1–11,4 (10,7)

6,2–9,7 (8,0)

7,7–10,6 (8,5)

Ancho interorbital

6,59–11,97 (8,49)

8,1–9,4 (8,7)

5,9–8,8 (6,9)

6,3–7,4 (6,8)

2,0–4,4 (3,0)

3,0–3,8 (3,4)

3,4–5,5 (4,4)

3,4–4,2 (3,9)

7,14–10,47 (8,97)

9,4–10,1 (9,8)

6,9–9,6 (7,9)

9,1–10,7 (9,8)

2,8–7,21 (4,2)

4,1–5,2 (4,7)

2,9–4,0 (3,3)

2,5–4,8 (3,9)

Diámetro ojo Longitud hocico Anchura entre narinas anteriores Datos merísticos Nº radios aleta dorsal

I,5–7

I,6

I,6

I,6

Nº radios aletas pectorales

I,7–8

I,8

I,8

I,8–9

Nº radios aletas pélvicas

I,5–6

I,4–5

I,5

I,5–6

Nº radios aleta anal

v–vi,7–9

iv,7

iv,6–7

iii,6–7

Nº radios aleta caudal

7–9/8–9

7–9/8–9

7/7–9

9/9

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1 cm

Fig. 1. Cetopsorhamdia boquillae, IUQ 466; 44,36 mm de longitud estándar. Río La Vieja, Alto Cauca, Colombia.

Fig. 1. Cetopsorhamdia boquillae, IUQ 466; 44.36 mm SL; Colombia, La Vieja River, Upper Cauca, Colombia.

1 cm

Fig. 2. Cetopsorhamdia nasus, IUQ 470; 36,6 mm de longitud estándar, Alto Río Magdalena, Colombia.

Fig. 2. Cetopsorhamdia nasus, IUQ 470; 36.6 mm SL, Colombia, Magdalena River, Colombia.

por dos bandas estrechas claras. Tres manchas oscuras presentes alrededor de la aleta dorsal: una en la base de la aleta dorsal, la segunda se localiza en la parte media posterior de esta aleta y la tercera se ubica entre la aleta dorsal y la aleta adiposa. Aletas café–claro con manchas oscuras sobre un fondo claro.

Ecología y distribución En las quebradas La Criolla y Cabuche en el Alto río Magdalena, los datos y observaciones obtenidas el 17 y 18 de diciembre de 1998 y el 28 de abril del 2002 fueron los siguientes: temperatura superficial del agua entre 18 y 24°C, temperatura del aire 18–26°C, oxígeno disuelto 5,1–7,3 ppm, pH 7,3–7,8. Color del agua cristalino en período de "verano", café en "invierno", sustrato conformado por lodo, piedra y arena, de ancho 3–4 m, profundidad 0,3–0,4 m. La especie habita pequeños remansos de sustrato conformado por piedras, material vegetal en descomposición y orillas conformadas por vegetación de tipo arbustiva.

Discusión Cetopsorhamdia boquillae fue descrita por Eigenmann (1922) con base en 12 ejemplares provenientes de Boquía en el río Quindío; este ejemplar no pudo ser fijado adecuadamente (Eigenmann, 1922). Según el artículo 32 del código internacional de nomenclatura zoológica (ICZN, 1999) y a pesar del error de ortografía, el nombre válido es C. boquillae, por que al parecer, Eigenmann (1922), confundió Boquia en el río Quindío–Alto Cauca, con Boquilla, localidad de la costa del Caribe de Colombia, cerca de Cartagena. Cetopsorhamdia boquillae se distingue de C. nasus por la distancia aleta adiposa–aleta dorsal y es estadísticamente significativa (F = 21, P = 0,05), por el número de radios simples principales de la aleta anal (5–6 en C. boquillae, 4 en C. nasus) (tabla 1), por el pterigióforo del primer radio de la aleta dorsal insertado anterior (a la novena vértebra en C. boquillae vs. octava vértebra en C. nasus). Extremo anterior de los palatinos (en C. boquillae es

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Animal Biodiversity and Conservation 29.2 (2006)

A

B

1 mm

1 mm

Fig. 3. Vista dorsal del complejo neural de Cetopsorhamdia boquillae, IUQ 474 (A) y de Cetopsorhamdia nasus, IUQ 475 (B).

Fig. 3. Neural complex dorsal area of Cetopsorhamdia boquillae, IUQ 474 (A) and of Cetopsorhamdia nasus, IUQ 475 (B).

A

B pm

mes

pvm

pvm

la

mes la

co

f

f co

es

es pt

pt

1 mm

so

1 mm

so

Fig. 4. Vista dorsal del cráneo de Cetopsorhamdia boquillae, IUQ 460 (A) y de C. nasus, IUQ 475 (B): co. Cápsula ótica; es. Esfenótico; f. Frontal; la. Lámina orbitonasal sensu latu; mes. Mesetmóides; pm. Premaxilar; pvm. Proceso ventral del mesetmóides; pt. Pterótico; so. Parieto–supraoccipital.

Fig. 4. Cranium dorsal area of Cetopsorhamdia boquillae, IUQ 460 (A) and of C. nasus, IUQ 475 (B): co. Otic capsule; es. Sphenotic; f. Frontal; la. Orbithonasal lamine sensu latu; mes. Mesethmoid; pm.

Premaxilla; pvm. Mesethmoid ventral process; pt. Pterotic; so. Parieto–supraoccipital.

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óseo, mientras que en C. nasus es cartilaginoso); longitud y forma de la fontanela craneal anterior y posterior (en C. boquillae es alargada y estrecha, mientras que en C. nasus es ancha y se bifurca en su extremo anterior (figs. 3A, 3B), por el número de vértebras (36 en C. boquillae, 39 en C. nasus), por una banda de cartílago que cruza el pterótico (presente en C. nasus, ausente en C. boquillae) (figs. 4A, 4B), por las dos apófisis posteriores del mesetmóides (reducidas en C. nasus, alargadas y se prolongan sobre el frontal en C. boquillae), por la de barra epifiseal (ausente en C. boquillae, presente en C. nasus), por la cápsula ótica (pronunciada en C. nasus, reducida en C. boquillae). Y finalmente C. boquillae se distribuye en el alto Cauca, mientras C. nasus se distribuye en el Alto Magdalena (en evidente distribución alopátrica), sin embargo, Schultz (1944) registra a C. boquillae para la cuenca del Magdalena cerca de Honda, lo cual es un error de localización, pues éste sitio corresponde a la distribución de C. nasus. Schultz (1944) no examinó material de C. boquillae.

Al comparar las especies objeto de éste estudio con C. iheringi se encontraron diferencias en la longitud y altura de aleta adiposa, también en el número de radios simples de la aleta anal (tabla 1). Dahl (1971) y Miles (1971) presentaron una clave diagnostica para las tres especies reportadas para la cuenca del río Magdalena (C. boquillae, C. molinae y C. nasus). Al aplicar la clave a especies de Cetopsorhamdia y las descripciones de Miles (1971, 1973) en las muestras examinadas en el presente trabajo, se observa que todos los caracteres para éstas especies no se cumplen.

Un caso semejante se observa en las “descripciones” simples con base en caracteres externos, sin datos sustentables, anotadas por Maldonado– Ocampo et al. (2005).

En el libro divulgativo (Ortega et al., 2000) se observa que el ejemplar fotografiado como Cetopsorhamdia sp. corresponde plenamente a C. boquillae, mientras la figura correspondiente a C. boquillae es una determinación errónea. No es posible efectuar un análisis comparativo con nuestros datos para su identificación, pues no hay observaciones (= datos) para una determinación confiable.

Cetopsorhamdia molinae fue descrita con base en un ejemplar colectado en Bugalagrande (Miles, 1943, 1973). No fue posible examinarlo porque en la actualidad no aparece en las muestras que aún subsisten y que fueron colectadas por Miles en la década de los años 40. En éstas condiciones, el ejemplar se perdió (Maldonado–Ocampo et al., 2005). Del material de Cetopsorhamdia capturado por nosotros en la cuenca del río Bugalagrande se observa que coincide en biometría con C. boquillae (tabla 1). Maldonado–Ocampo et al. (2005) la citan para algunas localidades del Alto Cauca, ríos Sumapaz y Coello afluentes del río Magdalena; lo cual evidencia un error en su modelo de distribución geográfica seguido por éstos pequeños bagres (C. molinae y C. nasus) en los Andes

de Colombia. Las figuras y las observaciones principalmente coloración en vivo (Ortega et al., 2000; Maldonado–Ocampo et al., 2005) anexa a C. molinae, son muy semejantes a la coloración en vivo observada en el río La Vieja para Pseudopimelodus zungaro (Román–Valencia, 2004). En estas condiciones no es posible analizar el estado taxonómico de C. molinae.

Agradecimientos A Francisco Langeani (DZSJRP) por el préstamo de material de comparación. Mario Cardona colaboró durante el trabajo de campo en algunas localidades del Alto Cauca y Alto Magdalena. Carlos A. García (IUQ) preparó las figuras 1 y 2. El artículo se benefició de las correcciones y sugerencias de Richard P. Vari (USNM), y dos revisores anónimos.

IDEA WILD suministró el equipo de campo.

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Diogo, R., Chardon, M. & Vandewalle, P., 2004. On the osteology and myology of the cephalic region and pectoral girdle of Franciscodoras marmoratus (Lütken 1874), comparison with other doradids, and comments on the synapomorphies and phylogenetic relationships of the Doradidae (Teleostei: Siluriformes). Animal Biology, 54: 175–193.

Eigenmann, C. H., 1922. The fishes of the northwestern South America. Part I. The fresh–water fishes of northwestern South America, including Colombia, Panama, and the Pacific slopes of Ecuador and Peru, together than appendix open fishes of the Rio Meta in Colombia. Memoirs of Carnegie Museum, 9: 1–346.

Eigenmann, C. H. & Fisher, H., 1916. New and rare fishes from South American rivers. Annals of the Carnegie Museum, 10: 77–86.

Eschmeyer, W., 2003. CAS. Ichthyology–Catalog of fishes. California Academy of Sciences, San Francisco, CA, USA.

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Tambien disponible en línea: http: //www.calacademy.org/research/ichthyology/ catalog//fishcatsearch.html.

Ferraris, C. J. Jr., 1988. Relationships of the Neotropical catfish genus Nemuroglanis, with description of a new species (Osteichthyes: Siluriformes: Pimelodidae). Proceedings of the Biological Society of Washington, 101: 509–516.

Fink, V. S. & Fink, W. L., 1981. Interrelationships of the ostariophysan fishes (Teleostei). Zoological Journal of the Linnean Society, 72: 297–353 ICZN (International Commision on Zoological Nomenclature), 1999. International Code of Zoological Nomenclature, 4th edition. International Trust of Zoological Nomenclature, London.

Lundberg, J. G. & McDade, L. A., 1986. On the South American catfish Brachyrhamdia imitator Myers (Siluriformes, Pimelodidae), with phylogenetic evidence for a large intrafamilial lineage. Notulae Naturae, 463: 1–24.

Lundberg, J. G., Bornbusch, A. H. & Mago–Leccia, F., 1991. Gladioglanis conquistador n. sp., from Ecuador with diagnoses of the subfamilies Rhamdiinae Bleeker and Pseudopimelodinae n. subf. (Siluriformes: Pimelodidae). Copeia, 1991: 190–209.

Maldonado–Ocampo, J. A., Ortega–Lara, A., Usma, O. J. S., Galvis, V. G., Villa–Navarro, F. A., Vasquez, G. L., Prada–Pedreros, S. & Ardila, R. C., 2005.

Peces de los Andes de Colombia. Instituto de Investigación de Recursos Biológicos "Alexander von Humboldt", Bogotá, D. C. Colombia.

Miles, C. W., 1943. Peces de agua dulce del Valle del Cauca. Publicaciones de la Secretaria de Agricultura del Depto. del Valle del Cauca, Cali.

– 1947. Los peces del río Magdalena. Ministerio de Economía Nacional, Sección de Piscicultura, Pesca y Caza, Bogotá.

– 1971. Los Peces del Río Magdalena. Edic.

Universidad del Tolima, Ibagué, Colombia. (reimpresión).

– 1973. Estudio económico y ecológico de los peces de agua dulce del Valle del Cauca.

Cespedesia, 5: 9–64 (reimpresión).

Ortega, L. O., Murillo, O. E. C., Pimienta, M. C. I. & Sterling, J. E., 2000. Peces de la cuenca alta del río Cauca: riqueza ictiológica del Valle del Cauca CVC. Román–Valencia, C., 1988. Clave taxonómica para la determinación de peces nativos del Departamento de Quindío, subsistema Alto río Cauca, Colombia. Actualidades Biológicas, 17: 107–114.

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– 1995. Lista anotada de los peces de la cuenca del río La Vieja, Alto Cauca, Colombia. Boletín Ecotrópica, 29: 11–19.

– 2004. Datos bioecológicos del peje sapo, Pseudopimelodus zungaro (Pisces: Pimelodidae), de los ríos Atrato y La Vieja, Colombia. Dahlia (Revista de la Asociación Colombiana de Ictiólogos), 7: 29–31.

Román–Valencia, C., Lehmann–A., P. & Muñoz, A., 1999. Presencia del género Callichthys (Siluriformes: Callichthyidae) en Colombia y descripción de una nueva especie para el alto río Cauca, Colombia. Dahlia (Revista de la Asociación Colombiana de Ictiólogos), 3: 53–62.

Román–Valencia, C. & Ruiz–C., R. I., 2005. Diet and reproduction aspects of Astyanax aurocaudatus (Teleostei: Characidae) from the upper part of the Río Cauca, Colombia. Dahlia (Revista de la Asociación Colombiana de Ictiólogos), 8: 9–17.

Román–Valencia, C. & Giraldo, P. A., 2006. Ecología trófica y reproductiva de Cetopsorhamdia boquillae (Pisces: Pimelodidae) en el río La Vieja, Alto Cauca, Colombia. Revista de Investiga– ciones, Universidad del Quindío, 16: 33–45.

Schubart, O. & Gomes, A. L., 1959. Descrição de "Cetopsorhamdia iheringi" sp. n. (Pisces, Nematognathi, Pimelodidae, Luciopimelodinae).

Revista Brasileira de Biología, 19: 1–8.

Schultz, L. P., 1944. The catfishes of Venezuela, with descriptions of thirty–eight new forms.

Proccedings of the United States National Museum, 94: 173–338.

Silfvergrip, A. M. C., 1996. A systematic revision of the Neotropical catfish genus Rhamdia (Teleostei, Pimelodidae). Swedish Museum of Natural History, Stockholm, Suecia.

Song, J. & Parenti, L. R., 1995. Clearing and staining whole fish specimens for simultaneous demonstration of bone, cartilage and nerves.

Copeia, 1995: 114–118.

Stewart, D. J., 1985. A new species of Cetopsorhamdia (Pisces: Pimelodidae) from the Rio Napo basin of Eastern Ecuador. Copeia, 1985: 339–344.

– 1986. A new pimelodid catfish from the deep– river channel of the Río Napo, eastern Ecuador (Pisces: Pimelodidae). Proceedings of the Academy of Natural Sciences of Philadelphia, 38: 46–52.

Taylor, W. R. & Van Dyke, G. C., 1985. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9: 107–119.

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"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 29.2 (2006)

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Effect of different mowing regimes on butterflies and diurnal moths on road verges A. Valtonen, K. Saarinen & J. Jantunen

Valtonen, A., Saarinen, K. & Jantunen, J., 2006. Effect of different mowing regimes on butterflies and diurnal moths on road verges. Animal Biodiversity and Conservation, 29.2: 133–148.

Abstract Effect of different mowing regimes on butterflies and diurnal moths on road verges.— In northern and central Europe road verges offer alternative habitats for declining plant and invertebrate species of semi– natural grasslands. The quality of road verges as habitats depends on several factors, of which the mowing regime is one of the easiest to modify. In this study we compared the Lepidoptera communities on road verges that underwent three different mowing regimes regarding the timing and intensity of mowing; mowing in mid–summer, mowing in late summer, and partial mowing (a narrow strip next to the road). A total of 12,174 individuals and 107 species of Lepidoptera were recorded. The mid–summer mown verges had lower species richness and abundance of butterflies and lower species richness and diversity of diurnal moths compared to the late summer and partially mown verges. By delaying the annual mowing until late summer or promoting mosaic–like mowing regimes, such as partial mowing, the quality of road verges as habitats for butterflies and diurnal moths can be improved.

Key words: Mowing management, Road verge, Butterfly, Diurnal moth, Alternative habitat, Mowing intensity.

Resumen Efecto de los distintos regímenes de siega de los márgenes de las carreteras sobre las polillas diurnas y las mariposas.— En Europa central y septentrional los márgenes de las carreteras constituyen hábitats alternativos para especies de invertebrados y plantas de los prados semi–naturales cuyas poblaciones se están reduciendo. La calidad de los márgenes de las carreteras como hábitats depende de diversos factores, de los cuales el régimen de siega es de los más fáciles de modificar. En este estudio se compararon las comunidades de lepidópteros de los márgenes de las carreteras que sufrieron tres regímenes distintos de siega, según el momento y la intensidad de la siega; siega a mediados del verano, siega a finales de éste, y siega parcial (una estrecha franja próxima a la carretera). Se estudiaron un total de 12.174 individuos y 107 especies de lepidópteros. Los márgenes segados a mediados de verano presentaban una menor riqueza de especies y abundancia de mariposas, y una menor riqueza de especies y diversidad de polillas diurnas, en comparación con los márgenes segados a finales de verano o segados parcialmente. Retrasando la siega anual hasta finales del verano, o promoviendo regímenes de siega en forma de mosaico, tales como la siega parcial, podría mejorarse la calidad de los márgenes de las carreteras como hábitats para las mariposas y las polillas diurnas.

Palabras clave: Gestión de la siega, Margen de la carretera, Mariposa, Polilla diurna, Hábitat alternativo, Intensidad de la siega.

(Received: 5 IV 06; Conditional acceptance: 29 V 06; Final acceptance: 30 VI 06) Anu Valtonen, Kimmo Saarinen and Juha Jantunen, South–Karelia Allergy and Environment Inst., Lääkäritie 15, FIN–55330 Tiuruniemi, Finland.

Corresponding author: A. Valtonen. E–mail: all.env@inst.inet.fi ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introduction A large number of plant and insect species living in temporal and boreal landscapes in Europe are ecologically fitted to semi–natural grasslands created by mowing or grazing regimes under traditional farming (Pykälä, 2000; Van Swaay, 2002).

The agricultural intensification and abandonment of low–productive agricultural areas throughout Western Europe has, however, led to the steep decline of semi–natural grasslands and the associated fauna and flora (Thomas, 1995; Van Swaay & Warren, 1999; Poschlod & WallisDeVries, 2002). The semi– natural biotopes in Finland, for example, now cover less than 1% of the corresponding area one century ago (Vainio et al., 2001). Consequently, many ruderal areas such as road verges are recognised as important habitats for several endangered species of semi–natural biotopes (Rassi et al., 2001).

The potential of road verges is based, on one hand, on their large area, which in Finland is at least 50–fold compared to the area of remaining semi– natural grasslands on mineral soils (Valtonen & Saarinen, 2005), and on the other hand on their regular mowing management, which somewhat resembles the management of semi–natural grasslands.

In general, a regular mowing regime followed by hay removal has a positive effect on vascular plant species richness on road verges (Parr & Way, 1988; Persson, 1995; Schaffers, 2000). In contrast, among invertebrates many species of Arachnida (Kajak et al., 2000), Orthoptera (Guido & Gianelle, 2001), Coleoptera (Morris & Rispin, 1988), Diptera and Lepidoptera (Völkl et al., 1993) and Hemiptera (Helden & Leather, 2004) suffer from mowing, although some species of these groups may respond favourably (Morris, 1981; Morris & Rispin, 1988). Butterflies are frequently used as indicators of changes in habitat structure and management and they are adversely affected by mowing (Erhardt, 1985; Feber et al., 1996; Gerell, 1997; New, 1997; Hogsden & Hutchinson, 2004; Valtonen & Saarinen, 2005). In the long term, however, mowing has a positive effect on meadow butterflies as it prevents the growth of bushes and trees (Erhardt, 1985). It has been observed to be a practical tool for maintaining an appropriate habitat for butterflies in savannahs in North America, for example (Swengel, 1995).

There are, however, profound differences in the management of road verges and traditional biotopes.

Traditional management of meadows included either one mowing event in July or grazing, whereas road verge management in general can be divided into two categories. It can include mowing of either the whole verge, or only part of it. Totally mown verges are generally subjected to one or two mowings per year, timed in mid–summer (from June to early July) and /or late summer (from late July to September).

Partially mown verges receive one or several mowings annually, covering a narrow (usually 2 m) strip next to the road; this is combined with total mowing at intervals of approximately 3 years in order to prevent the growth of trees and bushes. Partial mowings are

Valtonen et al.

also typical on verges mown totally every year, and can occur before or after the total mowing. Removal of cut material, inherent to the traditional management, is rare on road verges and the mowing equipment frequently includes crushing blades instead of the traditionally used cutting blades. In addition, in a large proportion of verges the soil is disturbed due to construction works on an average of once every 20– 30 years (Mahosenaho & Pirinen, 1999).

If available, decision–support systems using databases on road verge flora and fauna can be used to select the best management measure for each road verge site (Siepel, 1997). However, in most cases such information is lacking and more general guidelines are needed. Ways to increase the suitability of managed grasslands for butterflies include promoting native rather than non–native vegetation (Ries et al., 2001; Valtonen et al., in press), avoiding the use of herbicides (Ries et al., 2001), removing cuttings (Schmitt, 2003), and avoiding mid–summer mowing (Feber et al., 1996; Valtonen & Saarinen, 2005).

Although poorly studied, rotational (Gerell, 1997) and mosaic–like (Munguira & Thomas, 1992) mowing regimes on road verges have been recommended.

However, the narrow shape of road verges, the variable topography and vegetation, the large area, and demands for improving traffic safety set limits on management. Over–intensive mowing regimes, nowadays common on many urban road verges, are both expensive and harmful to meadow insects (Saarinen et al., 2005). Mowing once a year, however, the original mowing frequency on semi–natural grasslands, may not be sufficient for verges suffering from a predominance of hay grasses or other competitive plant species (Hellström, 2004). Partial mowing of road verges is a kind of a compromise that meets the demand of sustaining traffic safety throughout the summer while also avoiding mid–summer mowing in the major part of the verge. This management regime, that includes less intensive management of the "edge"’ vegetation of verges, is suggested to be beneficial to butterflies (Warren, 1985; Munguira & Thomas, 1992), but to our knowledge it has not yet been compared to other mowing regimes.

This study compared the effects of three different mowing regimes of road verges on butterfly and diurnal moth species richness, diversity, abundance, and species composition. The three regimes differed in timing and intensity of mowing. All road verges included some kind of mowing, as this measure is considered to ensure traffic safety. These three mowing regimes represent commonly applied mowing practices in Finland, thereby providing a realistic understanding of their long–term effects on Lepidoptera. The mowing regimes were: 1) total mowing in mid–summer (with possible partial mowing in late summer), 2) total mowing in late summer (with possible partial mowing in mid–summer), and 3) one or more partial mowings during the summer (leaving some undisturbed vegetation throughout the study season). Management in the last regime was the most variable, since the sites were either totally mown after the study season (September) or

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Animal Biodiversity and Conservation 29.2 (2006)

Material and methods Study sites and transect counts The same number of study sites (N = 54) was assigned to each of the three mowing regimes: (i) mid–summer mown verges (n = 18) were mown totally before or during week 28, (ii) the late summer mown verges (n = 18) were subjected to the first total mowing after or during week 31 and (iii) the partially mown verges (n = 18) were mown at any time during the study period, but a substantial part of the verge always remained unmown. Due to the variation in the timing and intensity of mowing within the three regimes, their validity was examined by calculating a mowing index describing the total effect of mowing on the vegetation over the study period. The index was based on the mowing week, the number of times the verge was mown and the area mown.

Each week was given a mowing intensity value (0 = no mowing, 1/2 = partial mowing, 1 = total mowing); the value was reduced to the lower level (from 1 to 1/2 and from 1/2 to 0) seven weeks after the mowing due to the regeneration of vegetation. The sum of weekly values, i.e. the mowing index for the site, ranged from 1 to 10.5.

The index of the partially mown verges was generally the lowest, that of the late–summer mown verges was intermediate, and that of the mid– summer mown verges was the highest (fig. 1).

Located along the road network in the Imatra– Lappeenranta region, SE Finland, the sites included highway verges (n = 19), urban road verges (n = 26) and paved rural road verges (n = 9). Study sites with strong spatial dependence, i.e. located in close proximity to each other, were considered to belong to the same study areas (N = 27). Six study areas included sites belonging to several mowing regimes, while all the others included only sites belonging to one regime.

Butterflies (Hesperioidea, Papilionoidea) and other day–active Lepidoptera (Zygaenoidea, Lasiocampoidea, Bombycoidea, Geometroidea, Noctuoidea) were studied along a 250 m transect in each site. The names of the Lepidoptera species follow the checklist by Kullberg et al. (2002).

All the transects were censused once a week between early June (week 23) and late August (week 35), resulting in 13 counts. All individuals

10 9 8 Mowing index

only once approximately every 3 years. Two hypotheses were assumed: (i) total mowing in late summer, leaving resources undisturbed during the peak flight period, is more favorable to the Lepidoptera fauna than total mowing in mid–summer and (ii) a management regime based on only partial mowing is more beneficial to Lepidoptera than the management regimes that include total mowing as some resources are always available for all life– stages of Lepidoptera. Suggestions for road verge management are given in the discussion.

7 6 5 4 3 2 1 0

Msm

Lsm

Pm

Fig. 1. Boxplot diagrams illustrating differences in mowing indices between the three mowing regimes: Intersection line. Median; Box. First and third quartiles; Whiskers. Largest and smallest observations falling within a distance of 1.5 times the box size from the nearest quartile; Circles. Outliers, observations with values between 1.5 and 3 box lengths from the upper or lower edge of the box; Msm. Mid summer mown; Lsm. Late summer mown; Pm. Partially mown.

Fig. 1. Diagramas de caja que ilustran las diferencias en los índices de siega entre los tres regímenes de siega: Línea de intersección.

Mediana; Caja. Cuartiles primero y tercero; Bigotes. Observaciones mayor y menor incluidas dentro de una distancia de 1,5 veces el tamaño de la caja desde el cuartil más próximo; Círculos. Outliers, observaciones con valores entre 1,5 y 3 veces la longitud de la caja desde los bordes superior o inferior de dicha caja; Msm. Siega a mediados de verano; Lsm. Siega a finales de verano; Pm. Siega parcial.

within a 5 x 5 m square in front of the recorder were noted (Pollard & Yates, 1993). Due to the low number of individuals recorded per count (17, on average), the probability of recounting the same specimen was low. All the transect counts were conducted between 9:00 a.m. and 5:30 p.m. in satisfactory weather conditions. The minimum temperature for censuses was 12°C, and the average was 20.5°C. The wind speed on the Beaufort scale was 5 or below, with the median wind speed being 2. Estimated in percentages (0, 25, 50, 75, 100%), the sunshine percentage was 75% or above in 86% of the counts, the median of all counts

Valtonen et al.

136

being 100%. Sites were censused over a 3–year period, and each site was studied in one year only: 15 sites in 2002, nine sites in 2003, and 30 sites in 2004. According to the Finnish Meteorological Institute, the three years differed in their weather conditions. Summer 2002 was warm, with a rainy June and July but a dry August. In summer 2003 a cool June was followed by a warm July and normal August, with rainfall following the long–term average. Summer 2004 was rainy, but temperatures followed long–term averages. A total of 702 counts resulted over the three seasons.

Environmental variables The verge width and the variables describing the vegetation and the surrounding environment were measured for each study site (N = 54) together with other environmental variables for each study area (N = 27). Road width was measured in metres, the local speed limit was used as a measure of the traffic speed (a reasonable measure in the local conditions), and the traffic density was estimated on an ordinal scale ranging from 0 (no traffic) to 4 (heavy traffic according to local scale, with up to 13,700 vehicles per day). The verge width was measured in metres and the age was evaluated as years since the last disturbance to the soil, for example for construction work. The oldest age was set at 25 years according to the average frequency of road verge construction. Soil moisture was estimated on an ordinal scale ranging from 1 (dry) to 3 (moist). The vegetation height and the plant species within the transect were recorded three times per season, i.e. in the middle of June, in July, and in August. Vegetation height was measured from the centre of the transect and in partially mown verges the average was taken from the mown and non–mown parts. Each plant species was given a value describing its abundance on the transect ranging from 1 (only a few observations) to 3 (very abundant). The information on the abundance of plant species was used when estimating the quality of the vegetation by summing the abundances of positive or negative indicator species of traditional biotopes in each site based on the classification by Pykälä (2001). Similarly, abundances of the most important larval host plants were summed for each site based on the information by Seppänen (1970).

The abundance of flowering plants (other than Poaceae) and nectar plants important for adult butterflies (Mikkola & Tanner, 2001) were calculated accordingly. The surrounding environment was classified using coverage (%) of open uncultivated land (meadows, fallow or unmanaged sites), open cultivated land (fields, gardens), and forests. The evaluation was based on two zones, the inner one (< 10 m) being evaluated on the side of the road where the transect was located and the outer one (10–50 m) being evaluated on both sides of the road. The value of the inner zone had double weighting in the calculation of the average cover for each landscape class around the study sites.

Data analysis Differences in butterfly and diurnal moth species richness, diversity and abundance between the study sites of the three mowing regimes were investigated by mixed–effects ANOVA conducted by the MIXED procedure of the SAS (SAS Institute, 1996).

The mowing regime was assigned as a fixed–effect, whereas the study area and the study year were set as the random–effect variables to account for the spatial and temporal dependence (e.g. differences in the weather conditions of the three study years) in the data. Pairwise comparisons (Tukey–Kramer) were undertaken where significant differences (P < 0.05) were found. The square root (diurnal moth abundance, diurnal moth species richness) and logarithmic (total abundance, butterfly abundance) transformations were conducted where appropriate to improve the normality. Species diversity was calculated using the Shannon index S H ' = – j pi ln pi , i

where S = number of species and pi = abundance of species i / total abundance.

Differences in the species composition the three mowing regimes and over the three study years were tested with a non–parametric multi–response permutation procedure (MRPP) using a Euclidean distance measure (Zimmerman et al., 1985). Indicator species analysis was used to find the most characteristic species of each regime (Dufrene & Legendre, 1997). The statistical significances of indicator values were tested using the Monte Carlo technique with 1,000 runs. The MRPP and indicator species analysis were performed by PC–ORD 4.0 (McCune & Mefford, 1999).

Differences in environmental conditions between the three mowing regimes were also compared.

Variables recorded for each study area, independent of the study year, were tested with a non–parametric Kruskal–Wallis test conducted by SPSS. The verge width and variables describing the surrounding environment recorded for each study site were also tested with the Kruskal–Wallis test by taking averages within each study area. Separate averages were calculated for sites belonging to the same study area but different mowing regime. Pair–wise comparisons were calculated according to Siegel & Castellan (1988). The differences in the vegetation variables were compared with mixed–effects ANOVA, using the same procedure as described above with the Lepidoptera variables. The abundance of host plants was square root transformed and the vegetation height was logarithmically transformed.

Finally, non–parametric Spearman correlations were calculated between Lepidoptera variables and the environmental variables to investigate alternative explanatory factors for the Lepidoptera species richness and abundance. A sequential Bonferroni correction was used in all tables to lower the risk of significant differences by chance, using an error rate of 10% as suggested by Chandler (1995).

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Animal Biodiversity and Conservation 29.2 (2006)

Results A total of 12,174 individuals and 107 species of Lepidoptera were recorded in censuses and approximately half of the species (46%) and individuals (51%) were butterflies (table 1). The 49 butterfly species recorded consisted of approximately 50% of the resident butterfly fauna in Finland (Huldén et al., 2000). One threatened butterfly species, the Green–underside Blue Glaucopsyche alexis (VU) (Rassi et al., 2001) was recorded.

Forty–one percent of the butterfly species and 79% of individuals represented species typical of meadows, 41% species and 10% of individuals represented species typical of forest edges and clearings and 16% of species and 11% of individuals represented species typical of field margins (table 1). The majority of diurnal moths belonged to either the Geometroidea (28 species / 4,134 individuals) or Noctuoidea (20 / 1,692) and 45% of species were typical of meadows, representing 94% of all moth individuals recorded (table 1).

The mid–summer mown verges had a significantly lower number of butterfly and diurnal moth species, lower butterfly abundance and lower diurnal moth diversity than the partially mown verges (table 2). In addition, the butterfly abundance of the mid–summer mown verges was lower than the late–summer mown verges. No differences were observed between the late–summer and partially mown verges. During the peak flight season of both butterflies (weeks 27–32) (figs. 2A, 2B) and diurnal moths (weeks 25–31) (figs. 3A, 3B), the weekly averages of species richness and abundance in the mid–summer mown verge were lower than the other mowing regimes. In contrast to butterflies, the partial mowing resulted in a lower abundance of diurnal moths than the late–summer mown verges during weeks 26–29. At the end of the study season (week 35), the mid–summer mown sites attracted most species and individuals.

The proportion of meadow butterflies was lower (73% of all butterfly individuals) and the proportion of butterflies typical to field margins was higher (19%) in the mid–summer mown verges as compared to both the late–summer mown verges (83% vs. 8%) and the partially–mown verges (78% vs.

10%). MRPP indicated an overall significant difference in the species’ composition of the three mowing regimes in both butterflies (P < 0.001) and diurnal moths (P < 0.001). The butterfly assemblages also differed between the three years (p = 0.031), but such a difference was not found for the diurnal moths (p = 0.076). Indicator species analysis found ten significant (P < 0.05) indicators, comprising four butterfly species and six diurnal moth species (table 1).

Mid–summer mown sites were preferred by only one species (the Small Tortoiseshell butterfly Nymphalis urticae), late–summer mown sites by three and partially–mown sites by six indicator species.

There were no significant differences between the three mowing regimes in respect to the physical

environment or the surrounding environment type (table 3). A total of 197 plant species were recorded along the transects, 155 species in the mid–summer mown verges, 151 species in the late–summer mown verges and 146 species in the partially– mown verges. Altogether, 37 plant species were classified as positive indicators and 39 as negative indicators of semi–natural biotopes, 31 as important host plant species, and 35 as important nectar plant species (table 4). The three mowing regimes differed significantly in terms of variables related to mowing, i.e. flower and nectar abundance and vegetation height (table 5). In all cases the mid–summer mown verges differed either from the late– summer and/or partially–mown verges.

After the Bonferroni correction, two significant correlations between the Lepidoptera numbers and environmental variables remained, these being the negative correlation between butterfly species richness and negative indicators of traditional biotopes and the positive correlation between the butterfly species richness and the cover of adjacent forests (table 6).

Discussion Lepidoptera abundance adversely affected by the mid–summer mowing Mowing in the mid–summer resulted in lower abundances of Lepidoptera as compared to the other mowing regimes during the peak flight period, confirming earlier studies (Munguira & Thomas, 1992; Feber et al., 1996; Gerell, 1997). Contrary to the first hypothesis, however, only the total abundance of butterflies was significantly lower in the mid–summer mown verges than in the late– summer mown verges. According to differences in environmental variables, the decline in butterfly abundance was mainly a result of factors that are directly dependent on the mowing: the decrease in nectar (Erhardt, 1985; Gerell, 1997) and breakdown of the vegetation structure (Erhardt, 1985).

The latter may lead to conversion of host plants unsuitable for egg–laying at a time when the majority of individuals reach their adult stage. In his study, Gerell (1997) observed the majority of butterflies on the wing in the mown road verge, indicating a lack of food resources. Nectar, in particular, influences the microdistribution of butterflies in their habitat (Loertscher et al., 1995) and increases their longevity and fecundity (Murphy et al., 1983). However, some butterfly species tend to return to mown sites to lay their eggs and may even benefit from the young regrowth (Erhardt, 1985; Pullin, 1987; Kuras et al., 2001). Since mid– summer mowing postpones flowering, these verges attract butterflies at the end of August, when the vegetation in the surrounding environment is already withering. Many of the attracted species overwinter as adults and then gather energy in the form of nectar during autumn.

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138

Table 1. Butterfly and diurnal moth species and their abundance in the three mowing groups: T. Total abundance; M. Mid summer group; L. Late summer group; P. Partially mown group; I. Significant indicator according to the indicator species analysis. Preferred habitat type: a Meadows; b forest edges and clearings; c Field margins. The classification of butterflies mainly following Pitkänen et al.

(2001) and diurnal moths by Kuussaari et al. (2003).

Tabla 1. Especies de mariposas y polillas diurnas y su abundancia en los tres grupos de siega: T. Abundancia total; M. Grupo de mediados de verano; L. Grupo de finales de verano; P. Grupo de siega parcial; I. Indicador de significación según el análisis de la especie indicadora. Tipo de hábitat preferido: a Praderas; b Lindes y claros del bosque; c Márgenes de los campos. La clasificación de las mariposas se ha basado principalmente en la de Pitkänen et al. (2001) y la de las polillas diurnas en la de Kuussaari et al. (2003)

T

M

L

P I

T

M

L P

I

Butterflies a

Aphantopus hyperantus a

Thymelicus lineola

1,563 416 523 624 a

Coenonympha glycerion Pieris napi

1,861 247 771 843 P 343

c

Polyommatus amandus

a

b

Gonepteryx rhamni Nymphalis urticae

b

Ochlodes sylvanus

a

Polyommatus semiargus Brenthis ino

a

Boloria selene

a

c

Nymphalis io

Polyommatus icarus

a

Lycaena virgaureae

a

Coenonympha pamphilus Pieris rapae

50 116 109

c

a

Lasiommata maera Plebeius argus Melitaea athalia

b b

Lycaena hippothoe Aporia crataegi Aricia eumedon

a

Lycaena phlaeas

a

5 L

Boloria euphrosyne

11

1

3

7

Nymphalis c–album

b

10

2

7

1

8

3

5

0

Euphydryas maturna

b

8

1

0

7

Glaucopsyche alexis

a

7

0

4

3

7

0

4

3

7

1

5

1

7

1

4

2

6

1

2

3

5

0

1

4

4

1

1

2

4

0

2

2

62 M

Vanessa cardui

76

Plebeius idas

35

a

Aricia artaxerxes

17

c

b b

181

53

84

44

Callophrys rubi

146

16

64

66

Albulina optilete a

136

16

51

69

Pyrgus malvae

113

13

64

36

Anthocharis cardamines

24 5

31 27

33 47

Argynnis paphia

Carterocephalus silvicola

67

11

19

37

Leptidea sinapis

64

6

13

45

Cupido argiades

c

41

20 20

10 4

11 17

Nymphalis antiopa

2

4

1

0

3

3

1

0

2 1

Thecla betulae

2

0

2

0

2

0

0

2

2

0

1

1

1

0

0

1

1

0

1

0

1

0

1

0

1

0

1

0

4

0

3

1

4

0

0

4

10

16

Argynnis niobe

1

18

11

Limenitis populi

b

13

2

0

13

2

0

1

30

19

4

2

39

8

b

b

b a

2

b

b

b

28

b

0 11

75

29 a

44 165 P

16 b

186

41 b

27

95 135

b

222 143

79

a

Argynnis adippe

75

275

88

a

Argynnis aglaja

305 236

c

73 148 122

Erebia ligea

Pyrgus alveus

a

13

Celastrina argiolus c

24

9

7

8

Vanessa atalanta

18

2

7

9

Pieris brassicae

17

6

2

9

b

c

Diurnal moths Scotopteryx chenopodiata Euclidia glyphica

a

Scopula immorata

a

a

Cryptocala chardinyi

2,861 8641245 752

Cabera exanthemata

1,159 249 585 325 L

Aplocera praeformata

496

Polypogon tentacularius Siona lineata

a

a

a

97 139 260 P

Parasemia plantaginis

a

4

1

1

2

a

184

27

48 109 P

Chersotis cuprea

4

1

0

3

183

34

55

94

Macaria brunneata

3

0

1

2

174

10 101

63

Angerona prunaria

3

0

1

2

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Animal Biodiversity and Conservation 29.2 (2006)

Table 1. (Cont.)

a

Odezia atrata

Xanthorhoe montanata Idaea serpentata

a

Cerapteryx graminis Callistege mi

a

a a

Chiasmia clathrata Ematurga atomaria Diacrisia sannio Scopula immutata

a

Camptogramma bilineata

a

T

M

L

113

14

62

37

Autographa bractea

106

36

15

55

Hyles gallii

97

19

44

80

58

48

1

46 42

P I a a

T

M

L P

3

2

1

0

2

1

0

1

2

0

0

2

2

0

1

1

2

0

0

2

34

Timandra griseata

17

5

Eupithecia satyrata

19

28

Adscita statices

20

7

19

Caradrina morpheus

2

2

0

0

9

18

15

Protodeltode pygarga

2

0

0

2

2

0

0

2

2

0

1

1

a

a

41

5

15

21

Rivula sericealis

31

1

17

13

Panemeria tenebrata

26

5

12

9

Aglia tau

1

0

0

1

a

Scopula ternata

21

2

15

4 L

Idaea emarginata

1

0

0

1

Rheumaptera hastata

20

13

4

3

Jodis putata

1

0

1

0

19

7

5

7

Rheumaptera undulata

1

0

1

0

Lomaspilis marginata

19

2

11

6

Chlorissa viridata

1

0

0

1

Eilema lutarellum

18

0

5

Spilosoma lubricipedum

1

1

0

0

Autographa gamma

17

4

5

8

Orgyia antiqua

1

1

0

0

14

2

8

4

Deltode candidula

1

0

1

0

12

0

6

6

Diachrysia chrysitis

1

1

0

0

Cybosia mesomella

9

0

2

7 P

Mythimna conigera

1

0

0

1

Cabera pusaria

9

2

2

5

Mythimna ferrago

1

0

1

0

8

1

1

6

Plusia festucae

1

0

0

1

6

4

1

1

Leucania impura

1

0

1

0

1

0

0

1

Epirrhoe alternata

a

Zygaena viciae Idaea pallidata

a

a

Colobochyla salicalis Lythria cruentaria Epirrhoe tristata

a

a

5

0

3

Besides altering the habitat characteristics of importance to adults, mowing may also destroy eggs, larvae and pupae (Courtney & Duggan, 1983; Erhardt, 1985; Feber et al., 1996). The mowing of road verges in mid–June, for example, caused complete destruction of the Orange Tip butterfly Anthocharis cardamines larvae during their third instar (Courtney & Duggan, 1983). In contrast, many larvae of the Karner Blue butterfly Lycaeides melissa samuelis were found on sites (including road verges) mown since or during the previous adult flight period, suggesting that not all butterflies or their earlier stages are vulnerable to occasional or annual mowing (Swengel, 1995). Since Lepidoptera species differ in their life cycles, there is no single time when mowing could be conducted without harming the early stages of some species. However, late summer mowing is suggested to best suit the life cycles of most invertebrates (Anderson, 1995),but more research on this matter is needed. Even if mowing destroys a large proportion of eggs, larvae and pupae, individuals

13 P

2

Lygephila pastinum

a

I

may arrive in the verges from the surrounding environment after the regeneration of vegetation.

Consequently, the presence of adult stages does not necessarily indicate the suitability of the area for breeding. Furthermore, different life stages may need different elements, thus requiring them to travel between patches (Dunning et al., 1992).

This phenomenon is also recognized in butterflies (Ouin et al., 2004). In this study, the Brimstone butterfly Gonepteryx rhamni was observed in large numbers nectaring on road verges both in early spring and in late summer, while its host plant Rhamnus frangula grows only in forests.

The species richness of both butterflies and diurnal moths declined after the mid–summer mowing, a finding that is in keeping with the results of Feber et al. (1996). However, the differences in total butterfly species richness and diversity between the mid–summer and late–summer mown verges were small compared to the differences in abundance, suggesting that the decline concerned both abundant and rare spe-

Valtonen et al.

140

A

Butterfly species richness

6

4

2

Msm Lsm Pm 23

B

24

25

26

27

28

29 30

31

32

33

34

35

25

Butterfly abundance

20

15

10

5 Msm Lsm Pm 23

24 25

26

27

28 29 Week

30

31

32

33

34

35

Fig. 2. Weekly averages of butterfly species richness (A) and abundance (B). (For abbreviations see fig. 1.)

Fig. 2. Promedios semanales de la riqueza de especies de mariposas (A) y de su abundancia (B).

(Para las abreviaturas ver la fig. 1.)

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Animal Biodiversity and Conservation 29.2 (2006)

A

Diurnal moth species richness

6

4

2

Msm Lsm Pm 23

B

24

25 26

27 28

29

30

31 32

33

34

35

25

Diurnal moth abundance

20

15

10

5

Msm Lsm Pm 23

24

25

26

27

28 29 Week

30

31

32

33

34

35

Fig. 3. Weekly averages of diurnal moth species richness (A) and abundance (B). (For abbreviations see fig. 1.)

Fig. 3. Promedios semanales de la riqueza de especies (A) y de la abundancia (B) de las polillas diurnas. (Para las abreviaturas ver la fig. 1.)

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142

Table 2. Differences in the Lepidoptera communities between the three management regimes.

Differences were tested by mixed–effects ANOVA and pair–wise comparisons by the Tukey–Kramer method: * 0.05 > P > 0.01; *** P < 0.001, significant differences after sequential Bonferroni correction are marked with S. Regimes with significant differences in pair–wise comparisons are indicated by separate letter a and b. (For other abbreviations see fig. 1.)

Tabla 2. Diferencias en las comunidades de lepidópteros entre los tres regímenes de gestión. Las diferencias se comprobaron mediante un ANOVA de efectos mixtos, y las comparaciones apareadas mediante el método de Turkey–Kramer: * 0,05 > P > 0,01, *** P < 0,001; las diferencias significativas tras el ajuste secuencial de Bonferroni se indican mediante una S. Los regímenes con diferencias significativas en las comparaciones apareadas se indican mediante las letras separadas a y b. (Para otras abreviaturas ver fig. 1.)

Msm

Lsm

Pm

Total

Mean

Std.

Total

Mean

Std.

Total

Mean

Std.

Species richness*S

36

12.4a

3.9

43

15.2ab

5.8

44

16.3b

5.4

Diversity (H’)

–

1.8

0.5

–

1.9

0.4

–

1.9

0.4

Butterfy

Abundance***S

1,299 72.2a 30.7

2,278

126.6b 69.4

2,678 148.8b 60.4

Diurnal moth Species richness*S S

Diversity (H’)* Abundance

33

9.2a a

–

1.3

1,496

83.1

2.5

41

0.4

–

48.3

2,481

cies. The correlations indicate that factors not directly associated with mowing, such as the surrounding environment type (Gerell, 1997; Pywell et al., 2004) and the site history, have a stronger influence on species richness than mowing. Forest edges, in particular, offer shelter to butterflies and have a diversifying influence on road verge butterfly fauna (Gerell, 1997). On the other hand, the abundance of negative plant indicators, was adversely associated with butterfly species richness and may indicate both recent disturbance to the soil and high amounts of nutrients in the soil, possibly caused by imported top soil typical on road verges.

Differences in the species’ composition between the mid–summer and late–summer mown verges suggest that the butterflies typical of field margins were relatively more abundant in the nectar–poor mid–summer mown verges. A closer examination of butterfly data during the week following the mowing event, however, indicated the predominance of meadow species in the verges. An alternative explanation may be that some abundant field margin species, such as the Peacock butterfly Nymphalis io and Nymphalis urticae, fly only in the spring and in the late summer and thus the adult stage avoids the adverse effect of mid– summer mowing. In urban areas in Canada both frequent and infrequent mowing events changed the structure and composition of butterfly assemblages such that only some disturbance–adapt-

11.9ab 1.5

ab

137.8

3.8 0.4 67.7

48 –

14.3b 1.7

b

1,942 107.9

4.6 0.3 43.6

able species returned to the mown sites (Hogsden & Hutchinson, 2004).

In contrast to butterflies, the absolute numbers of diurnal moths decreased after the mid–summer mowing but increased again after the vegetation regenerated towards the peak flight period. As a result, no significant differences resulted between the mid– and late–summer mown verges in total species richness, diversity or abundance. These trends reflect the differences between the ecology of two Lepidoptera groups.

The high vegetation seems to be particularly important for the diurnal moths, many of which seek hiding or resting places during the day (Saarinen et al., 2005). The recorded diurnal moths form a continuum of species flying solely during the day to species, which fly mostly as a result of being disturbed and are more active at night. The number of individuals decreased after mowing, because hiding places are scarce in low vegetation. Furthermore, diurnal moth individuals searching new resources or habitats are observed in lower numbers during day censuses in comparison to butterflies. Later in the summer the regrowth of vegetation offers an increasing number of hiding places for diurnal moths, while for flowers important to most butterflies and only some diurnal moths it takes a longer time to regenerate. It is noteworthy, however, that the transect method conducted in tall vegetation may underestimate the numbers of diurnal moths hiding. This concerns especially large–bodied species which need longer to warm up,

143

Animal Biodiversity and Conservation 29.2 (2006)

Table 3. Differences in the physical and surrounding environment between the three management regimes tested by Kruskal–Wallis. Values given to study areas or averages within each study area are used (mid summer mown verges n = 11, late summer mown verges n = 10, partially mown verges n = 12). (For abbreviations see fig. 1.)

Tabla 3. Diferencias en el medio físico y circundante entre los tres regímenes de gestión analizadas por medio del test de Kruskal–Wallis. Se utilizan los valores dados a las áreas de estudio o los promedios dentro de cada área de estudio (márgenes segados a mediados de verano n = 11, márgenes segados a finales de verano n = 10, márgenes parcialmente segados n = 12). (Para las abreviaturas ver la fig. 1.)

Msm

Lsm

Pm

Mean

Std.

Mean

Std.

13.2

8.6

13.2

6.8

Mean Std.

Physical environment (%): Road width Traffic speed (100/80/60/50 km/h)

2/4/4/1

Traffic density (0/1/2/3/4)

0/0/4/3/4

Verge width Verge age

10.3

6.5

2/1/5/2

2/4/4/2

0/1/5/1/3

0/2/2/2/5

8.2

3.7

6.9

1.7

6.0

2.0

20.7

8.1

19.1

9.5

23.3

5.8

Soil moisture (1/2/3)

1/6/4

1/7/2

3/7/2

Surrounding environment (%): Cultivated fields

17.9

21.6

17.5

20.8

32.3 34.8

Non–cultivated open

39.6

31.0

37.7

28.6

30.1 33.2

Forest

42.5

34.2

44.8

32.3

37.6 35.5

and individuals that are not on the top–layer of the vegetation or are located further from the counter, thus being less sensitive to any disturbance.

Partial mowing is most beneficial for road verge Lepidoptera The second hypothesis was confirmed only partly, since the partially mown verges had a higher species richness, diurnal moth diversity and butterfly abundance than the two regimes with total mowing, but the differences were significant only compared to the mid–summer mown verges. Based on these results, both the late–summer and the partial–mowing regime can be recommended in road verge management. The lower species richness and abundance, but similar diversity of butterflies in mid–summer mown verges compared to partially–mown verges suggests that the abundant species, in particular, were decreased. On the other hand, the lower species richness and diversity, but similar abundance of diurnal moths suggests that the rare species in particular have suffered from total mowing in mid– summer.

The high Lepidoptera species richness, diversity and abundance in the partially–mown verges is explained by the lowest mowing intensity. A time span of approximately three years since the last total mowing on some partially–mown verges allows com-

munities to recover from the disturbance. The partial mowing leaves untouched resources such as nectar, host plants and hiding places for adults throughout the flying season. In addition, mowing postpones the flowering and the mown part of the verge provides nectar later in the summer. However, the latter impact is likely to be small due to the low number of species and individuals in the late summer. The partial mowing also destroys fewer Lepidoptera offspring than the total mowing and leaves untouched resources in the vicinity for the larvae surviving from the mowing, if they are capable of moving on to a new host plant.

The partial mowing resembles the mosaic–like mowing regime, since it increases variety in mowing intensity and timing on different parts of the verge.

The mosaic–like mowing is often suggested as benefiting Lepidoptera (Munguira & Thomas, 1992) and other invertebrates (Morris & Rispin, 1988; Bakker, 1989; Völkl et al., 1993). In the traditional mowing and grazing management, some areas such as the edges and areas around stones, trees and bushes may have remained undamaged more or less regularly, thereby serving as untouched areas for species sensitive to mowing. On the other hand, the low vegetation next to the road, created by the partial– mowing regime, can offer different resources and conditions compared to the taller vegetation further from the road.

Valtonen et al.

144

Table 4. Plant species status: positive (Po) and negative (Ne) indicator species of semi–natural biotopes, host plant (H) and good nectar plant (N) species.

Tabla 4. Estatus de las especies vegetales: especies indicadoras positivas (Po) y negativas (Ne) de biotopos semi–naturales, especies de plantas huésped (H) y de plantas buenas suministradoras de néctar (N).

Species Achillea millefolium

Status N

Species

Status

Erigeron acer

Po

Achillea ptarmica

Ne

Erysimum cheiranthoides

Ne

Aegopodium podagraria

Ne

Festuca pratensis

Ne

Filipendula ulmaria

H

Alopecurus pratensis Angelica sylvestris Antennaria dioica

Ne, H N Po, N

Fragaria vesca

H, N

Galeopsis bifida

Ne

H

Galium album

Ne

Anthriscus sylvestris

Ne

Galium verum

Po

Arctium tomentosum

Ne

Geranium palustre

Po

Arctostaphylos uva–ursi

Po

Geranium sylvaticum

Artemisia campestris

Po

Gnaphalium uliginosum

Ne

Artemisia vulgaris

Ne

Heracleum sibiricum

Po

Barbarea vulgaris

H, N

Anthoxanthum odoratum

Hieracium sp.

H, N

N

Bistorta vivipara

Po

Hieracium umbellatum

N

Botrychium lunaria

Po

Hypericum perforatum

Po

H

Hypochoeris maculata

Po

Po, H, N

Juncus conglomeratus

Ne

Calamagrostis epigejos Calluna vulgaris Campanula glomerata

Po

Knautia arvensis

Capsella bursa–pastoris

Ne

Lathyrus pratensis

H, N

Po

Lathyrus sylvestris

Po, N

Cardamine pratensis Carduus crispus

Ne, N

Leontodon autumnalis

N

N

Carex ericetorum

Po

Centaurea jacea

N

Leucanthemum vulgare

Centaurea phrygia

N

Linaria vulgaris

Ne

Lotus corniculatus

Po

Luzula pilosa

Po

Centaurea scabiosa Chenopodium album Cirsium arvense

Po, N Ne Ne, N

Leontodon hispidus

Lychnis viscaria

Po, N N

Po, N

Cirsium helenioides

N

Maianthemum bifolium

Po

Cirsium oleracea

N

Matricaria matricarioides

Ne

Cirsium palustre

N

Melampyrum pratense

Cirsium vulgare

N

Myosotis arvensis

Ne

Dactylis glomerata

H

Myosotis stricta

Po

Deschampsia cespitosa

H

Persicaria lapathifolia

Ne

Deschampsia flexuosa Dianthus deltoides Elymus repens

Po, H Po Ne, H

H

Phleum pratense

H

Picris hieracioides

Po

Plantago lanceolata

Po

Epilobium adenocaulon

Ne

Plantago major

Ne

Epilobium angustifolium

Ne

Poa annua

Ne

145

Animal Biodiversity and Conservation 29.2 (2006)

Table 4. (Cont.)

Species

Species

Status

Poa pratensis Polygonum aviculare Potentilla anserina

H

Trifolium arvense

Po

Ne

Trifolium aureum

Po

Ne, H

Ranunculus polyanthemos

Status

Trifolium hybridum

Ne, H, N

Po

Trifolium medium

H, N

Rumex acetosa

H

Trifolium pratense

H, N

Rumex acetosella

H

Trifolium spadiceum

Po

Rumex crispus

Ne, H

Tripleurospermum inodorum

Ne

Rumex longifolius

Ne, H

Tussilago farfara

Ne

Selinum carvifolia

Po

Solidago virgaurea

Urtica dioica

N

Sonchus arvensis

Ne, N

Spergula arvensis

Ne

Ne, H

Vaccinium vitis–idaea

Po

Verbascum nigrum

Po

Veronica chamaedrys

H

Succisa pratensis

Po, N

Vicia cracca

H, N

Tanacetum vulgare

Ne, N

Viola canina

H

Taraxacum sp.

Ne, N

Viola palustris

H

Ne

Viola riviniana

Thlaspi caerulescens Thymus serpyllum

Po, N

Tragopogon pratensis

H

Viola tricolor

Po, H

Ne

Table 5. Differences in the vegetation variables between the three mowing regimes: ** 0.01 > P > 0.001, *** P < 0.001; significant differences after sequential Bonferroni correction are marked with S; regimes with significant differences in pair–wise comparisons are indicated by separate letter a and b. (For other abbreviations see fig. 1.)

Tabla 5. Diferencias en las variables de vegetación entre los tres regimenes de siega: ** 0,01 > P > 0,001, *** P > 0,001, las diferencias signifiativas tras la corrección secuencial de Bonferroni se indican mediante una S. Los regímenes con diferencias significativas en las comparaciones pair–wise se indican mediante las letras separadas a y b. (Para otras abreviaturas ver la fig. 1.)

Msm Plant species richness

Lsm

Pm

Mean

Std.

Mean

Std.

Mean

Std.

51.9

9.4

53.1

14.74

59.1

11.9

Positive indicator abundance

3.6

4.3

3.3

3.6

4.7

4.5

Negative indicator abundance

27.2

5.4

24.9

5.8

24.4

5.9

Host plant abundance

23.1

3.4

23.8

6.7

25.4

6.0

Flowering plant abundance**S

49.2a

15.0

65.4ab

20.5

78.9b

19.8

Nectar plant abundance***S

22.6a

7.1

34.4b

7.1

36.1b

8.3

5.9

b

13.8

b

15.6

Vegetation height**

S

25.2

a

40.6

38.3

Valtonen et al.

146

Table 6. Correlations between the Lepidoptera numbers and environmental variables of each site: * 0.05 > P > 0.01, ** 0.01 > P > 0.001; significant correlation after sequential Bonferroni correction is marked with S. Tabla 6. Correlaciones entre el número de lepidópteros y las variables ambientales de cada lugar: * 0,05 > P > 0,01, ** 0,01 > P > 0,001; las correlaciones significativas tras la corrección secuencial de Bonferroni se indican mediante una S. Species richness Butterflies

Butterflies

Diurnal moths

Road width

0.218

–0.222

0.070

0.199

Traffic speed

0.070

–0.254

0.101

–0.158

Traffic density

Diurnal moths

Abundance

0.029

–0.296

0.001

–0.197

Verge width

0.442**

–0.024

0.120

0.328

Verge age

–0.091

0.007

–0.112

–0.084

Soil moisture

–0.190

0.051

0.007

0.070

Plant species richness

0.155

0.333

0.050

–0.041

Positive plant indicators

0.305

0.149

0.083

0.026

S

–0.027

–0.285

–0.392*

Host plants

0.123

0.282

0.134

0.139

Flowering plants

0.096

0.334

0.322

0.028

Nectar plants

0.218

0.380*

0.482**

0.190

Vegetation height

0.085

0.400*

0.457**

0.254

Open uncultivated

–0.290

–0.285

0.045

–0.242

–0.436**

–0.108

–0.122

–0.180

S

0.200

0.057

0.303

Negative plant indicators

Open cultivated Forest

–0.538**

0.525**

Possibilities in road verge management – a case study on Finnish roads Regular mowing as required on road verges is expensive. In Finland verge management accounts for 12% of all road management costs (Finnra, 2000) and the annual costs of mowing are approximately 6 million euros (H. Lappalainen, pers. comm.). Thus, lowering the mowing intensity may lead to substantial savings in money and energy. We have made a rough estimation of the potential area of road verges in Finland where the mowing intensity could be lowered without any threat to traffic safety. The estimation is based on the "Road Register" by the Finnish Road Administration (Finnra). It includes data on the length of public roads belonging to different management classes and guidelines for mowing management in particular classes (Finnra, 2000). If special management classes and 15% of roads for which the management data are missing are omitted, the area of annual mowings along public roads covers about 46,000 ha. Using our recommendations, i.e. that mid–summer mowing be replaced with a narrow (2 m) partial mowing, while verges are fully mown in the late summer only, the

area of annual mowings would decrease to 39,500 ha.

In other words, a 14% reduction in the annually mown area is achieved. This is most likely an underestimate, because the minimum observed verge widths for each management class were used and 15% of public roads for which the management class information was missing potentially make a further contribution to the reduction in the mown area. Changes in management practices for promoting biodiversity usually increase the costs, but this is not necessarily so in road verge management, as demonstrated above.

Conclusions New methods, ideas and areas should be used to stop the ongoing decline in the biodiversity of European agricultural environments. In northern and central Europe road verges offer a large potential for restorative management and could serve as refuges or alternative habitats for species of semi–natural grasslands (Ouin & Burel, 2002). The majority of Lepidoptera individuals in this study represented meadow species. Factors influencing the quality of

Animal Biodiversity and Conservation 29.2 (2006)

road verges as alternative habitats, such as the soil, verge width and topography, can be influenced only in the construction phase. Mowing management, on the other hand, is a factor that can also be readily modified in old road verges. According to our results, lowering the mowing intensity (partial mowing) or delaying the mowing to late summer may have a positive effect on Lepidoptera along road verges without increasing costs or jeopardizing traffic safety.

As Lepidoptera are a sensitive indicator group of the invertebrate fauna, other insects are likely to benefit as well.

Acknowledgements We thank Leigh Plester for the English revision, the referees for providing valuable comments and suggestions, and Raija Merivirta, Heikki Lappalainen and Matti Raekallio from the Finnish Road Administration. Financial support from the Science Faculty of the University of Joensuu, Maj & Tor Nessling Foundation, The Finnish Cultural Foundation’s South Karelia regional fund, the Finnish Road Administration, and Finland’s Ministry of the Environment are gratefully acknowledged.

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Warren, M. S., 1985. The influence of shade on butterfly numbers in woodland rides, with special reference to the Wood White Leptidea sinapis.

Biological Conservation, 33: 147–164.

Zimmerman G. M., Goetz, H. & Mielke P. W., Jr., 1985. Use of an improved statistical method for group comparisons to study effects of prairie fire.

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Animal Biodiversity and Conservation 29.2 (2006)

149

Parataxonomy: a test case using beetles C. G. Majka & S. Bondrup–Nielsen

Majka, C. G. & Bondrup–Nielsen, S., 2006. Parataxonomy: a test case using beetles. Animal Biodiversity and Conservation, 29.2: 149–156.

Abstract Parataxonomy: a test case using beetles.— The present study examines the utility of parataxonomic sorting (groupings of similar individuals, categorized by non–experts, relying on features of external morphology) using data from a study of beetle communities in four forest habitats in Nova Scotia, Canada. Alpha diversity and the Shannon–Weaver, Simpson, Berger–Parker, and Brillouin indices of diversity, derived from both taxonomic species and parataxonomic units, are compared and yield identical habitat rankings. Beta diversity rankings derived from both data sets do not differ although they produce slightly different rankings. The Elateridae, Curculionidae, Cantharidae, and Staphylinidae had particularly large numbers of "lumping" and "splitting" errors. Although the overall gross sorting error was only 14%, individual families of beetles had errors between 0% and 200% with an average error of 38%. The limitations of the parataxonomic approach are discussed; both in regard to the practical application of the concept, as well its theoretical basis. We note the spillover of this discourse to the subject of what constitutes a species and observe that this discussion has been misplaced due to the unfortunate confusion of the two usages of the term "morphospecies".

Key words: Parataxonomy, Morphospecies, Beetles, Biodiversity, Conservation, Ecological management.

Resumen Parataxonomía: un test utilizando escarabajos.— El presente estudio examina la utilidad de la ordenación parataxonómica (agrupación de individuos similares, categorizados por aficionados, basada en caracteres morfológicos externos) usando los datos de un estudio de comunidades de escarabajos de cuatro hábitats forestales de Nueva Escocia, Canadá. Se comparan la diversidad alfa y los índices de diversidad de Shannon–Weaver, Simpson, Berger–Parker y Brillouin, obtenidos tanto de especies taxonómicas como de unidades parataxonómicas, dando como resultado rankings de hábitats idénticos. Los rankings de diversidad beta procedentes de ambas series de datos no se diferencian, aunque arrojan rankings ligeramente distintos. Los Elateridae, Curculionidae, Cantharidae y Staphylinidae presentaban gran cantidad de errores de "agrupación" y "escisión". Aunque el error de clasificación bruto global era tan solo del 14%, algunas familias de escarabajos presentaban errores de entre el 0 y el 200%, con un error medio del 38%. Se discuten las limitaciones del planteamiento parataxonómico; tanto en lo que hace referencia a la aplicación práctica del concepto, como a su base teórica. Esta discusión nos lleva al tema de en qué consiste una especie y nos permite ver como esta discusión ha sido mal enfocada debido a la desafortunada confusión de los dos usos del término "morfoespecie".

Palabras clave: Parataxonomía, Morfoespecies, Escarabajos, Biodiversidad, Conservación, Gestión ecológica.

(Received: 25 VIII 05; Conditional acceptance: 10 VI 06; Final acceptance: 10 VII 06) Christopher G. Majka, Nova Scotia Museum of Natural History, 1747 Summer St., Halifax, Nova Scotia, Canada, B3H 3L6.– Søren Bondrup–Nielsen, Dept of Biology, Acadia Univ., Wolfville, Nova Scotia, Canada, B4P 2R6.

Corresponding author: C. G. Majka. E–mail: c.majka@ns.sympatico.ca ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

150

Introduction The utility of invertebrates in environmental monitoring has often been limited by two factors: 1) many invertebrate groups are very species rich and (often) inadequately known taxonomically; and 2) limited pools of taxonomic expertise exist and the learning curves to acquire such expertise can be protracted. Hence a procedure to streamline the collection of useful data in such a way as to produce repeatable results would be a desirable goal.

With this in mind Oliver & Beattie (1993, 1996a, 1996b) proposed the concept of "morphospecies" (groupings of similar individuals, categorized by non– experts, relying on features of external morphology) as a tool to rapidly classify invertebrates in the context of environmental monitoring and conservation evaluation. Oliver and Beattie’s work was followed by Pik et al. (1999), Derraik et al. (2002), Barratt et al. (2003), and other empirical studies.

Krell (2004) subsequently pointed out that the term "morphospecies" is properly preoccupied by a term widely used in evolutionary biology and introduced

by Cain (1954). He proposed that parataxonomic unit (PU) be employed instead, a terminology which we follow in the remainder of this paper.

If this approach is validated it could provide a potentially useful technique since invertebrates can have significant utility in environmental monitoring (Rosenberg et al., 1986; Erhardt & Thomas, 1991; Kremen et al., 1993). Invertebrates are widespread, numerous, species–rich, and easily sampled. They exhibit greater site specificity than vertebrates, and often respond to environmental changes more rapidly than vascular plants or vertebrates (Oliver & Beattie, 1996a). Beetles (Coleoptera) are particularly well–suited for such purposes since in addition to being hyperdiverse and relatively easily sampled, they also include representatives of many free–living trophic guilds. If competitive exclusion as proposed by Hardin (1960) is correct, then measuring alpha diversity is indicative of the presence or absence of microhabitats occupied by each of the invertebrate species. Hence examining species richness, particularly of extremely diverse groups such as beetles, allows for an examination of at least some dimensions of the environment as seen through a very fine ecological mesh. Of course, indices of diversity are by their very nature radical simplifications. Much important ecological information, of significant potential interest in management or conservation contexts, is not conveyed by such simple measures and they should not serve as substitutes for detailed species —and population— based data that can ground management decisions in biological reality. They do, however, have utility in comparing similar sites and in monitoring changes at a site over time.

Parataxonomy has, nevertheless, proved to be a contentious and problematic approach. It has been subjected to a wide range of serious questions with respect to its theoretical soundness, how (or even if) such information one can be properly applied

Majka & Bondrup–Nielsen

and interpreted, and to what groups it might be applicable (Goldstein 1997, 1999a, 1999b; Brower, 1995). Krell (2004) surveyed a series of studies that evaluated the parataxonomic approach and offered a comprehensive theoretical examination of the concept. He showed that parataxonomic sorting errors depend not only on the taxonomic group in question, but also on the sorter and the sample, leading him to conclude that sorting error is itself not predictable. Furthermore, philosophical and theoretical considerations indicate that parataxonomy does not fulfill the criteria of a scientific method.

Such empirical and theoretical considerations lead him to exclude parataxonomy from a large spectrum of potential uses noting, however, that it is propedeutic and can be a heuristically valuable tool for determining patterns in taxonomically neglected groups. Consequently, Krell (2004) argued that PUs provide limited, but adequately accurate, data for: a) global comparisons of gross species richness; and b) non–comparative descriptions of species richness of single sites or comparisons of species numbers of different habitats within one area without considering species overlap.

The present study further investigates the parataxonomic approach in the context of the latter area, employing a set of Coleoptera data from the temperate, Nearctic region. Kehler et al. (1996, 2004) conducted a study of forest beetles caught in flight–intercept traps in four different forested habitats in Nova Scotia, Canada. The specimens were sorted into PUs (called "morphospecies" by the sorters) by non–experts roughly in accordance with the protocols of Oliver & Beattie (1993). Since that time, much of the collection has been donated to the Nova Scotia Museum and the first author (with the assistance of other experts in Coleoptera taxonomy) has completed the taxonomic determination of the specimens. Thus, it is now possible to assess the accuracy of the original PU data set.

Material and methods Coleoptera sampling took place in central Nova Scotia within an area 300 km long by up to 100 km wide (Kehler et al., 1996, 2004). Sampling was conducted in both 1994 and 1995, although only the 1995 data are considered in this paper. In 1995, 10 softwood and 10 hardwood stands were sampled. Four forest categories were distinguished; old softwood (OSW), young softwood (YSW), old hardwood (OHW), and young hardwood (YHW).

Softwood stands were defined as having more than 70% coniferous trees [principally red spruce (Picea rubens Sarg.) and balsam fir (Abies balsamea L.) Mill (Pinaceae)]. Hardwood stands were defined as having more than 70% deciduous trees [principally sugar maple (Acer saccharum Marsh.), red maple (Acer rubrum L.) (Aceraceae), yellow birch (Betula alleghaniensis Britt.) and white birch (Betula papyrifera Marshall) (Betulaceae)]. All stands were greater than 2.5 hectares, and were at least 300 m

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from any road. Sampling for beetles was carried out at distances at least 50 m from the stand boundary. Window flight–intercept traps were used to sample for beetles.

Sorting and classification was carried out on the basis of external morphology by individuals without particular knowledge or expertise in Coleoptera (as per the protocols of Oliver & Beattie, 1996a). While some effort was made at the time to attach Latin binomials to some of these "morphospecies" (Kehler et al., 1996) subsequent analysis (Kehler et al., 2004) treated them as PUs (apparently due to oversight, Kehler et al., 1996, 2004) neglected to include specimens of Byturus unicolor Say (Byturidae) in their analysis. Since this species was abundant in many of the OHW and YHW stands, their inclusion in the calculations of diversity indices affects diversities in these two stand types.

Unfortunately some of these specimens were not preserved hence it was not possible after the fact to exactly determine the exact number collected. Consequently this species was excluded from the calculations to allow for comparisons of taxonomic species to PUs). Subsequently the first author examined the extant material (some specimens had either been discarded, dispersed, or were unavailable for examination) and determined them to taxonomic species.

From these data the alpha diversities for each of the 20 forest stands were derived, as were average stand diversities for the four forest types.

To further examine dimensions of biotic diversity at the stand level, several indices of diversity were calculated for each stand as well as cumulatively for each forest category: 1. The Shannon–Weaver Diversity Index (Shannon & Weaver, 1949) is an information index that reflects both the equitability and evenness of a sample. It is affected by the randomness of sampling and is defined as: s

3 pi log pi

H' = –

i = 1

where pi is the proportion of the community that belongs to the ith species.

2. The Simpson Index of Diversity (Simpson, 1949), a dominance index, emphasizes the abundance of the more dominant species in a sample. It is defined as:

3 pi2

=

where pi is the proportion of the community that belongs to the ith species.

3. The Brillouin Index of Diversity (Brillouin, 1962) is a more effective measure of diversity in circumstances where the randomness of a sample cannot be guaranteed. It is defined as: ln N! –

3 ln ni!

HB = N where N is the total number of individuals and ni is the number of individuals in the ith species.

4. The Berger–Parker Index represents a different approach that is strongly influenced by the evenness of the sample. It is readily calculated as the largest species proportion of all species in a community thus: d = pMAX (œi: pMAX $ pi) where pi is the proportion of the community which belongs to the ith species, and pMAX is the largest such proportion.

The forest stands were ranked in terms of increasing taxonomic alpha diversity. This was compared to the ranking order derived from the PU data. The ratio of the diversity indices among the forest stands were compared between taxonomic species and PUs using a G–test.

5. Beta Diversity: because there were large differences between the faunal compositions of the different forest stand types (on average each stand type shared only 45% of its fauna with any other stand type) it was decided to employ Coefficient of Community (CC) (Whittaker, 1972) to measure beta diversity, recommended by Pielou (1974) as being applicable in such situations. Coefficient of Community (CC) was calculated as: 200sxy CC = sx + sy where sx is the number of species in habitat X; sy is the number of species in habitat Y; and sxy is the number of species in common to both habitats X and Y. Beta Diversity was compared using a non– parametric Mann–Whitney U test.

The correspondence ratio (accuracy) of taxonomic species to PUs, as per Oliver & Beattie (1996a) was calculated. Frequencies of lumping, splitting, and one–to–one correspondence derived in this study were compared to frequencies reported in Oliver & Beattie (1996a) and Derraik et al.

(2002). The gross sorting error (as per Krell, 2004) for each family of Coleoptera was also calculated.

Results Table 1 shows alpha, Shannon–Weaver, Simpson, Berger Parker, and Brillouin index of diversity values for all four forest composition categories. For both taxonomic species and PUs, the ranking of all categories remained invariant as (in increasing richness) YSW t OSW t OHW t YHW when calculated by all diversity measures. The only exception was the Brillouin values for OSW and OHW which, although very similar, were in reverse order. These results are noteworthy because the ratio of correspondence (accuracy) of sorting in this study is decidedly lower than in Oliver & Beattie (1996a). Figure 1 shows the frequency values of these from this study as well as, for comparison, the values from Oliver & Beattie (1996a) and Derraik et al. (2002). Categories on

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Table 1. Alpha diversity and diversity indexes: Tx. Taxonomic; PU. Parataxonomic units; SE. Standard error; YSW. Young Softwood; OHW. Old Hardwood; OSW. Old Softwood; YHW. Young Hardwood; 1 Adjusted G–test.

Tabla 1. Diversidad alfa e índices de diversidad: Tx. Taxonómico; PU. Unidades parataxonómicas; SE. Error estándar; YSW. Madera blanda joven; OHW. Madera dura vieja; OSW. Madera blanda vieja; YHW. Madera dura joven; 1 Test G ajustado.

Shannon–Weaver Tx

PU

Simpson (1/ ) Tx

Berger–Parker (1/d)

PU

Tx

PU

Brillouin Tx

PU

Alpha (mean±SE) Tx

PU

YSW

3,635 3,406

15,088 10,461

4,430 3,488

4,754 4,405

29,2±1.14 23,2±1.63

OHW

3,886 3,693

21,622 18,836

6,151 5,780

5,263 4,999

48,8±3.86 38,4±2.47

OSW

3,996 3,804

27,336 22,339

6,921 5,849

5,277 4,949

37,2±3.18 28,4±2.18

YHW

4,066 3,810

32,915 22,922

9,865 9,414

5,498 5,082

52,2±2.61 52,2±2.61

G–test1 Prob.

0,000

0,395

0,066

0,001

>> 0.05

>> 0.05

>> 0.05

>> 0.05

the x–axis to the left of "1–to–1" represent "lumping"; those to the right represent "splitting". In Oliver & Beattie (1996a), the one–to–one correspondence of taxonomic species to PUs was 80% while in Derraik et al. (2002) it was 62.8%. In this study the accuracy is 67% with roughly equal distribution tails of lumping (16.7%) and splitting (15.9%).

Four families, Elateridae, Curculionidae, Cantharidae, and Staphylinidae, accounted for 60% of the errors, and of these, the former two combined accounted for 42% (table 2). All four are species– rich families with many superficially similar members, differentiated by characters that may not be obvious to the non–expert. The number of taxonomic species and PUs for each family of Coleoptera is shown in table 3 as is the gross error of PU sorting (as per Krell, 2004). Although the overall gross error is only 15%, values for individual families range between 0% and 200% with a mean value of 38%.

Beta diversity as calculated by the Coefficient of Community (CC) method is shown in table 4. In this study the parataxonomic approach narrowly fails in producing the same ranking derived from taxonomic species. Beta diversity appeared higher using the taxonomic approach (mean (± S.E.) of 50.7 ± 3.70) versus the parataxonomic approach (mean (± S.E.) of 43.2 ± 2.42) but did not differ statistically (U = 10.0, p = 0.20). The ratio of the Beta diversities (see table 4) was not significantly different (adjusted G–test = 0.637, p << 0.05). The correlation between the two approaches based on the Beta diversity values presented in table 3 is 0.93 with a significance of 0.01. Nonetheless the results may indicate that at the 67% level of one– to–one taxonomic–to–parataxonomic correspondence (fig. 1) of the present study, beta diversity may begin to loose utility.

Discussion The results of this study indicate that the parataxonomic approach is surprisingly robust. Even at a 67% level of accuracy, the rankings of the four different types of forest stands —Young Softwood (YSW), Old Hardwood (OHW), Old Softwood (OSW), and Young Hardwood (YHW)— are preserved between taxonomic and parataxonomic approaches. This agrees with Oliver & Beattie (1996a) in which the ranking of the four habitats (dry, grassy, moist, and rain–forests), measured in terms of alpha and beta diversity, were preserved for taxonomic and parataxonomic data.

Beta diversity, as measured by the Coefficient of Community approach, appears, however, to have begun to deviate from a ranking correspondence although the ranks do not differ statistically. In the current study the accuracy is 67%. It may be that below this level of accuracy beta diversity ranking will not be conserved.

Although in this study the Elateridae and Cantharidae join the Staphylinidae, Curculionidae, and Scydmaenidae identified by Oliver & Beattie (1996a) as problematic groups for this approach, Krell’s (2004) survey of various studies employing parataxonomic sortings makes it clear that there is significant variability in accuracy from study to study, depending on sample and sorter. Many other groups surveyed by Krell (2004) show large and variable values in terms of gross sorting error.

Consequently sorting error is not a predictable value for a taxonomic group, making it difficult if not impossible to generalize for which groups the parataxonomic approach is amenable. Krell (2004) further reports the sorting accuracy for 11 studies (the only ones which he could find in the literature)

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Animal Biodiversity and Conservation 29.2 (2006)

90 Kehler et al., 1996 Oliver & Beattie, 1996

80

Derraik et al., 2002 70

Frequency

60

50

40

30

20

10

0

5 to 1

4 to 1 3 to 1 2 to 1 1 to 1 1 to 2 1 to 3 1 to 4 1 to 5 Ratio of taxonomic species to parataxonomic units

1 to 6

Fig. 1. Taxonomic species to parataxonomic unit correspondence.

Fig. 1. Correspondencia entre especies taxon贸micas y unidades parataxon贸micas.

Table 2. Lumping and splitting errors by family: Sp. % of species; L. Lumped; S. Split. T. Total.

Tabla 2. Errores de agrupamiento y escisi贸n por familias: Sp. % de especies; L. Agrupadas; S. Escindidas. T. Total.

Sp

L

S

T

Leiodidae

6

1

1

2

18

Melandryidae

8

1

1

2

9

Scarabaeidae

10

1

1

2

5

1

0

1

Family

Sp

L

S

T

Elateridae

41

10

10

20

Curculionidae

29

8

10

Cantharidae

10

5

4

Family

Staphylinidae

21

4

3

7

Anobiidae

Cerambycidae

17

3

2

5

Kateretidae

1

0

1

1

Carabidae

9

1

3

4

Chrysomelidae

8

0

1

1

Nitidulidae

8

3

1

4

Dermestidae

1

1

0

1

3

0

1

1

1

1

0

1

193

42

45

87

Coccinellidae

5

1

2

3

Lycidae

Mordellidae

8

0

3

3

Salpingidae

Erotylidae

2

1

1

2

Total

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Majka & Bondrup–Nielsen

Table 3. Number of taxonomic species (Tx) and paratxonomic units (PU) for each family of Coleoptera: GE. Gross error (|(A–B)/A|(%)).

Tabla 3. Número de especies taxonómicas (Tx) y unidades parataxonómicas (PU) de cada familia de Coleoptera: GE. Error bruto (|(A–B)/A|(%)).

Tx

PU

GE

Family

Tx

PU

Anobiidae

5

3

40

Lycidae

3

3

0

Apionidae

1

0

100

Melandryidae

8

6

25

Family

Byturidae Cantharidae Carabidae Cerambycidae

GE

1

1

0

Monotomidae

1

1

0

10

10

0

Mordellidae

8

3

63

9

4

56

Mycetophagidae

1

0

100

17

16

6

Nitidulidae

8

12

50

1

1

0

Cerylonidae

1

1

0

Oedemeridae

Chrysomelidae

9

8

11

Orsodacnidae

1

0

100

Ciidae

5

0

100

Pyrochroidae

1

1

0

Cleridae

1

1

0

Coccinellidae

5

6

20

Cryptophagidae

1

0

100

29

36

24

Curculionidae

Pythidae

1

1

0

Salpingidae

1

0

100

10

7

30

Scirtidae

4

3

25

Scarabaeidae

Dermestidae

1

3

200

Scraptidae

5

0

100

Dytiscidae

1

1

0

Silphidae

5

3

40

Elateridae

41

33

20

Silvanidae

2

1

50

Endomychidae

3

1

67

Sphindidae

1

0

100

Erotylidae

2

2

0

Eucinetidae

1

0

100

Eucnemidae

2

1

50

Hydrophilidae

1

1

Staphylinidae

21

23

10

Stenotrachelidae

1

1

0

Tenebrionidae

4

5

25

0

Tetratomidae

4

3

25

Kateretidae

1

1

0

Trogidae

1

1

0

Lampyridae

5

2

60

Trogossitidae

1

1

0

Leiodidae

6

7

17

Total

253

216

15

Lucanidae

2

2

0

with values ranging between 23% and 92%. Krell (2004) points out that this value this is of considerable importance in evaluating the parataxonomic approach. In one instance, Oliver & Beattie (1993) reported a Bryophyta sorting with only a 1% error; however, the accuracy of the sorting was only 23%, indicating a serendipitously equal number of splittings and lumpings. Such situations led Krell (2004, pp. 797) to conclude that, "It may be seriously questioned if a high level of inaccuracy in a sorting result is acceptable if the gross error is low, because the low overall error is caused only by good luck". Although in the present study the overall gross error of the sorting is only 15%, values for individual families range between 0% and 200% with a mean

Mean of families

38

error of 38% (table 3). This is almost double the mean sorting error of 22% in the 79 sortings surveyed by Krell (2004).

There are also unresolved questions as to what significance diversity measurements in general can have in relation to conservation objectives. Goldstein (1997, 1999a) argues that any ecosystem approach that decouples species– and population–specific requirements from management strategies risks compromising fundamental conservation objectives.

Wheeler (1995, pp. 481) argues for the inclusion of systematics within diversity calculations in saying, "more informative measures of biodiversity take into account both numbers of species and the cladistic diversity that they represent".

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Animal Biodiversity and Conservation 29.2 (2006)

Table 4. Beta diversity values: Tx. Taxonomic species; PU. Parataxonomic units. (For other abbreviations see table 1.)

Tabla 4. Valores de la diversidad beta: Tx. Especies taxonómicas; PU. Unidades parataxonómicas.

(Para las otras abreviaturas ver la tabla 1.)

OHW & YSW

YHW & YSW

OSW & YSW

OHW & OSW

OSW & YHW

OHW & YHW

Tx

39,29

41,59

50,49

52,50

57,02

63,08

PU

38,34

35,82

45,20

42,16

45,28

52,63

We are cogniscent of such concerns, and they apply in large measure to indices of diversity however calculated. Clearly any index of diversity is but one approach that attempts to illustrate a small subset of an ecosystem’s properties. It should not be used as a substitute for more detailed and species– based information, particularly in a management or conservation context. The concerns raised by Goldstein (1997, 1999a) make clear the potential pitfalls of conservation approaches based solely on the management of emergent properties of ecosystems or of ecosystem processes. Differences in diversity indices between sites, or changes in diversity over time, should serve as a springboard for further investigation —not as a substitute for it.

Another broad area of concern is with respect to the fundamental epistemological nature of parataxonomy as a discipline. Popper (1989) proposed two principal criteria which a research activity must meet in order to be considered a science: 1) falsifiability; and 2) inter–subjective testability due to reproducibility. Krell (2004) evaluated parataxonomy on these grounds and found that it does not meet the criteria of being a scientific method. This constitutes a serious limitation to the utility of the parataxonomic approach. Bearing this in mind Krell (2004) carefully delineated the spheres where the parataxonomic approach is of utility as being: a) global comparisons of gross species richness; and b) non–comparative descriptions of species richness of single sites or comparisons of species numbers of different habitats within one area without considering species overlap.

Oliver & Beattie (1996a) proposed morphospecies as a relatively quicker and less expensive surrogate for taxonomic species in environmental monitoring and conservation contexts. Nonetheless, even in contexts where the parataxonomic approach is of utility, the savings realized on the one hand may mean that results are only of a more limited applicability on the other —something that ecologists and environmental managers should bear in mind in designing studies.

Some of the debate around this issue has spilled over into the discussion of what constitutes a species and what sort of information we are seeking from nature when we apply any sort of taxonomic

system to it. This is a complex question with an extensive philosophical and biological literature.

Mayden (1997) enumerated and discussed 22 different concepts of "species" in use today. This discussion has perhaps been fueled by a pluralist interpretation of "species" which argues that multiple non–exclusive notions are useful and can yield different kinds of information (Mayden, 1997; Ereshefsky, 1998). A corollary as argued by Stanford (1995) is that the concept of species exists only relative to a given conceptual framework.

Thus species taxa have no unique and objective existence in the real world.

In large measure, however, this discussion is misplaced in this context by the unfortunate confusion between the term "morphospecies" sensu Cain (1954) and "morphospecies" sensu Olivier & Beattie (1993, 1996a, 1996b). As Krell (2004) has pointed out this latter usage is erroneous, not only because the latter is properly preempted by the former, but also what is being considered is not a "pecies" in any meaningful sense of the term, but rather the result of a parataxonomic sorting.

While this philosophical backdrop may not have a direct bearing on evaluating the empirical utility of parataxonomy, it does bear on the more general understanding of the kind of information we derive from nature in employing any analytic grid of classification. How useful it is, is something that we can assess. How real it is, is subject to interpretation.

Acknowledgements We thank all the taxonomic specialists who have assisted with the determinations of species: Robert Anderson (Curculionoidea), Yves Bousquet (Carabidae), Donald Chandler (Pselaphinae), Andrew Cline (Nitidulidae), Anthony Davies (certain Staphylinidae), John Jackman (Mordellidae), Jan Klimaszewski (Aleocharinae), David McCorquodale (Cerambycidae), Darren Pollock (Melandryidae, Scraptidae, and Tetratomidae), Wolfgang Rücker (Latridiidae), Ales Smetana (certain Staphylininae), and Quentin Wheeler (certain Leiodidae). Thanks also to Daniel Kehler and Christine Corkum who undertook the original fieldwork and to Ken Neil and

156

Daniel Kehler who did the original sorting. Thanks to Jan Klimaszewski, David McCorquodale, and David Nipperess for their constructive feedback on earlier versions of the manuscript. Particular thanks to Frank–Thorsten Krell, José G. B. Derraik, and an anonymous reviewer who contributed many constructive suggestions which greatly improved the manuscript. Thanks to Montserrat Ferrer for her encouragement. The first author thanks his colleagues, Andrew Hebda and Calum Ewing at the Nova Scotia Museum, for their continuing support, and most especially his spouse, Sheilagh Hunt, for her forbearance.

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Temporal variability of spawning site selection in the frog Rana dalmatina: consequences for habitat management G. F. Ficetola, M. Valota & F. de Bernardi

Ficetola, G. F., Valota, M. & De Bernardi, F., 2006. Temporal variability of spawning site selection in the frog Rana dalmatina: consequences for habitat management. Animal Biodiversity and Conservation, 29.2: 157–163.

Abstract Temporal variability of spawning site selection in the frog Rana dalmatina: consequences for habitat management.— We evaluated whether R. dalmatina females laid their eggs randomly within a pond or preferred particular microhabitats. The same measures were performed in the same area in two consecutive years to determine whether the pattern remained constant over time. In 2003, we observed a significant selection for areas with more submerged deadwood and vegetation, presence of emergent ground and low water depth. However, these results were not confirmed in the subsequent year when none of the microhabitat features measured had a significant effect. Although microhabitat features can strongly influence tadpoles, the temporal variability of habitat at this spatial scale suggests that habitat management could be more effective if focused on a a wider spatial scale.

Key words: Amphibians, Habitat management, Microhabitat, Rana dalmatina, Reproductive site, Spatial scale.

Resumen Variabilidad temporal en la elección de los lugares de freza de la rana ágil Rana dalmantina: consecuencias para la gestión del hábitat.— Evaluamos si las hembras de R. dalmantina ponían sus huevos al azar en una charca o preferían microhábitats particulares. Durante dos años consecutivos se realizaron las mismas mediciones en la misma área, para determinar si el patrón era constante a través del tiempo. En el año 2003 observamos una selección significativa de áreas con mayor cantidad de ramas muertas y otra vegetación sumergidas, con zonas del fondo emergentes y aguas más someras. Sin embargo, estos resultados no fueron confirmados al año siguiente, en el cual ninguna de las características del microhábitat medidas tuvo un efecto significativo. A pesar de que las características del microhábitat pueden tener gran influencia sobre los renacuajos, la variabilidad temporal del hábitat a esta escala espacial sugiere que la gestión del hábitat podría ser más efectiva si fuera proyectada según una escala espacial mayor.

Palabras clave: Anfibios, Gestión del hábitat, Microhábitat, Rana dalmantina, Lugar de reproducción, Escala espacial.

(Received: 6 VI 06; Conditional acceptance: 19 IX 06; Final acceptance: 21 X 06) Gentile Francesco Ficetola, Maurizio Valota, Fiorenza De Bernardi, Dip. Biologia, Univ. degli Studi di Milano, V. Celoria 26, 20133 Milano, Italy.

Corresponding author: G. F. Ficetola, Univ. de Savoie, Lab. d’Ecologie Alpine, équipe Génomique des Populations et Biodiversité, 73 376 Le Bourget du Lac cedex France. E–mail: francesco.ficetola@unimi.it

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introduction Oviposition habitat selection is a key determinant of reproductive success for many oviparous animals since it can affect important traits such as survival, development and growth rate of the offspring (Mousseau & Fox, 1998). In pond–breeding amphibians, ovoposition habitat selection is a process that can occur at several spatial scales (Resetaris, 2005). At the largest spatial scale, females select the ponds that are in the most favourable landscape, not only because the features of terrestrial habitat are critical for the survival of post–metamorphic stages but also because landscape features can influence the characteristics of ponds (Skelly et al., 1999; Halverson, 2003; Semlitsch & Bodie, 2003; Porej et al., 2004; Marsh et al., 2005). At a smaller spatial scale, within a suitable landscape, frogs do not usually select breeding waterbodies randomly. Both field observations and experimental studies have shown that females attempt to lay eggs in ponds with fewer predators, with greater food availability, with lower desiccation risk or with optimal thermal and chemical features, thus increasing survival or growth rate of tadpoles (e.g., Petranka et al., 1994; Viertel, 1999; Binkley & Resetaris, 2003; Ficetola & De Bernardi, 2004; Resetarits, 2005; Rudolf & Rödel, 2005). However, ponds are not homogeneous environments. Within each wetland, many microhabitats can be recognised, with differences in important features such as water temperature and depth, distribution of animals and plants, and sun exposure. These differences may affect survival and/or growth not only of embryos before hatching but also of tadpoles after hatching. Data on the movements of tadpoles in nature are scarce. However, in a given wetland, tadpoles that hatch close to the more suitable microhabitats could be advantaged when compared with tadpoles that hatched far from suitable areas. This suggests a third spatial scale at which the selection of laying site can occur, that is the microhabitat within a given pond (Tarano, 1998). Knowledge of a selection pattern for a given microhabitat within wetlands could have important consequences for the management of amphibian populations. However, only a limited number of studies have studied whether amphibians lay their eggs randomly within a pond and evaluated the possible consequences of site selection (Jacob et al., 1998; Tarano, 1998).

In this study, we investigated whether, within a pond, the Agile Frog Rana dalmatina lays eggs in microhabitats with selected features. Rana dalmatina could be an excellent species to study within–pond spawning selection since their egg masses are easily identifiable and are usually fixed to the substrate, thus minimizing the risk of movements after the laying. Moreover, as R. dalmatina is an explosive breeder, temporal differences between laying dates of females are minimal, reducing the risk that differences in selection are caused by

temporal variation. Finally, R. dalmatina is a species that is rigorously protected in the European Union (Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and wild fauna and flora) and wetland management is often performed to improve the survival of populations.

Methods Rana dalmatina is a brown frog that is widely distributed in Central and Southern Europe. It inhabits deciduous forests from sea level to an altitude of about 800m (Grossenbacher, 1997).

Rana dalmatina breeds in late winter–early spring in wetlands with stagnant water; each female lays a single egg mass that is usually fixed to the substrate (Nollert & Nollert, 1992). We studied a single R. dalmatina population breeding in a pond (diameter: about 50 m) within the "Ca’del Re" moor (Parco Regionale delle Groane, Lombardy, Northern Italy). The pond is generally permanent but can exceptionally be dry. A potential issue in studies analysing the relationship between species and habitat is their temporal stability. For the applicability of management studies, data need to be validated during subsequent intervals (Vaughan & Ormerod, 2005). We therefore collected the data in two subsequent breeding seasons (2003 and 2004) to evaluate whether the results obtained during one season can be generalized.

The number of R. dalmatina females breeding in this pond, estimated on the basis of egg masses, was 63 in 2003 and 72 in 2004. To improve its suitability for R. dalmatina and the Smooth Newt Triturus vulgaris, in 1998–2001 this wetland was subjected to habitat management (eradication of alloctonous plants; increase of wetland surface and depth) (Ferri et al., 2004).

Two other species of amphibians are also present in this area, the Italian Tree Frog Hyla intermedia and the Pool Frogs belonging to the Rana esculenta complex.

In early spring 2003, we haphazardly selected 36 R. dalmatina clutches laid within this pond. To reduce spatial autocorrelation we allowed a minimum distance of 1 m between two selected clutches. We also randomly selected 29 further points. The minimum distance allowed between two random points or between a random point and a clutch was 1 m. Random points were selected along the pond banks, since all egg masses were laid close to banks. For each egg mass and for each random point, we measured eight environmental variables (table 1). A square frame (1 m 2) divided by a 0.1 x 0.1 m grid was overlapped to each clutch and to each random point to improve measurement of environmental features. The same protocol was repeated in spring 2004 and we measured the microhabitat features of 20 clutches and 18 random points.

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Table 1. Environmental features measured (average ± SE).

Tabla 1. Características ambientales medidas (media ± EE).

Clutches

Random points

2003 (n = 36)

2004 (n = 20)

2003 (n = 29)

2004 (n = 18)

Slope of the nearest bank (0: < 30°; 1: < 45°; 2: > 45°)

0.69 ± 0.12

0.11 ± 0.11

0.52 ± 0.14

0.20± 0.12

Water depth (cm)

37.7 ± 2.29

35.4 ± 3.00

43.2 ± 2.65

32.15 ± 2.51

Distance from the woodland (m)

14.6 ± 1.87

15.8 ± 3.05

14.0 ± 2.07

13.6 ± 1.07

Number of submerged deadwoods (within the frame)

0.25 ± 0.11

0

0

0

Submerged vegetation % (within the frame)

62.6 ± 5.60

38.0 ± 8.48

50.7 ± 7.13

53.9 ± 10.9

Emergent vegetation % (within the frame)

12.9 ± 2.88

48.0 ± 8.10

26.2 ± 6.44

34.4 ± 10.4

Emergent ground % (within the frame)

1.53 ± 0.82

0

0

0

Submerged debris % (within the frame)

12.92 ± 3.57

8.8 ± 3.10

11.3 ± 4.08

5.56 ± 3.81

Environmental features

Data analysis We used logistic regression to analyse clutch distribution, using likelihood ratio (i.e., the change in deviance if a variable is added to the model) to calculate the significance (Menard, 1995). We built all possible models including only significant variables, then ranked the models according to their AIC values (Burnham & Anderson, 2002). The model with the lowest AIC value accounted for the greater deviance on the basis of the smallest number of parameters. AIC was thus used to rank the models according to their performance (Rushton et al., 2004). Models differing less than 2 AIC units from the best model are usually considered good candidates (Burnham & Anderson, 2002). However, as all models differed > 3.6 AIC units from the best model, only the best model was considered and shown in the results. The logistic regression model was built using the data collected in 2003 and was validated using data collected in 2004. It was not possible to perform the inverse procedure since no significant models were built using data collected in 2004.

To avoid multicollinearity, we calculated pairwise correlation between variables in the two years, considering that the risk of multicollinearity arises if pairwise correlation among variables is > 0.7 (Berry & Feldman, 1985). For environmental data collected in 2003, the model was not biased by multicollinearity as all |r| were d [ 0.6.

In 2004, we observed a strong, negative correla-

tion between the percentage of submerged vegetation and percentage of emergent vegetation (r = –0.788). However, as none of the variables were significant, multicollinearity could not be a source of bias.

We also used a t–test to determine whether pond features changed between 2003 and 2004.

Only the features of random points were considered for this analysis. Approximated degrees of freedom were used if variances were not homogeneous between groups.

To meet the assumptions of parametric tests, if necessary data were transformed using arcsine– square root (percentage data) or natural logarithms (distance from the nearest woodland, density of submerged deadwood).

Results We counted 63 egg masses in 2003 and 72 egg masses in 2004. In 2003, 35% of egg masses were isolated (no other egg masses at a distance < 1 m), while 65% of egg masses were aggregated in groups of 2–6 clutches. A similar pattern of aggregation was observed for a subset of 36 egg masses, for which we recorded the location in 2004 (table 2). The frequency distribution of aggregations was almost identical between the two years (Kolmogorov– Smirnov test, Z = –0.120, P > 0.99).

Our best model shows that, in 2003, clutch presence was positively associated to number of sub-

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Table 2. Frequency distributions of aggregations of egg masses during 2003 and 2004: Ne. Number of egg masses per aggregation.

Tabla 2. Distribuciones de frecuencia de los agregados de masas de huevos durante los años 2003 y 2004: Ne. Número de masas de huevos por agregación.

Frequency

Table 3. Logistic regression model explaining R. dalmatina distribution: B. Logistic regression coefficients; Nsdw. Number of submerged deadwoods; Wd. Water depth; Sv. Submerged vegetation; Eg. Emergent ground; C. Constant.

Tabla 3. Modelo de regresión logística que explica la distribución de R. dalmantina: B. Coeficientes de regresión logística; Nsdw.

Número de ramas muertas sumergidas; Wd. Profundidad del agua; Sv. Vegetación sumergida; Eg. Suelo emergente; C. Constante.

Ne

2003

2004

1

0.35

0.31

2

0.29

0.28

Variable

3

0.14

0.25

Nsdw

12.816

9.860

1

0.002

Wd

–0.062

6.318

1

0.012

Sv %

2.131

11.043

1

0.001

Eg %

24.503

5.695

1

0.017

C

0.348

4

0.13

5 6 N measured

0.10

0.17

63

36

merged deadwoods within the frame, submerged vegetation % and emergent ground %, and negatively associated to water depth (table 3). The model explained 28.1% of null deviance and strongly suggested that R. dalmatina females do not lay eggs randomly ((2 = 25.153, d.f. = 4, P < 0.0001).

In 2004, we did not detect the presence of deadwoods or emergent ground in the proximity of egg masses or in the random points (table 1); since these features were not variables we could not include them in the analysis. The model built in 2003 was not significant in 2004 ((2 = 2.516, d.f. = 2, P = 0.284) and explained only 5% of the null deviance. Moreover, we failed to find any significant relationship between the distribution of egg masses in 2004 and the environmental features. The percentage of submerged vegetation was the variable showing the strongest relationship with distribution of egg masses, but this relationship was far from significance ((2 = 1.793, d.f. = 1, P = 0.240).

Most pond features changed little between the years (table 4). In 2004 the pond tended to be shallower, but the random points did not differ significantly for water depth between the years.

Moreover, pond banks were significantly less steep in 2003 (table 4). The complete lack of submerged woods and of areas with emergent ground in 2004 (table 1) suggests that a substantial variations for these two features occurred.

However, the difference for the model between 2003 and 2004 was not entirely due to the lack of submerged deadwoods and of emerging ground in the pond during the 2004 breeding season. To show this, we built a logistic regression model for data collected in 2003, without including the variables

B

(2

d.f.

P

submerged deadwood and emergent ground. After the exclusion of these two variables, both water depth ((2 = 6.698, d.f. = 1, P = 0.010) and % of submerged vegetation (( 2 = 6.061, d.f. = 1, P = 0.014) had a significant effect on the distribution of egg masses. The model including only these two variables still explained 11% of null deviance.

Discussion Our study showed a different pattern in the two years. In 2003, a strong relationship was observed between microhabitat features and distribution of the egg masses of R. dalmatina. This relationship could suggest R. dalmatina selects the area where eggs are laid and allows speculation about the potential importance of this process for the offspring. However, in the same area the relationship was not confirmed during the successive year. The lack of validation with the dataset collected in 2004 makes it more complex to interpret the significant pattern observed in 2003 and to test its applicability in management.

The pattern of laying site selection observed in 2003 can be interpreted in light of the influence that environmental conditions can have on the development of embryos and tadpoles immediately after hatching (see below). Preference for areas with abundant submerged deadwoods is easily explainable since R. dalmatina and several other brown frogs frequently fix their eggs to submerged woods. Fixing eggs could reduce the risk of drifting, and at the same time, fixing eggs under the water surface could reduce the risk of freezing on cold nights and preda-

Animal Biodiversity and Conservation 29.2 (2006)

Table 4. Comparison of features of random points between 2003 and 2004: results of t– tests. Degrees of freedom are not always integer since in some cases they were corrected to account the non–homogeneity of variance: Wd. Water depht; Bs. Bank slope; Sv. Submerged vegetation; Ev. Emergent vegetation; Sd. Submerged debris; Dw. Distance from woodland.

Tabla 4. Comparación de las características de los puntos elegidos al azar entre 2003 y 2004: resultados de los tests t de Student. Los grados de libertad a veces presentan decimales, dado que en algunos casos fueron corregidos para tener en consideración la no homogeneidad de la varianza: Wd. Profundidad del agua; Bs. Pendiente de la orilla; Ev. Vegetación emergente; Sd. Restos sumergidos; Dw. Distancia desde el bosque.

t

d.f.

P

Wd

1.911

45

0.062

Bs

2.302

44.931

0.026

Sv %

–0.227

29.531

0.822

Ev %

–0.750

45

0.457

Sd %

1.272

45

0.210

Dw

–0.322

45

0.749

tion by ducks (Pozzi, 1980). As deadwoods were absent from the study pond in 2004 it was not possible to validate this relationship.

The association with shallow water might be explained by the different thermal conditions of these areas. In areas with lower water depth, the temperature rises more quickly on sunny days: a warm temperature increases the growth and development rate of both embryos and tadpoles (Bachman, 1968; Skelly et al., 2002); in turn, fast growth and development are believed to be important measures for the performance of embryos and larvae and frequently correlate well with their survival (Semlitsch, 2002 and references therein). Thermal conditions of the water have previously proven a major force influencing breeding site selection at both landscape and pond scale (Skelly et al., 1999, 2002; Ficetola & De Bernardi, 2004, 2005a). Association with areas of the pond with emergent ground could be explained on a similar basis. Finally, in areas with more submerged vegetation, tadpoles could find more food and greater shelter from large predators, such as fish. The association of R. dalmatina clutches with abundant vegetation has also been shown by Kescés & Puky (1992). However, an association with areas with abundant veg-

161

etation is not always favourable, since invertebrate predators (such as Odonata) can be more abundant in such an environment (Gunzburger & Travis, 2004). It should be noted that we measured only the distribution of egg masses, and not the survival pattern or tadpole growth. For a complete picture of the effect of the egg mass distribution on fitness it would be necessary to measure survival of eggs and tadpoles, and even their growth rate.

Behavioural interactions can also have important consequences on the distribution of egg masses.

For example, Vieites et al. (2004) showed that mating pairs of the frog Rana temporaria are often followed by clutch pirates which try to fertilize eggs in the deposited clutches after deposition. On one hand, females may spawn only when relatively undisturbed by pirates, while on the other, they may gain benefits from pirates as such behaviour may increase the rate of fertilization of the eggs. This trade–off of interests may well influence the distribution of egg deposition and it is also likely to occur in Rana dalmatina (see K. Grossenbacher, unpublished video recording, cited in Hettyey & Pearman, 2003). Furthermore, at the peak of the breeding season Rana dalmatina males can form aggregation and choruses which may increase the likelihood of attracting females and then scramble– compete over approaching females, but later in the breeding season fewer males may be present and they may be distributed more randomly over the ponds, forming territories (Picariello et al., 2006).

The distribution of males across the pond is strongly affected by these intraspecific interactions and probably plays an important role in the distribution of egg masses. As Rana dalmatina is the only species of brown frog breeding in this pond, interspecific interactions (see discussions by Petranka et al., 1994; Hettyey & Pearman, 2003, 2006; Ficetola & De Bernardi, 2005b, 2006) are not possible.

Surprisingly, the relationship observed in 2003 was not confirmed in the subsequent year even though the same sampling protocol was applied, and it is rather difficult that it occurs since during 2004 as we did not observe variation for two main features. Microhabitat features can be difficult to study, and at this spatial scale changes from the expected patterns are often seen (but see also Rudolf & Rödel (2005) for an example of model transferable in time). For example, Halverson et al.

(2006) studied the distribution of tadpoles of the Wood Frog Rana sylvatica in two ponds less than 50 m apart. From the outcome of laboratory studies, it would be expected that tadpoles were aggregated in kin groups (Blaustein & Waldman, 1992).

However, Halverson et al. (2006) observed an aggregated distribution of kin groups in only one of the two ponds, and found an opposite pattern in the second pond, with kin tadpoles more distant than would be expected if they were randomly distributed. This suggested that the optimal distribution of tadpoles can be context dependent and strongly modified by microhabitat variations. In our study, the absence of relationships might be caused by

162

the change in pond features over the two years. In 2004 the pond was shallower and slightly smaller, and no deadwoods were present. Nevertheless, the number of egg masses laid did not decrease between the years, suggesting that these changes in microhabitat did not have a major effect on the reproductive output of R. dalmatina.

Differences between years in tadpole performance are possible but these were not investigated in the present study. The contradictory results between the two years suggest that a larger sample is needed (higher number of oviposition sites collected over more years), as pond microhabitat features show a wide variation. Moreover, sampling more ponds would be necessary to evaluate whether the results are consistent across space.

Non–random choice of egg deposition site within breeding ponds has been demonstrated for several amphibians, including the Newt Triturus marmoratus and the anurans R. dalmatina, R. temporaria and Physalemus pustolosus (Ancona & Capietti, 1996; Jacob et al., 1998; Tarano, 1998). However, interpretation of relationships at this spatial scale can be difficult as patterns are not always confirmed in successive periods. Small environmental variations can partially explain the difficulty in finding a general pattern. Lack of a clear pattern and fast variation of microhabitat features with time can hamper the use of this information for habitat management (Wittingham et al., 2003). Indeed, actions performed at a microhabitat level can be quickly neutralized by natural events such as changes in precipitation or in the growth of vegetation. We therefore suggest concentrating the management effort at the largest spatial scales (pond and landscape) as these suffer less temporal instability. Features at the largest spatial scale can influence those at the smaller scale; the presence of surrounding woodlands, for example, can influence the presence of deadwoods but also the chemical and physical features of the waterbodies (Kiffney et al., 2003; Ficetola et al., 2004). Analogously, the introduction of fish can modify other features such as turbidity and the distribution of vegetation (Sheffer et al., 1993). Acting at the largest spatial scales could therefore provide more effective results for the management of amphibian populations.

Acknowledgments We thank M. Brambilla, M. Tejedo, M. Vences and an anonymous reviewer for useful suggestions on earlier versions of this manuscript.

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"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

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Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 29.2 (2006)

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Impacts of endangered Key deer herbivory on imperiled pine rockland vegetation: a conservation dilemma?

M. A. Barrett & P. Stiling

Barrett, M. A. & Stiling, P., 2006. Impacts of endangered Key deer hervivory on imperiled pine rocklands: a conservation dilemma? Animal Biodiversity and Conservation, 29.2: 165–178.

Abstract Impacts of endangered Key deer herbivory on imperiled pine rockland vegetation: a conservation dilemma?— In the lower Florida Keys, endangered Key deer (Odocoileus virginianus clavium) herbivory, along with fire, can affect pine rocklands, an endangered plant community. We compared pineland vegetation from three studies over approximately 50 years on four islands with either high or low deer density (historical analysis). We also compared extant vegetation samples between two islands with high or low deer density, which contained pinelands burned 10 years and 14 years prior to sampling and control areas (unburned for > 50 yr). In addition, experimental deer exclosures and control plots established in pineland were prescribe burned and analyzed for deer effects on an island with high density of Key deer. The historical analysis suggests that, over time, deer–preferred plant species declined while less–preferred species increased, regardless of fire history on islands. The extant vegetation analysis suggests that fire and Key deer herbivory both reduce hardwood plant density and growth. Densities of deer–preferred woody species were higher on an island with low deer density than on an island with high deer density in burn treatments, but relatively similar in control areas. On the high deer density island, a fire effect was evident in that the control area had higher densities of woody species than burned areas, and herbaceous species richness was higher in the control area, indicating a possible refuge from deer herbivory. In deer exclosures, preferred woody species and herbaceous species tended to increase after fire, but decrease in adjacent open plots. Results suggest that Key deer herbivory, along with fire, shapes pine rockland plant communities, and that overbrowsing might have substantial impacts on preferred herbaceous and woody species in pinelands. Therefore, efforts could be confounded in managing both the endangered Key deer and the endangered pine rocklands that they affect.

Key bwords: Browsing, Exclosure, Fire–deer interactions, Fire history, Island, Odocoileus virginianus clavium.

Resumen Impactos del pastoreo del ciervo de los cayos, una especie en peligro de extinción, sobre el también amenazado pinar rupícola: ¿un dilema conservativo?— En los cayos del sur de Florida, el pastoreo del ciervo de los cayos (Odocoileus virginianus clavium), junto con los incendios, pueden afectar a los pinares rupícolas, una comunidad vegetal en peligro. Hemos comparado la vegetación de los pinares de tres estudios llevados a cabo durante aproximadamente 50 años en cuatro islas con densidades de ciervos altas o bajas (análisis histórico). También comparamos muestras de vegetación existentes en dos islas con una densidad alta y baja de ciervos, que contenían pinares quemados 10 y 14 años antes del muestreo con áreas de control (sin incendiar durante más de 50 años). Además, se incendiaron intencionadamente y se analizaron parcelas experimentales con exclusión de ciervos y de control, para conocer los efectos de los ciervos en una isla con una gran densidad de éstos de los cayos. El análisis histórico sugirió que, con los años, las especies de plantas preferidas por los ciervos decayeron, mientras que las menos preferidas proliferaron, independientemente de los incendios sufridos. El análisis de la vegetación existente sugiere que tanto los incendios como la alimentación de los ciervos reducen la densidad y el crecimiento de la vegetación leñosa. Las densidades de las especies leñosas preferidas por los ciervos eran mayores en la isla con una densidad baja de ciervos, que en la isla con una densidad alta de ciervos tras los incendios, ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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pero eran relativamente similares en las áreas de control. En la isla con una mayor densidad de ciervos, los efectos del fuego eran evidentes, ya que el área de control poseía mayores densidades de especies leñosas que las áreas incendiadas, y la riqueza de especies herbáceas era mayor en la zona de control, lo que indicaba que se trataba posiblemente de un refugio ante los ciervos. En las zonas cerradas a los ciervos, las especies herbáceas y las leñosas preferidas por los ciervos tendían a aumentar tras el incendio, pero disminuían en las áreas abiertas adyacentes. Los resultados sugieren que el pastoreo del ciervo de los cayos, junto con el fuego, dan forma a las comunidades vegetales rupícolas, y que el sobrepastoreo puede tener un impacto sustancial sobre las especies herbáceas leñosas preferidas de los pinares. Por lo tanto, los esfuerzos para la gestión, tanto del amenazado ciervo de los cayos como de los pinares rupícolas afectados por éste, también en peligro, podrían ser contradictorios.

Palabras clave: Pastoreo, Exclusión, Interacciones fuego–ciervos, Historial de incendios, Isla, Odocoileus virginianus clavium.

(Received: 12 VII 06; Conditional acceptance: 7 XI 06; Final acceptance: 12 XII 06) Mark A. Barrett & Peter Stiling, Dept. of Biology, Univ. of South Florida, 4202 E Fowler Ave, SCA110, Tampa, FL 33620, USA. Corresponding author: M. A. Barrett. Present address: U.S. Fish and Wildlife Service, Arthur R. Marshall Loxahatchee National Wildlife Refuge, 10216 Lee Road, Boynton Beach, FL 33437 USA. E–mail: mark_barrett@fws.gov

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Introduction There is much impetus for conservation biologists to protect both endangered animals and imperiled plant communities, though measures to protect these two entities are not always mutually exclusive. That is, protecting an endangered animal species could result in unintentional impacts on an endangered plant community. This could complicate management and conservation efforts to concomitantly protect both animal species and plant communities. Such a scenario could be occurring in the National Key Deer Refuge (NKDR) where protection of federally endangered Key deer (Odocoileus virginianus clavium), a diminutive subspecies of white–tailed deer, has led to increased deer densities on certain islands. This, in turn, has subsequently caused strong browsing pressure on tropical plant communities, e.g., hardwood hammock, buttonwood transition, and mangrove wetland (Barrett, 2004; Barrett & Stiling, 2006a; Barrett et al., 2006). In this paper, we investigate whether elevated densities of Key deer might also impact pine rockland (hereafter pineland), a globally endangered plant community (Florida Natural Areas Inventory, 1990) found in the NKDR. Habitat loss and over–hunting of Key deer galvanized the establishment of the NKDR in 1957.

Furthermore, extensive development in the Florida Keys prompted conservationists to begin land acquisition efforts to protect both endangered Key deer and plant communities. The refuge, and federal protection of Key deer in 1967, allowed the deer population to increase from 25–80 animals in the 1950s to 300–400 in the 1990s and 500–700 by 2000 (Klimstra, 1990; Lopez, 2001). Despite a potential range of 26 islands, approximately 75% of the Key deer population resides on Big Pine and No Name keys, resulting in high deer densities on these islands (Lopez et al., 2004a).

Because Key deer prefer pinelands as an important habitat for foraging (Dickson, 1955; Klimstra et al., 1974; Silvy, 1975; Klimstra & Dooley, 1990; Carlson et al., 1993; Lopez et al., 2004b), it is anticipated that the increased densities of Key deer would result in strong browsing pressure that could affect the fundamental composition of pineland plant communities. Pinelands in the NKDR may also be affected by fire, which can accelerate, decelerate, or stabilize community succession (Abrahamson, 1984a, 1984b).

Pineland is considered a fire–climax system in the lower Florida Keys. In the absence of fire, pinelands may ultimately succeed into hardwood hammock, which may occur within 2 to 3 decades on the Florida mainland (Alexander, 1967) but may take longer (> 100 years) in the lower Florida Keys (Carlson et al., 1993). For example, Folk (1991) generally found higher densities of hardwood tree species in lower Key’s pinelands subject to less–frequent burns (possibly > 50 yrs), though ultimate succession to hardwood hammock was incomplete.

Browsing pressure by Key deer could also impact pinelands, as heavy herbivory by white–tailed deer has been noted to influence species composition, successional pathways, and regeneration of plant communities (e.g., Russel et al., 2001; Rooney & Waller, 2003). Deer browsing can affect plant communities associated with fire by reducing plant growth in relatively short–time periods after fire (e.g., Davis, 1967; Huffman & Moore, 2004). Fire in pinelands benefits Key deer by increasing plant availability and quality, and consequently Key deer more frequently browse certain woody and herbaceous plant species in recently burned pinelands (Carlson et al., 1993; U.S. Fish and Wildlife Service, 1999).

To determine if increased densities of endangered Key deer, along with fire, are impacting pineland communities, this study investigated the effects of browsing pressure and fire on pinelands between islands with high and low densities of deer. The study tested the null hypotheses that (1) plant species differentially preferred by deer show no difference in relative density over a long–term period (approximately 50 years) on islands with contrasting deer densities regardless of fire history, (2) there is no difference in vegetative cover or density between islands with high and low deer density in areas with identifiable fire history, and (3) deer exclusion along with fire has no impact on pineland vegetation.

Methods Study area In the lower Florida Keys, the mean annual temperature is ~25.2°C and mean annual rainfall is ~1,000 mm. The climate is subtropical with evident wet (May–October) and dry (November–April) seasons. Many lower keys have vegetation types ranging from inundated wetlands and transitional zones to uplands (Dickson, 1955; Folk, 1991), though pinelands (totaling < 1000 ha) are predominately found on only five islands within the NKDR boundaries (24° 36´ N – 81° 18´ W to 81° 34´ W).

For each island, percent pineland area of the total island area was as follows: Big Pine (28%), Little Pine (17%), No Name (11%), Sugarloaf (5%), and Cudjoe (5%), with relic stands on Howe (<1%) and Knockemdown keys (< 1%) (Lopez, 2001).

Pineland occurs 2 m or more above sea level and has the highest elevation among plant communities in the lower Keys (Folk, 1991). The soil is very shallow, underlain by oolitic limestone (exposed in many areas), which is continuous with Miami Oolite of mainland Florida (Dickson, 1955).

Vegetation is primarily of West Indian origin (Stern & Brizicky, 1957). The monotypic canopy is dominated by the only pine species in the lower Keys, slash pine (Pinus elliottii var. densa), while the mid–story includes silver–palm (Coccothrinax argentata), Key thatch palm (Thrinax morrisii) and

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black–bead (Pithocellobium keyense). Though pinelands may contain a high diversity of shrubs and herbaceous species (Snyder et al., 1990), characterization of the understory depends on successional stage and fire history. Plant nomenclature throughout the paper follows Scurlock (1987) for woody species and Wunderlin (1998) for herbaceous species.

Key deer densities Key deer densities were estimated by various methods for each sampling period. Dickson (1955) and Folk (1991) employed less rigorous methods, such as deer pellet counts, track counts, and informal census (i.e., casual sightings) to assign a relative use index of Key deer per island. Dickson (1955) only provided a qualitative account of deer incidence. Folk (1991), however, used the information of deer observations to create a quantitative index (e.g., 0 representing no use and 10 representing maximum use) that was used to coarsely estimate a range of deer abundance per island (Folk 1991 in Klimstra, 1990) —we used the midpoint of this range to present deer density per island in the present study. Between 1999 and 2000, infrared— triggered cameras placed near areas frequented by Key deer were used to estimate Key deer abundance on most islands (Lopez, 2001) following protocol of Jacobson et al. (1997) by using 1 camera/50 ha for periods > 3 months. On Big Pine and No Name keys, deer numbers were estimated via census and radio–telemetry (Lopez, 2001; Lopez et al., 2004a). Estimates of deer abundance from the Folk (1991) and Lopez (2001) studies were divided by island size (km2) to conservatively calculate Key deer densities (deer/km2) (table 1).

Fire history Though fire history is limited in the lower Keys, Bergh & Wisby (1996) mapped occurrences (but not intensities) of controlled burns and wildfires between 1960 and 1996 within the NKDR. Big Pine experienced periodic fires in certain pineland areas (some areas were burned repeatedly) occurring in 1966, 1977, 1987, 1990, 1991 and 1994 whereas other areas have not been burned in > 50 years. Frequent fires likely occurred on Big Pine before the 1950s as well (Dickson, 1955; Alexander & Dickson, 1970). Pinelands on Sugarloaf were burned in 1987, 1990, and 1991 and also contained areas unburned in > 50 years.

All pineland areas were burned on Little Pine, Cudjoe, and No Name in various years between 1960–1996, whereas no fires have occurred on Howe for at least 50 years.

Deer selectivity among plant species Key deer preference among woody plant species (based on foliage consumption) were established from feeding trials (Barrett & Stiling, 2006a), ru-

Barrett & Stiling

men analyses (Klimstra & Dooley, 1990), and direct or indirect observations of Key deer browse (Dickson, 1955; Klimstra et al., 1974; personal observations). Woody plant species were grouped by deer preference as follows: (1) preferred species were Bursera simaruba, Erithalis fruticosa, Bumelia celastrina, Jacquinia keyensis, Guapira discolor, Pithecellobium keyense, and Morinda royoc and (2) less–preferred species were all other species besides those in the final category and (3) other species were fruit suppliers (three palm species and Byrsonima lucida) of which Key deer mainly consume the fruits (impact of Key deer frugivory on recruitment of plant species is uncertain). The following classification of deer preference was used for herbaceous species based on Dooley (1975), Folk (1991) and personal observations: (1) preferred species were notably grazed including Chiococca pinetorum, Smilax havanensis, and Chamaecrista aspera, (2) less–preferred species were the remaining species besides grasses and (3) other species were all grass species of which Key deer mainly consume the seeds.

Historical analysis Pineland vegetation was analyzed on islands with high (Big Pine and No Name) and low (Cudjoe and Sugarloaf) deer densities over a long–term period of approximately 50 years.

Three studies were used for temporal comparison including Dickson (1955), Folk (1991) and the present study, conducted in 2001. The historical analysis was utilized to track overall pineland condition as deer densities have increased, regardless of fire history. However, pineland on Sugarloaf was not sampled in the 1955 study.

For vegetation sampling protocol, densities (ha– 1) of woody plant species were estimated by counting individual plants in 1 x 30.5 m rectangular quadrats in the 1955 and 1991 study and a 1 x 50 m rectangular quadrat for the 2001 study. Woody seedlings < 30.5 cm tall were sampled in 1 m2 quadrats (n = 3 per rectangular quadrat) nested within the larger quadrat in the 1991 study, whereas the 1955 and 2001 studies quantified woody seedlings in the entire larger quadrat. The same number of larger quadrats was used for each island (n = 10) among studies. Densities of woody plant species were summarized to height classes: < 1.2 m tall (within Key deer reach) and > 1.2 m tall (midstory / canopy). The former height class was examined for changes in understory vegetation that can be directly attributable to browsing effects, and the latter height class was examined for any changes in midstory / canopy species composition, potentially caused by lack of regeneration or stunted plant growth following deer herbivory. Key deer herbivory can be distinguished from other herbivory types as the petiole is left intact after browsing the leaf / leaflet.

Standardized relative densities (species density / 3 all species densities) of plant species

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Animal Biodiversity and Conservation 29.2 (2006)

Table 1. Estimates of Key deer densities or incidence on four islands in 1955, 1991 and 2001. For 1955, estimates are of deer incidence via observational analyses, and for 1991 and 2001, Key deer densities were calculated by dividing the estimated number of deer per study year by island size. The estimated population size represents the predicted size of the entire Key deer population throughout its range in the NKDR during each study year.

Tabla 1. Estimas de las densidades o presencia del ciervo de los cayos en cuatro islas, en 1955, 1991 y 2001. Para el año 1955, las estimas de la presencia de ciervos se hicieron mediante análisis de observación, y para 1991 y 2001, las densidades del ciervo de los cayos se calcularon dividiendo el número estimado de ciervos por año de estudio por el tamaño de la isla. El tamaño estimado de la población representa el tamaño predicho de la población total del ciervo de los cayos en todo su hábitat de distribución en el Refugio Nacional del ciervo de los cayos (NKDR) durante cada año de estudio.

Island size

Key deer km–2

Deer incidence

km2

1995

1991

2001

Big Pine

25.03

Extensive evidence

7.39

17.74

No name

4.91

Extensive evidence

13.75

21.59

Cudjoe

14.35

Very little evidence

0.21

0.35

Sugarloaf

8.06

No evidence

0.50

0.62

25–80

300–400

500–700

Island name

Estimated population size

were statistically evaluated per sampling period to alleviate effects of variation in quadrat size among studies on absolute plant densities. The relative densities of plant species, categorized by preferred, less–preferred and other species, were compared between each year (1955 vs.1991, 1955 vs. 2001, and 1991 vs. 2001) employing a similar analysis used by Whitney (1984) by testing the equality of two percentages (Sokal & Rohlf, 1969). This test compares the relative density, or percentage, between two samples (i.e., study years) by analyzing the sample proportions and the total sample size using the formula:

between studies following the formula (Gotelli & Graves, 1996): S

E(Sj) = 3 1 – (1 – aj / AT)

ni

i=1

where a j is the area of the jth subsample (i.e. the smaller 1991 quadrat), AT is the area of the larger sample (i.e. the larger 2001 quadrat), n i is the abundance of species i per island, and E(Sj) equals the expected number of species in the 2002 sample. We qualitatively compared plant species richness from the 2001 passive sample to species richness from 1955 and 1991.

Analysis of deer–fire effects

arcsin /p1 – arcsin /p2 ts = /(820.8 × (1/n1 + 1/n2) where p1 and p2 are the proportions of each sample (e.g., relative density of preferred species in a study year), n 1 and n 2 are the representative sample size (i.e., total density of preferred species in a study year), and 820.8 is a constant representing the parametric variance of the distribution of arcsine transformations of proportions.

Variation in vegetation quadrat sizes between the studies also likely influenced estimates of plant species richness. This concern was minimized by passively sampling species richness (all height classes combined) from 2001 samples by equilibrating vegetation quadrat areas

Due to limitations in equivalent fire history among all islands, pineland communities were compared on two islands with contrasting deer densities, Big Pine and Sugarloaf, each containing areas with similar burn years and unburned areas. Deer densities were high on Big Pine and low on Sugarloaf, and fire history on both islands included areas burned in 1991 and 1987, and unburned areas.

Therefore, data collected in 2001 (present study) are referred to as 10 years after fire (YAF), 14 YAF, and Control (unburned), respectively.

Vegetation in pinelands was sampled during the dry season from January to May of 2001. Digital habitat maps (MacAuley et al., 1994) were used in conjunction with maps from Bergh & Wisby (1996) to determine sample units for fire treatments on Big Pine and Sugarloaf keys. In the designated pineland

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Table 2. Relative densities of woody plant species < and > 1.2 m tall categorized by deer preference, and plant species richness (S) of both height classes combined on islands with high and low deer densities. Plant measures were from three studies in pinelands from 1955, 1991, and 2001.

Different letters among years within an island indicate significant difference (equality of percentages test —see Methods for explanation).

Tabla 2. Densidades relatives de las especies vegetales leñosas < y > de 1,2 m de altura, clasificadas según la preferencia de los ciervos, y riqueza de especies vegetales (S) de ambos grupos de alturas combinados en islas con densidades grandes y pequeñas de ciervos. Las mediciones de plantas proceden de tres estudios de pinares de 1955, 1991 y 2001. Las distintas letras entre los años dentro de una isla indican diferencias significativas (tests de igualdad de porcentajes —véase Methods para la explicación).

Less–preferred relative density Island

Preferred relative density

Other relative density

Year

< 1.2 m

> 1.2 m

S

< 1.2 m

> 1.2 m

S

< 1.2 m

> 1.2 m

S

1995

35.6 a

69.8 a

10

27.4 a

17.0 a

5

37.1 a

13.2 a

3

1991

67.2 b

76.2 a

15

22.7 a

8.2 a

6

10.1 b 115.6 a

3

2001

63.4 b

70.2 a

17

14.8 b

11,9 a

6

21.5 c

17.9 a

3

1995

19.0 a

19.6 a

17

68.1 a

67.6 a

5

12.9 a

12.8 a

3

High deer density Big Pine

No name

1991

54.3 b

74.2 b

19

41.4 b

18.0 b

4

4.3 b

7.7 a

3

2001

62.8 b

73.4 b

20

28.6 c

18.3 b

3

8.6 ab

8.3 a

3

1995

38.8 a

40.4 a

18

47.1 a

45..7 a

5

14.1 a

13.9 a

4

1991

43.2 a

46.3 ab 16

45.2 a

45.3a

4

11.6 a

8.4 a

3

2001

46.4a

57.2 b

20

43.7 a

33.7 a

6

9.9 a

14.1 a

4

1995

–

–

–

–

–

–

–

–

–

1991

72.2 a

47.1 a

23

22.1 a

29.8 a 5.7 a

23.1 a

2

2001

65.5 a

56.7 a

23

28.2 a

24.5 a

6.3 a

18.9 a

Low deer density Cudjoe

Sugarloaf

areas, a total of 43 vegetation rectangular quadrats (n = 5–13 quadrats per burn treatment per island) were randomly located and sampled.

Rectangular 1 x 50 m quadrats were used to sample woody plant species that were assigned to height classes: < 1.2 m and > 1.2 m. Plant species that branched underground were considered individuals if the protruding stems were separated.

Herbaceous ground cover was estimated at five circular plots (1 m2) placed every 10 m along the 1 x 50 m quadrat using percentage cover classes described by Daubenmire (1969) as follows: < 1, 1–5, 6–25, 26–50, 51–75, and > 75. Canopy cover (5 samples per quadrat) was measured with a concave densiometer (Forest Densiometers, Bartlesville, Oklahoma) on a tripod (45 cm high) placed every 10 m along the 1 x 50 m quadrat.

Methodology for recording densiometer readings was according to Lemmon (1957). Data were summarized for each burn treatment per island.

7

5

For quadrat data, density of woody plants (all species combined within each < 1.2 m tall and > 1.2 m tall classes), species richness, herbaceous % cover, and canopy % cover were each analyzed separately within each island of low (Sugarloaf) or high (Big Pine) levels of deer density using 1–way ANOVA with burn treatment (10YAF, 14YAF, Control) as the main effect.

Bonferonni post hoc tests were used to compare differences among means. To meet normality assumptions as analyzed with Lillifor’s test, data for plant density (both < 1.2 m and > 1.2 m class) were each log + 1 transformed. Jaccard similarity was used to compare species composition among burn treatments per island. Furthermore, each preferred woody species (< 1.2 m tall and > 1.2 m tall) was analyzed separately using nonparametric Mann–Whitney U tests comparing densities between Sugarloaf and Big Pine within each burn treatment (10YAF, 14YAF, Control).

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Animal Biodiversity and Conservation 29.2 (2006)

Table 3. Mean (! SE) percent canopy cover, density of woody species (< and > 1.2 m tall) and percent cover of herbaceous species on islands with high deer density (Big Pine) and low deer density (Sugarloaf). Burn year treatments were 10YAF, 14YAF, and Control; Cc. Canopy cover; Ch. Cover of herbaceous species.

Tabla 3. Porcentaje medio (! EE) de la cobertura del dosel forestal, densidad de especies leñosas (< y > de 1,2 m de altura) y porcentaje de cobertura de especies herbáceas en islas con densidades de ciervos alta (Big Pine) y baja (Sugarloaf). Los incendios intencionados tuvieron lugar 10 años tras el fuego (YAF), 14YAF, y Control (C). Cc. Cobertura arbórea; Ch. Cobertura de especies herbáceas.

Density woody species % Cc Treatment

X

< 1.2 m tall ! SE

X

> 1.2 m tall

% Ch

! SE

X

! SE

X

! SE

High deer density 10 YAF

51.6

5.7

14000

741.1

1550

320.2

16.0

2.8

14 YAF

47.1

3.3

14235

1891.1

2625

517.5

12.9

1.9

Control

59.6

5.9

22762

3099.1

4723

770.5

12.7

1.3

Lower deer density 10 YAF

71.4

5.4

23400

1398.6

6480

804.0

9.5

1.2

14 YAF

68.8

4.4

34450

4952.3

11975

1570.7

8.8

2.0

Control

80.7

7.9

28040

5805.0

10240

1497.2

7.0

0.6

Due to pseudoreplication (Hurlbert, 1984), with only one area per burn treatment on each island, data were analyzed assuming that sampling error represented the experimental error (Webster, 1992).

Pseudoreplicated designs for many fire studies are problematic but can be somewhat moderated (Mantgem et al., 2001). For example, because our study design did not allow burn treatments to be independently applied (i.e., vegetation quadrats were considered the independent units within each burn treatment per island), inferences derived from the analyses only include the study islands. However, because Key deer use is mainly confined to Big Pine and No Name, the limited inference space of this study still has valuable applicability for management of Key deer and their habitat.

Deer exclosures In August 2001, two square 37 m2 deer exclosures were constructed that were randomly located in pinelands on No Name Key. Control plots were non–randomly selected within 10 m of exclosure plots that had a relatively similar composition of plant species. Chain–linked fencing 1.8 m high was erected for exclosure plots to exclude Key deer, but was raised 15 cm above the ground to allow access by other species including the lower Keys marsh rabbit (Sylvilagus palustris hefneri), raccoon (Procyon lotor) and the Florida box turtle (Terrapene carolina bauri).

Data were collected every 6 months from August 2001 to July 2004. In June 2003 a prescribed fire burned > 95% of the area in both exclosures and their adjacent open plots. To examine deer–fire effects on plant composition and structure, the plots were sampled directly after the burn, then in August 2003, January 2004 and July 2004 (1 year post–burn). Woody species were quantified over the entire plot. Mean percent cover of herbaceous species was quantified from 9 circular subplots (1 m2), and percent frequency of herbs was determined from the 18 subplots summarized over treatment replicates. To limit edge effects, data were not recorded in a buffer zone (0.3 mW x 2.1 mH) within the plot perimeters.

To separate potential deer effects from fire effects in the deer exclosure study, statistics were employed separately for data collected pre–fire (August 2001 to January 2003) and post–fire (June 2003 to July 2004). Plant abundances were summarized per treatment (open / exclosure) within each species group (i.e., preferred, etc.) for each replicate plot from the first sample date and last sample date for each pre–fire and post– fire event. The difference in plant abundance per species per replicate plot between the two times (abundance of last sample–abundance of first sample) was then calculated and averaged within treatment. Data (mean difference between first and last sampling dates) were tested using a two sample t–test for each plant category (e.g., pre-

172

Barrett & Stiling

10YAF

High deer density

7500

Low deer density

6000 4500 3000 1500

Mean density (ha–1)

0 7500

14YAF

6000 4500 3000 1500 0 Control 7500 6000 4500 3000 1500 0 Mr

Pk

Ra

Ef Gd Species

Jk

Bc

Bs

Fig. 1. Mean (! SE) densities of preferred woody plant species < 1.2 m tall in pinelands on islands with high deer density (Big Pine) and low deer density (Sugarloaf). Burn year treatments were 10YAF, 14YAF, and Control (unburned). Asterisks indicate significant differences (P < 0.05) based on Mann– Whitney U tests. Species: Mr. M. royoc; Pk. P. keyense; Ra. R. aculeata; Ef. E. fructicosa; Gd. G. discolor; Jk. J. keyensis; Bc. B. celastrina; Bs. B. simaruba.

Fig. 1. Densidades medias (! DE) de las especies leñosas preferidas < 1,2 m en pinares en islas con una densidad de ciervos alta (Big Pine) y baja (Sugarloaf). Los incendios intencionados fueron 10YAF, 14YAF y Control (sin incendio). Los asteriscos indican diferencias significativas (P < 0,05), basándose en los test U de Mann–Whitney. (Para las abreviaturas, ver arriba.)

ferred, etc.) for woody abundance and herb percent cover. Herb percent cover was arcsine square root transformed prior to analysis to meet normality assumptions. All statistical analyses were tested at the P = 0.05 significance level. For data analyses, SYSTAT® (1998) was used for conventional statistics (e.g., ANOVA, t–tests) and Microsoft® Excel (Microsoft, 1997) was used to set up and perform analyses that were not readily available (e.g., equality of percentages test, passive sampling).

Results Historical analysis Regardless of fire history, relative plant densities < 1.2 m tall of deer–preferred species significantly declined while less–preferred species increased on islands with high deer density (table 2). Relative densities of preferred species in the > 1.2 m height class also tended to decline on islands with high density of deer. Comparatively, islands

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Animal Biodiversity and Conservation 29.2 (2006)

10YAF

High deer density

2000

Low deer density 1500 1000 500 0

Mean density (ha–1)

2000

14YAF

1500 1000 500 0 2000

Control

1500 1000 500 0 Mr

Pk

Ra

Ef Gd Species

Jk

Bc

Bs

Fig. 2. Mean (! SE) densities of preferred woody plant species > 1.2 m tall in pinelands on islands with high deer density (Big Pine) and low deer density (Sugarloaf). Burn year treatments were 10YAF, 14YAF, and Control (unburned). Asterisks indicate significant differences (P < 0.05) based on Mann– Whitney U tests. (For abbreviations of species see figure 1.)

Fig. 2. Densidades medias (! EE) de las especies leñosas preferidas > 1,2 m en pinares en islas con una densidad de ciervos alta (Big Pine) y baja (Sugarloaf). Los incendios intencionados fueron 10YAF, 14YAF y Control (sin incendio). Los asteriscos indican diferencias significativas (P < 0,05), basándose en los test U de Mann–Whitney. (Para las abreviaturas de las especies ver la figura 1.)

with low deer density showed little change in relative density of plant species regardless of deer preference (table 2). Observed changes in species richness were predominately found on islands with many deer, especially increases in less–preferred species.

Deer–fire effects on vegetation Among burn treatments in pinelands, percent canopy cover was similar on both Sugarloaf (F2, 15 = 0.21,

P = 0.813) and Big Pine (F2, 22 = 2.64, P = 0.093) (table 3). Mean densities of woody plant species < 1.2 m tall were similar on Sugarloaf (F2, 15 = 1.64, P = 0.227) but marginally differed on Big Pine (F2, 22 = 3.38, P = 0.053) (table 3). Mean densities of woody plants for the > 1.2 m tall class were significantly different among burn treatments on Sugarloaf and on Big Pine (both P < 0.009), with densities in the 10YAF less than Control (Bonferonni post–hoc: P = 0.062 (marginal significance) for Sugarloaf and P = 0.007 for Big Pine) (table 3). Mean woody

174

Barrett & Stiling

A

Open Exclosure

Non–preferred species 80 60 40 20

Mean number of stems

0 Preferred species 80 60 40 20 0 Other species 80 60 40 20 0 Aug 01

Jan 03 Jun 03 (fire) Time

Jul 04

Fig. 3. Mean (! SE) abundance (number of stems) of woody species (A) and % cover of herbaceous species (B) in exclosure and open plots in pinelands on No Name. A fire occurred in June 2003. For woody species, plant abundances were all height classes combined for each category of deer preference, and plant species are categorized as preferred, non–preferred, and other (Palm spp. and Byrsonima lucida). Herbaceous species are categorized as preferred, less–preferred and grass species (other).

species richness was similar on Sugarloaf among 10YAF, 14YAF, and Control plots with 29, 33, and 30 species respectively (F2, 15 = 0.88, P = 0.430), compared to Big Pine’s 18, 27 and 30 species respectively (F2, 22 = 6.13, P = 0.011) where 10YAF differed from 14YAF and Control (Bonferonni post hoc: P < 0.017). Differences were mainly caused by absence of deer–preferred (hammock associated) species in 10YAF. Jaccard similarity indices indicated that plant species composition among burn treatments on Big Pine were all < 69%, whereas similarities were > 89% among burn treatments on Sugarloaf.

Compared to Sugarloaf, Big Pine had lower densities of most preferred woody plant species < 1.2 m tall (Mann–Whitney U tests; fig. 1). The species highly preferred by Key deer that were absent or virtually absent from Big Pine pinelands were Bursera simaruba, Erithalis fruticosa, Jacquinia keyensis, Guapira discolor and Bumelia celastrina, which are all mainly associated with

hardwood hammock. As time from last burn increased, a pattern of increasing density and number of preferred species was evident on Big Pine, suggesting that unburned pinelands support more deer–preferred woody species on this island. Similar trends also occurred for densities of preferred plant species > 1.2 m tall (fig. 2).

Mean percent cover of herbaceous species was similar among burn treatments on Sugarloaf (F 2 , 15 = 0.39, P = 0.681) and on Big Pine (F 2, 22 = 0.30, P = 0.744) (table 3), though control plots tended to have the lowest cover values on both islands. For 10YAF, 14YAF, and Control areas, herb species richness significantly differed on Big Pine with 15, 16, and 25, respectively (F 2, 22 = 5.23, P = 0.015) with Control having the highest richness (Bonferonni post hoc: P < 0.025), but did not differ on Sugarloaf (F 2, 15 = 0.78, P = 0.476) with of 6, 9, and 7, species respectively.

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Animal Biodiversity and Conservation 29.2 (2006)

B 40

Open Exclosure

Less–preferred species

30 20 10

Mean % cover

0 15

Preferred species

10 5 0

8

Grass species

6 4 2 0 Aug 01

Jan 03

Jun 03 (fire) Time

Jul 04

Fig. 3. Abundancia media (número de tallos) (! DE) de especies leñosas (A) y % de cobertura de especies herbáceas (B) en áreas cerradas y abiertas en los pinares de No Name. Hubo un incendio en junio del 2003. Para las especies leñosas, las abundancias son el resultado de la combinación de todas las clases de altura para cada categoría de preferencia de los ciervos, y las plantas se clasificaron en preferidas, menos preferidas y otras (especies de palmáceas y Byrsonima lucida). Las especies herbáceas se clasificaron como preferidas, menos preferidas y especies de hierbas (otras).

Deer exclosures and fire For both exclosures and open plots, some woody individuals (e.g., P. keyense and Myrsine floridana), that were burned and appeared dead re–flushed within two months after the fire. Though differences between time periods in abundance or percent cover were analyzed for plant data, raw data are presented in figures 3A and 3B. For the pre–fire analysis, the difference in abundance of less–preferred woody species was significantly higher in open plots than exclosure plots (t = 10.82, P = 0.008) (fig. 3A). However, the difference in woody plant abundance did not significantly differ between treatments for preferred (t = 1.37, P = 0.304) or other species (t = 3.13, P = 0.089). For post–fire analysis, the difference in abundance of less–preferred woody plant species was higher in open plots than exclosure plots (t = 6.60, P = 0.022) (fig. 3A). Difference in abundance of preferred plant species was significantly higher in exclosures than control

plots after fire (t = 8.49, P = 0.014) (fig. 3A). Palm species and Byrsonima lucida increased in both open and exclosure plots but the difference in abundance did not vary between treatments (t = 3.09, P = 0.091) (fig. 3A). Woody species richness increased inside exclosures from 15 pre–fire to 18 post–fire, but declined in open plots from 14 pre– fire to 12 post–fire.

For the pre–fire analysis, the difference in percent cover was similar between exclosure and open plots for less–preferred herbaceous species (t = 0.60, P = 0.609), preferred species (t = 4.13, P = 0.054) and grasses (t = 1.89, P = 0.198) (fig. 3B), though preferred species showed a marginal trend in difference. For post–fire analysis, the difference in percent cover of less–preferred herb species was not significant (t = 0.987, P = 0.428). The difference in percent cover did significantly vary for grasses (t = 0.753, P = 0.017) and preferred species (t = 12.33, P = 0.007). The trend of all preferred herb species was driven by Chamaecrista aspera, which

176

continually increased in cover (from 1% to 12%) and frequency (from 22% to 83%) from Aug 2001 to Jul 2004. Herb species richness increased by 2 inside exclosures and decreased by 2 in open plots from pre–fire to post–fire. Though not quantified, many herb species were observed (post–fire) flowering inside exclosures compared to open plots, and certain species were observably (post–fire) taller inside exclosures compared to open plots.

Discussion Imperiled pineland plant communities on certain islands in the NKDR are being impacted by high densities of endangered Key deer. Although Key deer densities are not directly comparable between studies (historical versus present) due to different methodologies, Big Pine and No Name have had relatively higher deer densities or incidence compared to other islands, and thus browsing impacts are presently pronounced on these two islands. Whether this impact is negative, however, remains to be seen. For example, although deer browsing is causing preferred plant species to decline in pinelands, many of these are hardwoods that are mainly associated with hammock communities. This may aid in retarding succession and maintaining open pinelands, a natural landscape pattern on Big Pine (Snyder et al., 2005) and deter heavy fuel buildup that could cause damaging fires. Also, Key deer frugivory may aid in dispersing the seeds of certain plant species, such as palms, via endozoochory. Contrarily, Key deer herbivory may have detrimental impacts on the herbaceous layer causing certain pineland associated species to remain depleted, e.g., C. aspera incidence on No Name. Our results indicate that strong browsing pressure may outweigh the benefits of fire on pineland communities, a pattern found in other herbivore–fire studies (e.g., Romme et al., 1995; Hessl, 2002).

On Big Pine and No Name, Key deer herbivory appears to have longer–term impacts on composition of woody plant species, compared to fire, as strong browsing pressure deters the establishment and growth of preferred hardwood species, while less–preferred species increase. These results negate the first null hypothesis regarding a deer effect on vegetation, regardless of fire history, over a long–term period on islands with contrasting deer densities. Though it is certainly not the rule, a lack of a fire effect on plant species composition can occur (e.g., Dix, 1960; Daubenmire, 1969; Abrahamson, 1984a). For example, in pinelands on Sugarloaf (low deer density), Folk (1991) found a relatively short–term effect (2–3 years) of fire on composition of woody plant species, though the effect of fire is lacking in the long term (> 10 YAF) as indicated in the present study. However, fire could revitalize some herbaceous species that notably suffer from heavy browsing by Key deer as evidenced from the deer exclosure study on No

Barrett & Stiling

Name. Herbaceous species tend to recover slowly after release from browsing pressure by white– tailed deer (Balgooyen & Waller, 1995), yet fire often aids in the recovery (Lay, 1956; Snyder, 1986).

For example, mean cover of C. aspera increased only slightly inside exclosures, relieved of Key deer herbivory for a 2–year period, until fire impacts caused mean cover and frequency of C. aspera to considerably increase within 2 months post–burn and remain elevated by 1 year post–burn. Yet, even after fire on No Name, mean % cover of C. aspera and other deer–favored species remained very low outside deer exclosures. These results contradict null hypothesis 3 regarding deer exclosures. Further evidence for fire–deer effects on herb species was observed on Big Pine in unburned pinelands, which had the highest herb species richness compared to other areas, thus negating null hypothesis 2. Because white–tailed deer tend to forage on herbaceous species more in burned areas (McCulloch, 1969) and Key deer frequently browse burned areas (Carlson et al., 1993; Snyder et al., 2005), unburned pinelands where Key deer browsing is not prevalent could offer a "refuge" for some herb species. On Sugarloaf, where browsing pressure is relatively much lower, however, substantial canopy cover likely limits the establishment of herbaceous species indicating that a complex interaction of fire and deer herbivory likely determines herbaceous composition and richness in NKDR pinelands.

Our study suffered from un–replicated fire treatments among islands, so our results should be viewed with caution and interpretations should mainly be limited to the three islands of study (Big Pine, Sugarloaf and No Name). However, Big Pine and No Name contain the majority of the Key deer population and the only other island with relatively extensive pineland is Little Pine, so our study does provide valuable information for NKDR biologists regarding Key deer and fire management. Furthermore, our results were consistent with other pineland vegetation studies in the NKDR. For example, Snyder et al. (2005) found that stem length, cover and richness of pineland plant species was higher in small exclosures (1 m 2) compared to open plots 1 year post–burn on Big Pine. Furthermore, we found more preferred woody species in unburned pinelands on Big Pine (again negating hypothesis 2). This result is comparable to previous vegetation surveys on Big Pine that found deer–preferred woody species in unburned pinelands (Dickson, 1955; Alexander & Dickson, 1970). However, Key deer densities on Big Pine were much lower during the studies in the 1950s and 1970s, which resulted in the presence of certain deer–preferred plant species (seedlings and trees) that are lacking from the present study, such as E. fruticosa and J. keyensis, both of which are state–listed threatened species. Impacts from high densities of Key deer on preferred species in pineland are comparable to effects on the same preferred species in other plant communities on

Animal Biodiversity and Conservation 29.2 (2006)

Big Pine and No Name (Barrett & Stiling, 2006a; Barrett et al., 2006), suggesting that the herbivore effects are not spurious. Furthermore, impacts from other herbivores are not likely as marsh rabbit populations are very small on islands they occupy and are generally not found in pinelands or near the deer exclosures on No Name (Faulhaber 2003); also insect herbivory is not considerable in pinelands (personal observation) or in other communities in the NKDR (Barrett & Stiling, 2006b).

A simple solution to managing Key deer and pinelands is likely not possible. Instead, a more comprehensive and complicated approach is required that takes into account deer–fire interactions on plant communities, species–specific responses of plants to fire, selective deer herbivory, and fire effects on deer population dynamics. Perhaps burning pinelands in small tracts of 20–40 ha when possible could (1) allow unburned areas to serve as refuges from heavy deer herbivory, (2) provide a mosaic of successional stages to potentially increase plant species diversity over the landscape, and (3) gradually establish small areas with quality food plants for deer, but (4) deter large–scale nutrient inputs that could substantially augment Key deer populations. Undoubtedly, striking a careful balance of adaptive deer management and controlled burn regimes is required in the NKDR to alleviate a potential conservation dilemma of protecting both the endangered Key deer and endangered pine rocklands.

Acknowledgements For their assistance, we thank C. Borg, J. Mott, and J. McCune. We thank P. A. Frank and the NKDR staff for providing logistical support and professional guidance. We thank R. R. Lopez for expert advice and valuable information on Key deer ecology. Special thanks to G. Huxel, G. A. Fox, S. Focardi and two anonymous reviewers for their insightful comments. U. S. Fish and Wildlife Service (permit no. 41580–03–317) supported this study. NSF grant DEB 03–15190 and the Key West Garden Club provided financial support.

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Rarity of birds in the Jaú National Park, Brazilian Amazon S. H. Borges

Borges, S. H., 2006. Rarity of birds in the Jaú National Park, Brazilian Amazon. Animal Biodiversity and Conservation, 29.2: 179–189.

Abstract Rarity of birds in the Jaú National Park, Brazilian Amazon.— The rarity patterns of 368 bird species recorded in the Jaú National Park (JNP), Brazilian Amazon, were analysed using the method of seven forms of rarity based on the interaction of geographical distribution, habitat specificity, and local population size. Rare species were identified in a wide taxonomic, ecologic and body size spectrum, indicating the complexity of distinguishing rare and common species. Birds with large populations tended to occupy several habitats in a highly significant relationship. General rarity was not correlated with body size. Birds foraging in ground, understory and antbirds (Thamnophilidae and Formicariidae), were identified as especially rare in JNP. The method of seven forms of rarity is useful as a first step in identifying rare species for conservation purposes since it considers several biological features at once.

Key words: Amazonian birds, Extinction, Rarity, Neotropical birds.

Resumen Rareza de aves en el Parque Nacional de Jaú, Amazonia Brasileña.— Los patrones de rareza de 368 especies de aves en el Parque Nacional de Jaú (PNJ), Amazonia Brasileña, fueron analizados usando el método de las siete formas de rareza basado en la interacción de distribución geográfica, especificidad de hábitat y tamaño de la población local. Las especies raras fueron identificadas según un amplio espectro taxonómico, ecológico y de tamaño del cuerpo lo que explica la complejidad de distinguir especies raras y comunes. Las aves con poblaciones grandes tienden a ocupar varios hábitats en una relación altamente significativa. No fue encontrada ninguna correlación entre rareza y tamaño del cuerpo. Las aves que forrajean en el suelo, sotobosque y hormigueros (Thamnophilidae y Formicariidae) fueron consideradas como especialmente raras en el PNJ. El método de las siete formas de rareza es útil como primer paso en la identificación de especies raras en proyectos de conservación ya que considera varias características biológicas al mismo tiempo.

Palabras clave: Aves amazónicas, Extinción, Rareza, Aves neotropicales.

(Received: 23 VI 06; Conditional acceptance: 29 XI 06; Final acceptance: 27 XII 06) Sérgio Henrique Borges, Museu Paraense Emílio Goeldi, Depto. de Zoologia, Av. Perimetral 1901/1907, 66077–530, Belém, PA, Brazil.

Current address: Fundação Vitória Amazônica, R. Estrela D’Alva, casa 07, Conjunto Morada do Sol, Aleixo, 69060–510, Manaus, AM, Brazil. E–mail: sergio@fva.org.br

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introduction Protection of ecosystems or individual species threatened by extinction are common strategies to conserve biodiversity. Protection of individual species in tropical regions is limited by the relative scarcity of natural history information. To deal with this limitation, conservation biologists identify features that make species susceptible to extinction (Terborgh, 1974; Terborgh & Winter, 1980; Arita et al., 1990).

Since rare species tend to be more susceptible to extinction (Terborgh & Winter, 1980; Dobson et al., 1995; but see Karr, 1982 for exceptions) determining the relative rarity of a particular species can be useful in defining its conservation status.

At least two complementary approaches have been adopted by researchers in the study of rarity: temporal and static (Dobson et al., 1997). The temporal approach implies monitoring populations and updating natural history information of species identified as threatened by extinction. This approach is used by conservation institutions such as IUCN and Birdlife International. The static approach uses general biological parameters to classify species into rarity categories (Dobson et al., 1997; Yu & Dobson, 2000). The static approach deals with qualitative and less–detailed biological information to identify species that require further study of their conservation status (Roma, 1996; Dobson et al., 1997).

The most popular method for the static analysis of rarity is the seven forms of rarity proposed by Rabinowitz et al. (1986), based on geographical distribution, habitat specificity and local population size. In this method, species with reduced geographic distributions, low abundance, and restricted habitat use show the highest level of rarity. In contrast, species with wide geographical distributions that use several habitats and have large populations are considered common. Researchers have considered the method of Rabinowitz et al. (1986) simple and useful and have applied it to investigate patterns of rarity in plants (Rabinowitz et al., 1986; Pitman et al., 1999), butterflies (Thomas & Mallorie, 1985), birds (Kattan, 1992; Goerk, 1995; Roma, 1996), and mammals (Yu & Dobson, 2000).

The rarity of Neotropical birds has been investigated in regions severely impacted by human activities in Colombia and Brazil (Kattan, 1992; Goerk, 1995; Roma, 1996). In this study the method of Rabinowitz et al. (1986) is applied to investigate patterns of rarity in the resident avifauna of the Jaú National Park (JNP), a region dominated by relatively undisturbed habitats. The avifauna of the region has been studied over the last 10 years (Borges et al., 2001; Borges, 2004a), providing an opportunity to investigate natural patterns of rarity.

The principal aim of this study was to investigate the rarity of birds in a specific region of the Amazon and compare the results with other studies to evaluate the generality of rarity patterns obtained in distinct ecological and geographic context in the Neotropics. The paper also analyses the importance of ecological traits of birds such as body size

Borges

and diet to determine the rarity in JNP avifauna.

These traits were chosen since they have been found to correlate with rarity and susceptibility to extinction in several studies (Terborgh, 1974; Willis, 1979; Kattan, 1992). Specifically, the following questions were asked: (1) what proportion of JNP avifauna fall into each of the rarity categories proposed by Rabinowitz et al. (1986)? (2) are rarity patterns associated with different guilds and taxonomic affiliations or are they random, or at least independent of, ecological and taxonomic groupings? (3) is there a relationship between rarity categories and the body size of birds? (4) are the patterns of rarity in JNP avifauna similar to other Neotropical sites?

Material and methods Study area Jaú National Park (JNP) covers 2,272,000 ha and is located in the central region of the Brazilian Amazon on the west bank of the lower portion of the Rio Negro (fig. 1). Several forest and non– forest vegetation types compose the complex landscape of the region which is dominated by natural or near–undisturbed vegetation (Borges et al., 2001).

Terra firme forest is the dominant vegetation in the region, covering approximately 70% of JNP (Ferreira & Prance, 1998). The next most common habitat type at JNP is igapó forest, occupying approximately 12% of the JNP area. Igapó forests are forests that are seasonally inundated by blackwater rivers and streams and the floristic composition is very distinct from terra firme forests (Ferreira, 1997).

JNP also has small areas of vegetation associated with sandy soils generally categorized as campinaranas, low–canopy woods and campinas; open fields with sparse cover of small trees (Anderson, 1981; Vicentini, 2004). Other vegetation types found at JNP include palm forests (buritizais) and a mosaic of disturbed vegetation resulting from human activities, mainly traditional agriculture.

These vegetation types occupy only a very small proportion of the JNP area.

Parameters of rarity The JNP Bird Checklist, updated with recent fieldwork, was used to examine rarity patterns (Borges et al., 2001; Borges, S. H., unpublished data).

Aquatic (e.g. herons) and migrant species were omitted from the analyses. Birds were identified to subspecies by examining geographical distributions of subspecies and comparing birds collected in the region with voucher specimens deposited in the Museu Paraense Emílio Goeldi bird collection (Borges, 2004a). The catalogues of Pinto (1944, 1978) and more recent taxonomic revisions of selected species (e.g. Isler et al., 1999; Zimmer & Whittaker, 2000; also see Borges, 2004a for a more extensive list of references) were used to classify

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Fig. 1. Mapa del Parque Nacional de Jaú (JNP), estado de Amazonas, Brasil.

specimens to subspecies. The taxonomic rank of subspecies was chosen because it more accurately depicts the geographical distributions of the taxons.

For example, the Great Tinamou (Tinamus major), a bird widely distributed in the Amazon basin, has 12 different subspecies with a much more restricted geographical distribution (Del Hoyo et al., 1992). A potential problem in using subspecies in the analysis is that future taxonomic revisions could demonstrate that some taxa considered here are not valid taxonomic entities. However, recent taxonomic studies on Neotropical birds, including some taxons analysed here, resulted in recognition of several subspecies as good species (e.g. Isler et al., 1999).

The method of seven forms of rarity requires information on geographical distribution, with species classified as either widespread or restricted; habitat specificity, with species categorized as specialists or generalists; and population size, with populations considered either large or small. For each of these parameters, the following procedure was adopted: Geographical distributions Bird species or subspecies distributed along the northwestern edge of the Amazon basin, mainly north of the Rio Amazonas and west of the Rio Negro, were classified as having a restricted geographical distribution. The range of some of these

species extends into more eastern regions of the Amazon (e.g. Roraima state in Brazil), but they are likely not found in the Guyana. Birds distributed in more than one sector of the Amazon Basin (e.g. both west and east of the Rio Negro) were considered to have a wide distribution. This classification included a few exceptions. The antwren Myrmotherula klagesi, for example, is found along the upper Rio Tapajós and lower Rio Negro and may be categorized as a widely distributed species. However, the known range of M. klagesi is very small and associated with fluvial islands (Ridgely & Tudor, 1994). The catalogues of Pinto (1944, 1978), Ridgely & Tudor (1989, 1994) and Del Hoyo et al. (1992, 1993, 1996, 1997, 1999, 2001, 2002, 2003, 2004) were used to determine the geographical distributions of bird species and sub– pecies.

Habitat specificity Bird species were classified by habitat according to information in the JNP Checklist (Borges et al., 2001). This classification was modified in some cases, according to more recent field observations. A bird species was considered a habitat specialist if it was recorded in only one habitat type; those recorded in more than one habitat type were considered generalist species. Only natural or near–undisturbed habitats were considered in this classification.

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Population size This is the hardest information to obtain due to the difficulty of quantitatively evaluating bird populations in tropical ecosystems. General classifications such as rare, infrequent, or common have been adopted in bird rarity studies (Kattan, 1992; Goerck, 1997).

The populations of bird species in JNP were categorized as large or small in a qualitative way based on a previous ten–year field study complemented with quantitative studies (Borges & Carvalhaes, 2000; Borges et al., 2004; Borges, 2004a). The absolute population size was considered. The hummingbird Polytmus theresiae, for example, is a common bird in campinas, but the population was considered small since campinas make up a very small proportion of the region, making this species rare when considering JNP as a whole.

Statistical analyses The parameters described above make–up an eight–cell matrix (table 1) into which each bird species is incorporated. Each cell in the matrix was numbered one through four indicating the vulnerability index (VI) of a species (Goerk, 1995).

The values one through three indicate whether a species is considered rare in one, two, or three of the rarity parameters. Species that are not rare in any of the three parameters received the number four, and are assumed to have low vulnerability to extinction. Rarity was analyzed considering all three parameters (global rarity), as well as considering only population size and habitat specificity (local rarity). On a local scale, a species was rare if it had a small population and used only one habitat. A G–test was used to test for dependence among the rarity parameters and separate (2 tests for pairwise comparisons among parameters (2 x 2 contingency tables). In order to examine relationships among vulnerability index and body size, bird species were classified as small (below median weight) or large (above median weight). The body size data (weight in grams) was taken from previous JNP field work or the literature (Borges, unpubl. data; Karr et al., 1990; Del Hoyo et al., 1992, 1993, 1996, 1997, 1999, 2001, 2002, 2003, 2004). Guild membership was determined by diet (e.g. frugivores, insectivores etc.) and foraging strata (ground, understory and canopy), and was based on literature (Karr et al., 1990) and personal field experience. Homogeneity tests (( 2) were used to see if birds from different guilds and families were homogeneously distributed across vulnerability categories.

Results Forms of rarity Rarity patterns of 368 bird species distributed across 40 families or subfamilies were considered in this

Borges

study (annex 1). Most species (77%) have a wide geographical distribution throughout the Amazon Basin. Approximately 83 species (23%) are restricted to the northwestern part of the Amazon basin, mostly north of the Rio Amazonas and west of the Rio Negro. Almost half (46%) the birds are restricted to only one habitat and approximately 106 (29%) were classified as having small populations. The majority of species (58%) were classified as rare in one (124 species) or two (89 species) of the three rareness measures (table 1).

One hundred and thirty–six species (37%) were classified as not rare in any of the three parameters (table 1). In contrast, only 19 species were considered rare in all three parameters.

The parameters defining rarity were not independent of each other (G = 68.11, df = 3, p < 0.01).

The geographical distribution of species was not significantly associated with population size or habitat specificity (table 2). In contrast, birds with large populations tended to occupy several habitats in a highly significant relationship (table 2).

Population size and habitat specificity determined the rarity of birds at a local scale. Accordingly, 170 species were restricted to one habitat, while 198 were habitat generalists. In terms of population size, 262 bird species had large populations and 106 small. Eighty–four species were both habitat specialists and had small populations, these being the rarest birds in JNP. The majority of the locally rare species were restricted to either igapó flooded forest (n = 37) or terra firme forest (n = 34). Few rare species were specialists of campinas (n = 8) and campinaranas (n = 5).

There was no difference in the mean weight of habitat specialists (148 ± 29 g, n = 170) and generalists (150 ± 28 g, n = 198; T value = –0.042, df = 366, P = 0.48). In contrast, birds with small populations at JNP were heavier (231 ± 59 g, n = 106) than species with large populations (116 ± 15 g, n = 262) (T value = 2.62, df = 366, P = 0.005).

Guilds and rarity patterns No significant association was found between the vulnerability index and diet of bird species in either global ((2 = 12.75, df = 12, P = 0.387) or local analyses ((2 = 0.96, df = 34, P = 0.91). In contrast, the vulnerability index was significantly associated with foraging strata ((2 = 14.87, df = 6, p = 0.02), with more ground– and understory–foraging birds falling into the highly vulnerable category (IV1) than expected by chance.

Body size was not related to vulnerability within diet categories. The mean weights of rare and common species at a local scale were not different from each other when compared within diet groups (T test, P < 0.10 for all comparisons).

Significant associations were found between population size and habitat specificity in canopy insectivores ((2 = 8.77, df = 1, P = 0.003), understory

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Table 1. Number and proportions of bird species in Jaú National Park distributed across the seven forms of rarity of Rabinovitz et al.

(1986). The numbers in parenthesis are vulnerability index.

Tabla 1. Número y porcentaje de especies de aves en el Parque Nacional de Jaú distribuidas entre las siete formas de rareza de Rabinovitz et al. (1986). Los números entre paréntesis son los índices de vulnerabilidad.

Table 2. Number of bird species of Jaú National Park distributed across rarity–defining parameters. P –values were obtained from (2 tests of independence.

Tabla 2. Número de especies de aves del Parque Nacional de Jaú distribuidas según los parámetros que definen rareza. Los valores P fueron obtenidos a través de pruebas (2 de independencia.

Rarity defining parameters Geographic distribution Wide Several

Restricted One

Several

One

Large population 136–37% (4)

67–18% (3)

40–11% 19–5% (3) (2)

Small population 17–5% (3)

65–18% (2)

5–1% (2)

Geographic distribution x habitat (P = 0.93; df = 1)

19–5% (1)

One

Several

Wide

132

153

Restricted

38

45

Geographic distribution x population (P = 0.91; df = 1) Large

Small

Wide

203

82

Restricted

59

24

Large

Small

One

86

84

Several

176

22

Habitat x population (P = 0.000; df = 1) insectivores ((2 = 63.574, df = 1, P = 0.0000), and canopy omnivores ((2 = 8.20, df = 1, P = 0.004). In all cases, species with large populations occupied several habitats and species restricted to one habitat were near–equally distributed in both large and small populations.

Taxonomic affiliation and rarity patterns Comparisons within bird families with large sample sizes (more than 20 species) showed that antbirds (Thamnophilidae and Formicariidae) had a greater number of species in the high vulnerability categories (VI 1 and 2) than expected by the general distribution ((2 = 8.51, df = 3, P = 0.03). In contrast, the flycatchers (family Tyrannidae) had more species in the low vulnerability categories (IV 3 and 4) than expected ((2 = 8.53, df = 3, P = 0.03).

Analysis at a more refined taxonomic level is constrained by the reduced sample sizes. However, the genus Myrmotherula is illustrative, as there are 10 species in the JNP region. One species (M. klagesi) was considered rare in all three parameters, four species (M. ambiqua, M. haematonota, M. multostriata, and M. assimilis) were rare in two parameters, and one species (M. cherriei) was rare in one parameter (geographical distribution). Four species (M. brachyura, M. axillaris, M. longipennis, and M. menetriesii) were classified as common in all three parameters.

No relationship was detected between body size and rarity at global or local scales in within–family analyses. Neither was there any difference in the

mean weight of rare and common species at the local scale (T test, P < 0,10 for all comparisons).

There was a strong dependence of population size on habitat specificity among the antbirds ((2 = 17, df = 1, P < 0.001), with species restricted to one habitat tending to have small populations.

The same pattern was observed in ovenbirds and woodcreepers (Furnariidae and Dendrocolaptidae) ((2 = 6.74, df = 1, P = 0.009). In this case, however, birds with high habitat specialization were near– equally distributed in large and small populations.

Discussion Rarity in Neotropical avifaunas The seven forms of rarity methodology has been applied to other Neotropical regions, including the Andean region of Colombia (Kattan, 1992), Brazilian Atlantic forest (Goerck, 1997), and eastern Amazon (Roma, 1996). Several modifications to the original methodology were made in these studies. For example, birds were identified to subspecies only in the JNP and eastern Amazon studies

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(Roma, 1996). Although these differences may influence comparability among studies, these four studies allow us to search for general patterns of rarity in Neotropical birds.

Geographical distribution, population size and habitat specificity were found to be inter–dependent in all studies. However, only in JNP was geographical distribution independent of population size and habitat specificity, suggesting that the importance of geographical distribution to define patterns of rarity in birds vary among the regions. Indeed, the proportion of species with restricted distributions was higher in the Andes (61%) and Atlantic Forest (30%) compared with JNP (23%). This pattern likely results from the fact that the geographic range of birds in the Andean region and, perhaps in Atlantic forests, tends to be narrower and defined by a highly fragmented (naturally and anthropogenic) montane landscape (Peterson & Watson, 1998). In contrast, the distribution of Amazonian birds is broadly delimited by large expanses of lowland forest subdivided by the major rivers (Peterson & Watson, 1998; Haffer, 1992).

The proportion of species with a small population is similar in the Andes (34%), the Atlantic forest (31%) and the JNP (29%). In contrast, habitat specialists are responsible for a larger proportion of species in Andes (62%) and Atlantic forest (63%) than in JNP (46%). Habitat specialists in Colombia, Atlantic Forest and eastern Amazon were birds found only in primary forests and generalists were also found in edges and secondary habitats. In the current study, all non–anthropogenic vegetation types (forest and non–forests) found in JNP were considered in habitat categorization. The differences in proportion of habitat specialists could result from distinct criteria used for setting the habitat specialization in the studies compared.

Species of the families Dendrocolaptidae, Thamnophilidae, Formicariidae and Furnariidae have been identified as especially rare in Colombia and eastern Amazon (Kattan, 1992; Roma, 1996).

In JNP, only the antbirds show a tendency towards intrinsic rarity. The flycatchers (Tyrannidae), in contrast, tend to have large populations and occupy several habitats. Bird families traditionally recognized as rare and threatened by extinction, such as Accipitridae (hawks) and Psittacidae (parrots), were not identified as especially rare in JNP, but were so in the Andes and eastern Amazon. The antwrens (genus Myrmotherula) and the tyrant flycatchers (genus Hemmitricus) are prone to rarity and highly threatened by extinction in the Atlantic forest (Goerck, 1997). In contrast, members of these genera exhibit variable levels of rarity in JNP (annex 1).

Insectivorous and frugivorous birds were disproportionately rare in the eastern Amazon, Colombia, and Atlantic Forest (Kattan, 1992; Goerck, 1997; Roma, 1996). In contrast, no relationship was found among rarity categories and feeding guilds in the JNP avifauna. Canopy omnivores had an excess of

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species in the less–vulnerable categories in eastern Amazon (Roma, 1996). This relationship was not found in the JNP avifauna, but a high number of flycatcher species, most of them canopy omnivores, also fell into less vulnerable categories of rarity (IV3 and IV4).

Body size has been identified as a good indicator of rarity in mammals (Arita et al., 1990; Dobson & Yu, 1993; Yu & Dobson, 2000). In birds, however, the relationship between body size and rarity is highly variable among taxons, guilds and scales of analyses. In this study, no correlation was found between general rarity and body size, although large birds tended to have small populations. In the eastern Amazon a significant, yet weak, correlation between body size and both global (rs = 0.127) and local (rs = 0.174) vulnerability (Roma, 1996) was found. In Colombia, rare frugivorous birds and tanagers (Thraupinae) tended to be larger than common species (Kattan, 1992).

The studies compared herein were conducted in distinct ecological zones (e.g. Andes region, Amazon lowland) with different levels of habitat degradation in a widespread Neotropical region. Although some coincident results emerge, no largely consistent patterns of bird rarity were found. Uncertainly remains whether these inconsistencies result from modifications in Rabinowitz et al.’s (1986) method or are due to inherent characteristics of different Neotropical avifaunas.

Conservation Results of this study call attention to several factors that, if focused on, may strengthen future studies of rarity in Neotropical birds. Population size is strongly associated with habitat specificity. Some of the rarest birds of JNP are found in very restricted habitats such as campinas (e.g. Polytmus theresiae, Formicivora grisea, and Schistochlamys melanopis), igapó flooded forests (e.g. Nonnula amaurocephala), or fluvial islands (e.g. Thamnophilus nigrocinereus and Myrmotherula klagesi). This finding reinforces the importance of habitat heterogeneity to regional bird distribution in the Amazon basin (Remsem & Parker, 1983; Rosenberg, 1990; Kratter, 1997; Whitney & Alvarez, 1998; Borges & Carvalhaes, 2000; Borges, 2004b). The inclusion of local vegetation heterogeneity in the sampling design for biological inventories is crucial in rarity analyses.

The taxonomic categories adopted also affect the results of rarity studies (Goerck, 1997). This is particularly relevant in the Amazon basin, where a high number of polytypical species is found and the application of Biologal Species Concept underestimates the bird species diversity (Bates et al., 1998; Bates & Demos, 2001). In these cases, geographical distributions of species can only be accurately delimited by analyzing the distributions of subspecies involved. Moreover, subspecies ranking is suggested to be useful in conservation analysis, especially in the Neotropics (Bates & Demos, 2001; Phillimore & Owens, 2005).

Animal Biodiversity and Conservation 29.2 (2006)

Rare species were singled out of a large pool of species, across a wide taxonomic, ecologic and body size spectrum. Even species in the same genus with similar diet and body size varied greatly in rarity. Such variability complicates the process of distinguishing between rare and common species.

Because it considers several biological features in conjunction, the methodology of seven forms of rarity is especially useful as a first approximation to identifying rare species for conservation purposes (Roma, 1996).

Acknowledgments Financial and logistical support for this study came from WWF–Brazil, Fundação Vitória Amazônica, and CAPES. Technicians at Fundação Vitória Amazônica, especially S. Iwanaga, C. Durigan, R. von Lira and Marcelo Moreira, provided much help throughout the study. My Ph. D. committee, A. Aleixo, M. Luiza, T. Cristina, M. A. dos S. Alves, L. P. Gonzaga, and J. M. Cardoso da Silva (adviser) reviewed an early version of the manuscript and made helpful contributions. Catherine Bechtoldt did the English proofreading.

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Annex 1. Bird species and subspecies included in the analysis of rarity of Jaú National Park avifauna distributed in Rabinovitz et al.’s seven forms of rarity of (1986). Nomenclature of species follows the recommendations of the Brazilian Ornithological Records Committee (http://www.cbro.org.br).

Annex 1. Especies y subespecies de aves incluidas en el análisis de rareza de la avifauna del Parque Nacional de Jaú agrupadas en las siete formas de rareza según Rabinovitz et al. (1986). La nomenclatura de especies sigue las recomendaciones del Comité de Registros Ornitológicos de Brasil (http://www.cbro.org.br).

Rarity form 1 Restricted geographic distribution, habitat specialists, small population sizes Crypturellus cf. duidae, Chordeiles pusillus esmeraldae, Phaethornis rupurumii amazonicus, Nonnula amaurocephala, Eubucco richardsoni nigriceps, Frederickena unduligera unduligera, Thamnophilus nigrocinereus cinereoniger, Myrmotherula klagesi, Formicivora grisea rufiventris, Myrmoborus lugubris stictopterus, Conopophaga aurita inexpectata, Formicarius analis zamorae, Grallaria varia cinereiceps, Automolus rubiginosus venezuelanus, Schiffornis major duidae, Ramphocaenus melanurus duidae, Polioptila guianensis facilis, Schistochlamys melanopis aterrima, Lanio fulvus peruvianus.

Rarity form 2 Restricted geographic distribution, habitat specialists, large population sizes Tinamus major serratus, Odontophorus gujanensis buckleyi, Nyctiprogne leucopyga latifascia, Selenidera nattereri, Picumnus lafresnayi pusillus, Veniliornis affinis orenocensis, Myrmotherula haematonota pyrrhonota, Myrmotherula ambigua, Hypocnemis cantator flavescens, Hypocnemoides melanopogon occidentalis, Hylopezus macularius diversus, Deconychura longicauda connectens, Synallaxis rutilans confinis, Todirostrum maculatum anectans, Heterocercus flavivertex, Hylophilus ochraceiceps ferrugineifrons, Microcerculus bambla albigularis, Tachyphonus surinamus brevipes, Hemithraupis flavicollis aurigularis.

Rarity form 3 Restricted geographic distribution, habitat generalists, small population sizes Topaza pyra pyra, Percnostola minor minor, Myrmeciza disjuncta, Hylexetastes stresemanni stresemani, Dolospingus fringilloides.

Rarity form 4 Wide geographic distribution, habitat specialists, small population sizes Pipile cumanensis cumanensis, Mitu tuberosum, Leptodon cayanensis cayanensis, Harpagus bidentatus, Geranospiza caerulescens caerulescens, Leucopternis melanops, Busarellus nigricollis nigricollis, Spizaetus ornatus ornatus, Leptotila rufaxilla dubusi, Touit huetii, Amazona kawalli, Deroptyus accipitrinus accipitrinus, Opisthocomus hoazin, Coccycua minuta minuta, Tapera naevia naevia, Lophostrix cristata cristata, Nyctibius aethereus longicaudatus, Nyctibius bracteatus, Lurocalis semitorquatus semitorquatus, Caprimulgus cayennensis cayennensis, Glaucis hirsutus hirsutus, Threnetes leucurus leucurus, Campylopterus largipennis largipennis, Chrysolampis mosquitus, Polytmus theresiae leuchorous, Galbula galbula, Notharchus ordii, Micromonacha lanceolata, Pteroglossus pluricinctus, Taraba major semifasciatus, Thamnophilus schistaceus heterogynus, Thamnomanes ardesiacus obidensis, Pygiptila stellaris occipitalis, Myrmotherula multostriata, Myrmotherula assimilis assimilis, Dichrozona cincta, Microrhopias quixensis microstictus, Hylophylax punctulatus punctulatus, Xiphorhynchus kienerii, Cranioleuca vulpina vulpina, Ancistrops strigilatus strigillatus, Hyloctistes subulatus subulatus, Xenops milleri, Sclerurus caudacutus brunneus, Onychorhynchus coronatus castenaui, Neopipo cinnamomea cinnamomea, Attila citriniventris, Tityra inquisitor albitorques, Pachyramphus surinamus, Phoenicircus nigricollis, Perissocephalus tricolor, Cephalopterus ornatus, Pipra filicauda filicauda, Vireolanius leucotis leucotis, Atticora melanoleuca, Eucometis penicillata penicillata, Tachyphonus phoenicius, Euphonia plumbea, Euphonia chrysopasta chrysopasta, Emberizoides herbicola sphenurus, Saltator grossus grossus, Saltator maximus maximus, Psarocolius bifasciatus yuaracares, Molothrus oryzivorus oryzivorus, Sturnella militaris militaris.

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Rarity form 5 Restricted geographic distribution, habitat generalists, large population sizes Penelope jacquacu orienticola, Psophia crepitans ochroptera, Aratinga pertinax chrysogenys, Pyrrhura melanura melanura, Brotogeris chrysoptera tenuifrons, Pionopsitta barrabandi barrabandi, Amazona autumnalis diadema, Phaethornis malaris insolitus, Thalurania furcata nigrofasciata, Momotus momota microstephanus, Pteroglossus azara azara, Thamnophilus aethiops polionotus, Thamnophilus amazonicus cinereiceps, Myrmotherula cherriei, Terenura spodioptila signata, Myrmoborus myotherinus ardesiacus, Schistocichla leucostigma infuscate, Gymnopithys leucaspis laterallis, Rhegmatorhina cristata, Hylophylax poecilinotus duidae, Phlegopsis erythroptera erythroptera, Myrmothera campanisona dissors, Xiphocolaptes promeropirhynchus orenocensis, Dendrocolaptes certhia radiolatus, Xiphorhynchus obsoletus notatus, Automolus infuscatus badius, Xenops minutus remoratus, Sclerurus rufigularis brunnescens, Todirostrum chrysocrotaphum guttatum, Zimmerius gracilipes gracilipes, Tolmomyias assimilis neglectus, Terenotriccus erythrurus venezuelensis, Cnemotriccus fuscatus duidae, Lepidothrix coronata carbonata, Hylophilus brunneiceps, Hylophilus hypoxanthus hypoxanthus, Thryothorus coraya griseipectus, Cyphorhinus arada transfluviatilis, Tangara chilensis coelicolor, Cyanerpes cyaneus dispar.

Rarity form 6 Wide geographic distribution, habitat specialists, large population sizes Crypturellus undulatus yapura, Nothocrax urumutum, Ictinia plumbea, Buteogallus urubitinga urubitinga, Ibycter americanus, Falco rufigularis rufigularis, Orthopsittaca manilata, Aratinga leucophthalma callogenys, Touit purpuratus viridiceps, Pionus fuscus fuscus, Amazona festiva festiva, Crotophaga major, Crotophaga ani, Glaucidium brasilianum ucayale, Nyctibius grandis grandis, Hydropsalis climacocerca schomburgki, Phaethornis bourcieri bourcieri, Trogon curucui peruvianus, Trogon violaceus ramonianus, Pharomachrus pavoninus pavoninus, Notharchus macrorhynchos hyperrhynchus, Notharchus tectus tectus, Monasa nigrifrons nigrifons, Chelidoptera tenebrosa tenebrosa, Campephilus rubricollis rubricollis, Sakesphorus canadensis loretoyacuensis, Cercomacra tyrannina tyrannina, Sclateria naevia argentata, Nasica longirostris, Xiphorhynchus picus picus, Berlepschia rikeri, Mionectes macconnelli macconnelli, Hemitriccus minor pallens, Camptostoma obsoletum napaeum, Phaeomyias murina wagae, Inezia subflava subflava, Tolmomyias poliocephalus poliocephalus, Platyrinchus platyrhynchos platyrhynchos, Lathrotriccus euleri lawrencei, Knipolegus poecilocercus, Pitangus sulphuratus sulphuratus, Philohydor lictor lector, Conopias trivirgatus berlepschi, Tyrannopsis sulphurea, Attila cinnamomeus, Pachyramphus castaneus saturatus, Gymnoderus foetidus,Chiroxiphia pareola regina, Hylophilus semicinereus viridiceps, Atticora fasciata, Stelgidopteryx ruficollis ruficollis, Thryothorus leucotis albipectus, Polioptila plumbea plumbea, Turdus fumigatus fumigatus, Habia rubica peruviana, Tachyphonus cristatus cristatellus, Tachyphonus luctuosus luctuosus, Ramphocelus nigrogularis, Ramphocelus carbo carbo, Thraupis palmarum melanoptera, Chlorophanes spiza caerulescens, Hemithraupis guira nigrigula, Sicalis columbiana goeldii, Paroaria gularis gularis, Psarocolius decumanus decumanus, Cacicus haemorrhous haemorhous, Lampropsar tanagrinus tanagrinus.

Rarity form 7 Wide geographic distribution, habitat generalists, small population sizes Crypturellus cinereus, Accipiter bicolor bicolor, Buteo nitidus nitidus, Harpia harpyja, Spizaetus tyrannus serus, Herpetotheres cachinnans cachinnans, Micrastur mirandollei, Micrastur semitorquatus semitorquatus, Strix huhula huhula, Asio stygius stygius, Nyctibius leucopterus, Caprimulgus rufus rufus, Chlorestes notata, Elaenia ruficeps, Myiornis ecaudatus miserabilis, Rhytipterna immunda, Pachyramphus rufus rufus.

Common species Wide geographic distribution, habitat generalists, large population sizes Crypturellus soui sou, Crypturellus variegatus, Rupornis magnirostris magnirostris, Daptrius ater, Milvago chimachima cordatus, Micrastur ruficollis concentricus, Micrastur gilvicollis, Aramides cajanea cajanea, Patagioenas speciosa, Patagioenas cayennensis cayennensis, Patagioenas plumbea wallacei, Patagioenas

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Annex 1. (Cont.)

subvinacea purpureotincta, Leptotila verreauxi brasiliensis, Geotrygon montana Montana, Ara ararauna, Ara macao macao, Ara chloropterus, Pionites melanocephalus melanocephalus, Pionus menstruus menstruus, Amazona amazonica, Amazona farinosa farinosa, Piaya cayana cayana, Piaya melanogaster melanogaster, Megascops choliba crucigerus, Megascops watsonii usta, Pulsatrix perspicillata perspicillata, Nyctibius griseus griseus, Nyctidromus albicollis albicollis, Caprimulgus nigrescens, Phaethornis ruber nigricinctus, Florisuga mellivora mellivora, Anthracothorax nigricollis, Chlorostilbon mellisugus subfurcatus, Hylocharis sapphirina, Hylocharis cyanus viridiventris, Amazilia versicolor milleri, Amazilia fimbriata fimbriata, Heliodoxa aurescens, Heliothryx auritus aurita, Heliomaster longirostris longirostris, Trogon viridis viridis, Trogon rufus sulphureus, Trogon melanurus eumorphus, Galbula albirostris chalcocephala, Galbula leucogastra, Galbula dea brunneiceps, Jacamerops aureus aureus, Bucco tamatia tamatia, Bucco capensis, Malacoptila fusca, Monasa morphoeus peruana, Capito auratus, Ramphastos tucanus cuvieri, Ramphastos vitellinus culminatus, Melanerpes cruentatus, Colaptes punctigula guttatus, Celeus grammicus grammicus, Celeus elegans jumanus, Celeus torquatus occidentalis, Dryocopus lineatus lineatus, Campephilus melanoleucos melanoleucos, Cymbilaimus lineatus intermedius, Thamnophilus murinus murinus, Megastictus margaritatus, Thamnomanes caesius glaucus, Myrmotherula brachyura brachyuran, Myrmotherula axillaris axillaries, Myrmotherula longipennis longipennis, Myrmotherula menetriesii pallida, Herpsilochmus dorsimaculatus, Cercomacra cinerascens cinerascens, Hypocnemis hypoxantha hypoxantha, Pithys albifrons peruvianus, Hylophylax naevius naevius, Formicarius colma colma, Dendrocincla fuliginosa neglecta, Dendrocincla merula bartleti, Deconychura stictolaema secunda, Sittasomus griseicapillus amazonus, Glyphorynchus spirurus rufigularis, Dendrexetastes rufigula devillei, Dendrocolaptes picumnus validus, Xiphorhynchus guttatus guttatoides, Philydor pyrrhodes, Mionectes oleagineus oleagineus, Corythopis torquatus anthoides, Hemitriccus zosterops zosterops, Hemitriccus minimus, Tyrannulus elatus, Myiopagis gaimardii guianensis, Myiopagis caniceps cinerea, Ornithion inerme, Cnipodectes subbrunneus minor, Platyrinchus coronatus coronatus, Myiobius barbatus barbatus, Legatus leucophaius leucophaius, Conopias parvus, Empidonomus varius rufinnus, Tyrannus melancholicus melancholicus, Rhytipterna simplex frederici, Myiarchus tuberculifer tuberculifer, Myiarchus ferox ferox, Ramphotrigon ruficauda, Tityra cayana cayana, Pachyramphus marginatus nanus, Cotinga cayana, Lipaugus vociferans, Laniocera hypopyrra, Xipholena punicea, Neopelma chrysocephalum, Tyranneutes stolzmanni, Piprites chloris tschudii, Xenopipo atronitens, Dixiphia pipra pipra, Pipra erythrocephala erythrocephala, Schiffornis turdina amazona, Cyclarhis gujanensis gujanensis, Hylophilus thoracicus griseiventris, Troglodytes musculus albicans, Microbates collaris collaris, Turdus albicollis phaeopygus, Coereba flaveola minima, Tangara mexicana boliviana, Tangara punctata punctata, Tangara velia iridina, Dacnis flaviventer, Dacnis cayana cayana, Cyanerpes caeruleus microrhyncha, Euphonia chlorotica amazonica, Euphonia rufiventris, Sporophila angolensis torridus, Caryothraustes canadensis canadensis, Cyanocompsa cyanoides rothschildii, Psarocolius viridis, Cacicus cela cela, Icterus chrysocephalus.

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

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Ribosomal DNA ITS–1 sequencing of Galba truncatula (Gastropoda, Lymnaeidae) and its potential impact on fascioliasis transmission in Mendoza, Argentina M. D. Bargues, R. L. Mera y Sierra, H. G. Gómez, P. Artigas & S. Mas–Coma Bargues, M. D., Mera y Sierra, R. L., Gómez, H. G., Artigas P. & Mas–Coma, S., 2006. Ribosomal DNA ITS–1 sequencing of Galba truncatula (Gastropoda, Lymnaeidae) and its potential impact on fascioliasis transmission in Mendoza, Argentina. Animal Biodiversity and Conservation, 29.2: 191–194.

Abstract Ribosomal DNA ITS–1 sequencing of Galba truncatula (Gastropoda, Lymnaeidae) and its potential impact on fascioliasis transmission in Mendoza, Argentina.— Sequencing of the rDNA ITS–1 proved that the lymnaeid snail species Galba truncatula is present in Argentina and that it belongs to the haplotype HC, the same as that responsible for the fascioliasis transmission in the human hyperendemic area with the highest human prevalences and intensities known, the Northern Bolivian Altiplano.

Key words: Galba truncatula, Lymnaeid vectors, Human and animal fascioliasis, Transmission, Mendoza, Argentina.

Resumen Secuenciación del ITS–1 del ADN ribosomal de Galba truncatula (Gastropoda, Lymnaeidae) y su impacto potencial en la transmisión de la fascioliasis en Mendoza, Argentina.— La secuenciación del ITS–1 del ADNr demostró que la especie de gasterópodo lymnaeido Galba truncatula se encuentra en Argentina y que pertenece al haplotipo HC, el mismo responsable de la transmisión de la fascioliasis en el área de hiperendemia humana con las mayores prevalencias e intensidades de fascioliasis conocidas, el Altiplano Norte Boliviano.

Palabras clave: Galba truncatula, Vectores Lymnaeidae, Fascioliasis humana y animal, Transmisión, Mendoza, Argentina.

(Received: 15 XI 06; Final acceptance: 15 I 07) M. D. Bargues, R. L. Mera y Sierra, H. G. Gómez, P. Artigas & S. Mas–Coma, Depto. de Parasitología, Fac. de Farmacia, Univ. de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot (Valencia), España (Spain).– R. L. Mera y Sierra, Fac. de Ciencias Médicas, Univ. Nacional de Cuyo, Av. Libertador 80 Centro Universitario, P. O. Box 33, 5500 Mendoza, Argentina (Argentina).

Corresponding author: M. D. Bargues. E–mail: M.D.Bargues@uv.es

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Bargues et al.

Introduction

Materials and methods

Fascioliasis is a well–known parasitic disease transmitted by freshwater snail species of the family Lymnaeidae (Gastropoda) (Mas–Coma et al., 2005). Fasciola hepatica is believed to be of European origin, with the lymnaeid Galba truncatula as the original vector species. G. truncatula is a species which reproduces by selfing and spread to other continents, most probably together with the commercial export of livestock (Mas–Coma et al., 2001).

When carrying out animal fascioliasis studies in the province of Mendoza, Argentina, Mera y Sierra (2001) collected lymnaeids which he classified as belonging to the species G. truncatula, by comparing with morphological descriptions (Oviedo et al., 1995; Samadi et al., 2000).

This was the first time that G. truncatula was cited in Argentina. Studies performed during subsequent years showed that morphology is not sufficient to differentiate lymnaeid species belonging to the so–called Galba–Fossaria group (Bargues et al., 2001; Durand et al., 2002).

Problems in morphological differentiation of lymnaeid species have already been detected in Mendoza (Mera y Sierra et al., 2005, 2006; Artigas et al., 2005).

The present paper aimed to verify the species classification of the lymnaeids collected by Mera y Sierra (2001) in Mendoza, by analysis of the complete sequence of the first internal transcribed spacer (ITS–1) of the nuclear ribosomal DNA (rDNA). This molecular marker has recently proved its usefulness in Lymnaeidae (Bargues & Mas– Coma, 2005; Bargues et al., 2006).

The rDNA ITS–1 sequence was obtained from each of 5 lymnaeid specimens collected in the locality of El Salto, province of Mendoza, Argentina. DNA extraction procedure steps were performed according to methods outlined previously (Bargues et al., 2001). Total DNA was isolated according to the phenol–chloroform extraction and ethanol precipitation method, the ITS–1 fragment was amplified by the Polymerase Chain Reaction (PCR), sequencing performed by the dideoxy chain–termination method, and sequences were aligned using CLUSTAL–W version 1.8 (Bargues et al., 2001; Mas–Coma et al., 2001). Homologies were performed using BLAST (http://www.ncbi.nlm.nih.gov/ BLAST). The following ITS–1 sequences present in GenBank were used for comparisons: Galba truncatula haplotype A (AJ243018), haplotype B (AJ296270), and haplotype C (AJ272052) (Mas– Coma et al., 2001).

Results The five ITS–1 sequences from the 5 lymnaeid specimens analyzed presented the same length of 504 base pairs (bp) and a scarcely biased GC content of 57.5%. The nucleotide sequence was in all cases the same and it is shown in table 1. The Argentinian lymnaeids presented an ITS–1 sequence showing a 99.6% similitude with the G. truncatula haplotype A (HA) from Europe. The nucleotide differences detected were only two mutations: the transition G / A in position 74 and the transversion T / G in position 75. Concerning G. truncatula haplotype B

Table 1. Complete nucleotide sequence of the first internal transcribed spacer ITS–1 of the nuclear ribosomal DNA of lymnaeids from the population of El Salto, Mendoza, Argentina.

Tabla 1. Secuencia nucleotídica completa del primer espaciador transcrito interno ITS–1 del ADN ribosomal nuclear de los lymnaeidos de la población de El Salto, Mendoza, Argentina.

1 ATCATTAACG

AGCAGCCAAC CGAGCGTTGA CTACTTTGTT GTCTCAGTCA GTCAGTCAGT

61 CAGGCCCCGC GGCGTGCACG CATGAAGCGC TGTCGCGGGG CTGTGTCCGC TTCGTCTTTC 121 GGGGTACCTA TTACTGTCCT CGATGCGACC CACGGTGACG GCTTAGAGCC CGTGTGCTCG 181 CCGGGTCGCG ACGGTTCAAA GAGTGGCCGG CTTGGCTCAG CTCGAGAGTC AGCCGGCGAC 241 CGCCCCGCCG TCGCAAAAAA ACAGGAGGTT AGTCCGGGGT ACCTATGCCC TGCCCGCGCT 301 CGCTCTCGCG CCGGCAAGGC GGTAGCTCCA GCTCGCTATT TGGCCGCGAG GTTCAAAGAG 361 ACGACCGTGC CTTAACTTGC TCTCTCCGTG GGCAACGGTC GCCGCCCCGG GCCTCCTAAA 421 ATTTCCTTTA ATAAAACGAA ATTATTTTTT 481 CGAAAAACAA

ACAAAAGTC TTAT

AAAAATGTGT GTCGGCTCGA TCGTGGCACA

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Table 2. Sequence length, nucleotide contents and differences found in the comparison of the sequences of ITS–1 of the nuclear ribosomal DNA of lymnaeid populations from Argentina and known haplotypes of Galba truncatula.

Tabla 2. Longitud, composición y diferencias nucleotídicas encontradas en la comparación de las secuencias del primer espaciador transcrito interno ITS–1 del ADN ribosomal nuclear de los lymnaeidos argentinos y los haplotipos conocidos de Galba truncatula.

G. truncatula haplotypes

Positions 75 132

GenBank Acc. No.

A

G

T

AJ243018

57.5

A

G

C

AJ296270

57.5

G

T

T

AJ272052

57.5

G

T

T

present work

Origin

Lenght

% GC

74

Spain, Portugal, Switzerland, Corsica

504 pb

57.5

HB

Morocco

504 pb

HC

Northern Bolivian Altiplano

504 pb

HC

El Salto, Mendoza, Argentina

504 pb

HA

(HB) from Morocco, the similitude was of 99.4% and a total of three mutations were detected: two transitions G / A and T / C in positions 74 and 132, respectively, and one transversion T / G in position 75 (table 2). When comparing the ITS–1 sequence of the Mendoza lymnaeid specimens with that of G. truncatula haplotype C (HC) from the Northern Bolivian Altiplano, no nucleotide differences appeared (table 2).

Discussion The present work demonstrates that the lymnaeids of Mendoza belong to G. truncatula haplotype HC. The presence of G. truncatula HC in the Andean area of Argentina represents a great potential risk of fascioliasis. The haplotype HC of this lymnaeid is the same as that responsible for transmission of the disease in the endemic area with the highest prevalences and intensities known in humans, the Northern Bolivian Altiplano (Mas–Coma et al., 1999).

Although of a somewhat lower level, prevalence and intensity situations found in other Andean areas of Peru are similar (Mas–Coma et al., 2005).

The province of Mendoza is also located in the Andean area and although the altitudes are not as high as those of hyperendemic zones in Bolivia and Peru, temperatures are similar because of the southern latitude (Fuentes et al., 1999). This suggests a high disease transmission capacity in Mendoza.

The wide ecological features of G. truncatula do allow it to come close to human settings (Mas– Coma et al., 1999). This explains why this lymnaeid is in the background of many human infections.

Moreover, G. truncatula is markedly linked to areas where livestock is present, enabling its passive transportation by domestic animals from one place to another. The disease–spreading risk in Mendoza is evident.

Acknowledgements Studies funded by Projects No. BOS2002–01978 and No. SAF2006–09278 of the Ministry of Education and Science, Madrid, and Red de Investigación de Centros de Enfermedades Tropicales–RICET (Projects No. C03/04, No. ISCIII2005–PI050574 and RD06/0021/0017, Programa de Redes Temáticas de Investigación Cooperativa), FIS, Ministry of Health, Madrid. Studies in Argentina funded by Universidad Nacional de Cuyo. Technical support provided by the Servicio Central de Secuenciación para la Investigación Experimental (SCSIE) of the Universidad de Valencia (Dr. A. Martínez).

References Artigas, P., Mera y Sierra, R. Correa, A. P., Morales, J. R., Zuriaga, M. A., Jiménez, M., Khoubbane, M., Bargues, M. D. & Mas–Coma, S., 2005.

Comparison of the conchiologic morphology of lymnaeid molluscs from eastern and western Andean slopes of the endemic zones of fasciolosis in Argentina and Chile. Acta Parasitologica Portuguesa, 12: 243–244.

Bargues, M. D. & Mas–Coma, S., 2005. Reviewing lymnaeid vectors of fascioliasis by ribosomal DNA sequence analyses. Journal of Helminthology, 79: 257–267.

Bargues, M. D., Vigo, M., Horak, P., Dvorak, J., Patzner, R. A., Pointier, J. P., Jackiewicz, M., Meier–Brook, C., & Mas–Coma, S., 2001. European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS–2 sequences. Infection, Genetics and Evolution, 1: 85–107.

Bargues, M. D., Artigas, P., Jackiewicz, M., Pointier, J. P. & Mas–Coma, S., 2006. Ribosomal DNA ITS–1 sequence analysis of European

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stagnicoline Lymnaeidae (Gastropoda). Heldia, München, 6: 29–40.

Durand, P., Pointier, J. P., Escoubeyrou, K., Arenas, J. A., Yong, M., Amarista, M., Bargues, M. D., Mas–Coma, S. & Renaud, F., 2002. Occurrence of a sibling species complex within Neotropical lymnaeids, snail intermediate hosts of fascioliasis. Acta Tropica, 83: 233–240.

Fuentes, M. V., Valero, M. A., Bargues, M. D., Esteban, J. G., Angles, R. & Mas–Coma, S., 1999. Analysis of climatic data and forecast indices for human fascioliasis at very high altitude. Annals of Tropical Medicine and Parasitology, 93: 835–850.

Mas–Coma, S., Angles, R., Esteban, J. G., Bargues, M. D., Buchon, P., Franken, M. & Strauss, W., 1999. The Northern Bolivian Altiplano: a region highly endemic for human fascioliasis. Tropical Medicine and International Health, 4: 454–467.

Mas–Coma, S., Funatsu, I. R. & Bargues, M. D., 2001. Fasciola hepatica and lymnaeid snails occurring at very high altitude in South America.

Parasitology, 123: S115–S127.

Mas–Coma, S., Bargues, M. D. & Valero, M. A., 2005. Fascioliasis and other plant–borne trematode zoonoses. International Journal for Parasitology, 35: 1255–1278.

Mera y Sierra, R. L., 2001. Distribución de

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Lymnaeidos en el sistema hidrográfico andino de la provincia de Mendoza, Argentina. Tesis de Maestría, Master Internacional en Enfermedades Parasitarias Tropicales (XIV Edición). Tutor: M. D. Bargues. Depto. de Parasitología, Fac. de Farmacia, Univ. de Valencia, 22 Junio 2001.

Mera y Sierra, R. L., Artigas, P., Abraham, C., Hynes, V., González, M., Jiménez, M., Khoubbane, M., Bargues, M. D. & Mas–Coma, S., 2005.

Conchiologic morphology of lymnaeid molluscs in the endemic zones of fasciolosisis in Mendoza province, Argentina. Acta Parasitologica Portu– guesa, 12: 313–314.

Mera y Sierra, R. L., Artigas, P. & Mas–Coma, S., 2006. Lymnaeid vectors of fascioliasis in endemic areas of Mendoza, Argentina. In: XI International Congress of Parasitology–ICOPA XI (Glasgow, UK, 6–11 August 2006): CD–ROM. Oviedo, J. A., Bargues, M. D. & Mas–Coma, S., 1995. Lymnaeid snails in the human fascioliasis high endemic zone of the Northern Bolivian Altiplano. Research and Reviews in Parasitology, 55: 35–43.

Samadi, S., Roumegoux, A., Bargues, M. D., Mas– Coma, S., Yong, M. & Pointier, J. P., 2000.

Morphological studies of lymnaeid snails from the human fascioliasis endemic zone of Bolivia.

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A new land snail from the Quaternary of Mallorca (Balearic Islands, Western Mediterranean): Darderia bellverica n. gen., n. sp.

(Gastropoda, Pulmonata, Helicodontidae) C. R. Altaba

Altaba, C. R., 2006. A new land snail from the Quaternary of Mallorca (Balearic Islands, Western Mediterranean): Darderia bellverica n. gen., n. sp. (Gastropoda Pulmonata, Helicodontidae). Animal Biodiversity and Conservation, 29.2: 195–200.

Abstract A new land snail from the Quaternary of Mallorca (Balearic Islands, Western Mediterranean): Darderia bellverica n. gen., n. sp. (Gastropoda, Pulmonata, Helicodontidae).— A new genus and species of land snail is described from pre–human paleosoils at Bellver hill in the island of Mallorca. It is a medium–sized helicodontid with 6 tight coils, dome–shaped spire, obtuse peripheral keel, eccentric umbilicus, narrow aperture inclined forward, sinuous reflected peristome, a low angular tooth, 5 infrapalatal denticles, teleoconch with many regular riblets and widely scattered hair pits, and protoconch with simple wrinkles and very thin spiral lines. This very rare species had been reported as a member of the Iberian–Maghribian Oestophora. Similar Plio–Pleistocene fossils from the Balearics and Sardinia are placed in the new genus.

This may constitute a biogeographic link within the Lindholmiolinae, now surviving at both ends of the Mediterranean basin. It remains unknown when, why or whether it became extinct.

Key words: Taxonomy, Land snail, Quaternary, fossil, Helicodontidae, Balearic Islands.

Resumen Un nuevo caracol terrestre del cuaternario de Mallorca (islas Baleares, Mediterráneo occidental): Darderia bellverica gen. n., sp. n. (Gastropoda, Pulmonata, Helicodontidae).— Se describe un nuevo género y especie de caracol terrestre de paleosuelos prehumanos de la colina de Bellver en la isla de Mallorca. Se trata de un helicodóntido de talla media con 6 vueltas apretadas, espira abovedada, quilla periférica obtusa, ombligo excéntrico, apertura inclinada hacia delante, peristoma sinuoso reflejado, un diente angular bajo, 5 dentículos infrapalatales, teleoconcha con muchas costillitas regulares y depresiones de pelos muy dispersas, y protoconcha con arrugas simples y líneas espirales muy finas. Esta rarísima especie se había dado a conocer como un miembro del género ibero–magrebí Oestophora. Algunos fósiles semejantes del pliopleistoceno de las Baleares y Cerdeña se asignan al nuevo género. Éste podría constituir un enlace biogeográfico en el seno de Lindholmiolinae, que sobrevive hoy a ambos extremos de la cuenca mediterránea. Se desconoce cuándo, por qué o si realmente se extinguió.

Palabras clave: Taxonomía, Caracol terrestre, Cuaternario, fósil, Helicodontidae, Islas Baleares.

(Received: 27 XI 06; Conditional acceptance: 23 I 07; Final acceptance: 8 II 07) Cristian R. Altaba, Lab. of Human Systematics, Univ. de les Illes Balears, 07071 Palma de Mallorca, Balearic Islands (Spain).

ISSN: 1578–665X

© 2006 Museu de Ciències Naturals

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Introduction The Mediterranean islands stand apart from other archipelagoes in the exceedingly low rate of known extinctions for most taxa during the Holocene, particularly among land snails (Altaba, 2004). Only one instance is known outside the Balearics, this being in Santorini, where a historical volcanic eruption wiped out the island’s ecosystems (Riedel & Norris, 1987).

The Quaternary of the Balearic Islands is known from numerous well–preserved sites, often involving extensive stratigraphic sequences with abundant molluscan remains (Cuerda, 1989). Land snails are common in terrigenous sediments, and provide a valuable tool to understand the evolution of the native fauna (Gasull, 1972; Altaba, 1993). In the early Pleistocene, a remarkably diverse fauna lived in the southern group (Eivissa and Formentera), also known as the Pytiusic Islands (Paul, 1984; Paul & Altaba, 1992). A mass extinction event left a depauperate biota and the ecological conditions changed towards those of oceanic islands (Alcover et al., 1994). In the northern group (Mallorca and Menorca, also known as the Gymnesics), there is no evidence of such a radical change, and the pre– human fauna largely survived throughout the Quaternary (Cuerda, 1989; Altaba, 1993).

Throughout the Balearics, the most recent levels (Wurmian, or last glacial) contain the extant native land snail species, plus a few that apparently became extinct in the postglacial or even the Holocene. Among these extinctions, a few Pytiusic endemics were probably extirpated through the ecological changes triggered by human occupation. In the northern island group, only two species in these top layers have stratigraphic value because they appear to be missing today; one belonging to the family Hygromiidae and one to the Enidae likely disappeared before the arrival of humans (Cuerda, 1959; Gasull, 1964; Altaba, in press). In this paper a third Gymnesic extinct land snail species,, which apparently existed in Mallorca until the latest Pleistocene, is described.

Material and methods A shell exhibiting distinctive traits was found by Lluís Gasull in 1963, at a roadcut in the outskirts of the city of Palma. The building of new houses in the hillside near the castle of Bellver exposed a late Pleistocene paleosoil where this whitened shell had been preserved within a matrix of hardened clay.

Two other specimens were found at a comparable site in Mallorca’s northern coast. All three were identified as Oestophora barbula (Rossmässler, 1838), providing the only reports of this species in the Balearic archipelago (Gasull, 1963; Cuerda, 1989). Remarkably, O. barbula lives in the western half of the Iberian Peninsula (an area subject to strong climatic influence from the Atlantic ocean), but this has not prevented mentioning the fossils from Mallorca as proof of a previously wider distribution for this species (Puente, 1996). Outside of

Altaba

Atlantic drainages, O. barbula has its easternmost stations in an isolated locality in the Pyrenees in northwestern Aragon (Prieto, 1986). The species has also been collected at three sites in the mountains of easternmost Andalusia and southwestern Murcia (Hidalgo, 1875; Ortiz de Zárate, 1962; Gasull, 1975).

These stations are located in subdesertic areas, and the specimens found there (not studied by Puente, 1996) cannot be adscribed to this species (unpubl. obs. on the Gasull specimens). O. barbula was also mentioned from northeastern Catalonia (Ortiz de Zárate, 1962), but this was based on a single shell purportedly collected in a well–known area (Banyoles), thus constituting an obviously erroneous record. This taxon has never been found alive anywhere in the Balearics, and it is unlikely that it could survive under the Mediterranean conditions prevailing there since the Pliocene. The identity of the Mallorcan specimens was questioned in the context of the fossil land snail fauna found in the Pytiusics (Paul & Altaba, 1992), but as no further studies have been reported, the biogeographic puzzle remains.

The Gasull collection was donated by his widow to the Museu de Zoologia in Barcelona (MZB, now part of the Museu de Ciències Naturals de la Ciutadella). A partial revision of the materials housed in this collection revealed two further specimens of the same species. They were collected in 1965 at a roadcut very close to the intial finding, and although fragile, they exhibit a remarkably fine state of preservation. These two specimens collected near Bellver remained well kept and catalogued, yet unstudied for four decades.

Prior to revising their identity, these shells had to be better cleaned. Initially some loose clay was removed after immersion in water for three days.

However, in order to eliminate the hardened clay covering the aperture and much of the delicate shell surface, they were subsequently treated with ultrasound for short intervals, with careful rinsing at every step. Given the fragility of the specimens, this procedure caused some mechanical damage. The cleaning process was halted as soon as the diagnostic traits were clearly visible, and before the damage became extensive.

Extensive collecting in a large number of Quaternary sites throughout the Balearics during the last 15 years has not yielded a single specimen of this species. The area around Bellver is now completely built up, and there are no remnants available of the fossiliferous paleosoils mentioned by Gasull. The other specimens mentioned by Gasull (1963) and Cuerda (1989) were housed in the Cuerda collection, now partially kept at the Societat d’Història Natural de les Balears in Palma, but they have not been located. Thus, only the two specimens in Barcelona have been studied.

In the absence of anatomical data, the assessment of taxonomic affinities for a gastropod fossil needs to be based solely on the preserved shell.

Careful preparation and detailed observation appear to have been absent from the early identifications by Gasull and Cuerda. However, this shortcoming was

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Fig. 1. Holotype of Darderia bellverica, n. gen., n. sp. from Bellver in Mallorca (MZB 84–6550A).

Maximum diameter is 10.1 mm. Not shown are tiny remnants of encrusted hardened soil on the spire and within the umbilicus, and a crevice in the lower surface.

Fig. 1. Holotipo de Darderia bellverica, gen. n., sp. n. de Bellver en Mallorca (MZB 84–6550A). Su diámetro máximo es de 10,1 mm. No se muestran los pequeños restos de suelo endurecido incrustados sobre la espira y en el interior del ombligo, ni una grieta en la superficie inferior.

due mostly to the limited equipment available to these scientists working in severely adverse conditions.

Their merit remains, highlighted by their explorations, findings and patient gathering of data and specimens.

Results The two specimens studied are very similar to each other and differ from any extant or fossil species.

The general shape, sculpture and aperture traits confirm it is a helicodontid. This group of land snails includes several genera with one or a few species each (Hesse, 1918; Germain, 1930; Gittenberger, 1968; Schileyko, 1991; Prieto et al., 1993; Arrébola et al., 2006). The group is considered here as a family of Helicoidea, following the phylogenetic analysis of Steinke et al. (2004) and the classification proposed by Nordsieck (1987) and Bouchet & Rocroi (2005). Being unable to fit the Mallorcan fossils into any known taxon below the family level, they are herewith described as a new genus and species.

Phyllum Mollusca Cuvier, 1795 Classis Gastropoda Cuvier, 1795 Ordo Pulmonata Cuvier in Blainville, 1814 Superfamilia Helicoidea Rafinesque, 1815 Familia Helicodontidae Kobelt, 1904 Darderia, n. gen.

Diagnosis A medium–sized helicodontid with about 6 tumid, tightly coiled whorls, dome–shaped spire, shallow but incised suture, obtuse peripheral keel, and moderately wide, slightly eccentric umbilicus; aperture inclined forward, narrow and oblique trapezoidal,

with low angular tooth and sinuous, reflected, thickened peristome preceded by a conspicuous constriction and carrying 1–5 infrapalatal denticles of various shapes and orientation; teleoconch with numerous strong, regular, backwardly curving riblets, becoming obsolete on the lower side, and very thin, dense longitudinal lines and widely scattered hair pits in between; protoconch with simple wrinkles reminiscent of the teleoconch riblets and very thin spiral lines.

Darderia has a general habitus similar to Oestophora Hesse, 1907, but differs in having much more developed apertural armature, protoconch microsculpture lacking distinctive spiral incised lines, and showing hair pits in the teleoconch. Other helicodontid genera have very different aperture and/or spire.

Species included Darderia bellverica sp. nov. from the late Pleistocene of Mallorca, and D. dentata (Paul, 1984) from the Plio–Pleistocene of the Balearic Islands and perhaps Sardinia (see below).

Etymology In memory of Emili Darder i Cànaves, mayor of Palma from 1933 to 1937. A physician and a politician, he introduced tremendous improvements in public health, education, culture, water supply, housing and labor conditions. He was imprisoned and murdered at the onset of the Spanish Civil War in the Bellver castle, very close to the site where the type specimens were found.

Darderia bellverica n. sp.

Description Shell (fig. 1) lenticular, of about 1 cm maximum diameter. The spire is low dome–shaped and con-

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Altaba

sists of six somewhat tumid, tightly coiled whorls separated by a distinctly incised yet shallow suture; the last whorl is slightly descending and thus appears narrower in top view; the periphery is keeled, forming an obtuse angle somewhat above the middle of the last whorl. The umbilicus is moderately wide, spanning 1/8 of the maximum diameter; it is conic and slightly eccentric, especially so by the last whorl.

The aperture is inclined forward, forming an angle of about 50º with the coiling axis; it is preceded by a marked constriction, and is narrow and oblique, having a trapezoidal shape; it is armed with a low angular tooth and several palatal denticles: two basally fused into a nearly lamellar structure just under the peripheral keel; one prominent at the lower angle, a small one between the previously mentioned, and a more bulky, blunt, forward protuding thickening at the lower angle.

The peristome is rather sinuous, well reflected, and conspicuously thickened.

The teleoconch surface is covered by a dense sculpture consisting of numerous strong, regular, backwardly curving riblets; these become obsolete on the lower side, especially in the end 3/4 of the last whorl; in between , there is a very fine sculpture of longitudinal lines and widely scattered hair pits. The protoconch has one whorl and is ornamented with two kinds of surface sculpture: radial, backwardly curving, simple wrinkles reminiscent of the teleoconch riblets, but lower and more inclined; and very thin spiral lines, some of which are fused into very fine ridges on the outer side.

Range Known only from the island of Mallorca, in the west–central part of the Serra de Tramuntana mountain range and its southern foothills at Serra de na Burguesa, near Palma.

Type material Holotype (MZB 84–6550A) and paratype (MZB 84–6550B) in the malacological collection of the Museu de Ciències Naturals de la Ciutadella, in Barcelona. The paratype is almost identical to the holotype, although it has a slightly less developed basal tooth, and has a narrow fracture in the last whorl.

Discussion

Type locality Late Pleistocene paleosoil near the surface, at the crossroad of Andrea Doria and Son Armadans streets, near the main entrance to the park of Bellver forest, in Palma de Mallorca (Balearic Islands, Spain); 15 II 1965; L. Gasull, col. UTM 31S DD 6780; 35 m a.s.l.

Etymology The species name is derived from Bellver ("lovely sight"), a hill overlooking the city of Palma from the southwest and crowned by a round gothic castle.

The castle and surrounding forest became a public property and park under Darder’s administration.

Common names It is proposed to call this species "Darder’s toothed snail" in English, "caracol dentado de Darder" in Spanish, and "caragol denticulat d’en Darder" in Catalan.

Comparison with similar taxa Darderia bellverica n. sp. cannot be confused with any of the living or fossil species of land snails known in the Balearics. Likewise, there is no clear similarity to any species known from the neighboring mainland, including various restricted– range helicodontid species (Gasull, 1975; Altaba, 1991; Puente et al., 1998; Martínez–Ortí & Robles, 2003). It is only similar to the fossil Oestophora dentata Paul, 1984 from the island of Eivissa (Paul, 1984). Although this species has a different shape and apertural traits, and is slightly larger, it shares various traits with the new species such as the inclined aperture and microsculpture. Therefore, it is proposed to transfer O. dentata into the new genus, as Darderia dentata (Paul, 1984).

Older fossils from Menorca, attributed to the genus Oestophora and presumed to be of Messinian age (Quintana, 1995), although incompletely known and possibly dating from the Plio–Pleistocene, can be attributed to D. dentata. The specimens identified as Oestophora from the Quaternary of Sardinia (Esu, 1978 also) probably belong to Darderia, and can be assigned with caution to D. dentata. However, this adscription is only tentative, given the fragmentary nature of the Sardinian materials (not studied here).

A point needs to be made about the decision to create a new genus and species for the Mallorcan specimens. They cannot be placed within any known species, either Recent or fossil, without stretching the morphological variation of the recipient taxon far beyond the limits known in extant species. Likewise, the new species cannot be allocated into any of the currently recognized genus–level taxa, without considerably blurring the definition of the existing taxonomy. Describing a new genus is not convenient simply because its hypothesized relationships are not with Oestophora or any other superficially similar taxa.

The dilemma between multiplying genera and moving species among existing genera is not a purely nomenclatural problem, but a fundamental issue if our goal is to know the history of life through a coherent, logical classification based on monophyletic groupings (Cela–Conde & Altaba, 2002). The description of a new genus and species appears herewith justified under the premises of building a taxonomy that aims at reflecting cladistic relationships and being phylogenetically informative. The overall shape of Darderia bellverica is intriguingly reminiscent of Lindholmiola Hesse, 1931, a taxonomically iso-

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lated helicodontid genus comprising several species from the Eastern Mediterranean region. The only other genus belonging to the Lindholmiolinae Schileyko, 1978, is Atenia Gittenberger, 1968, a rare, monotypic endemic of eastern Iberia, whose aspect and aperture are quite distinctive and unusual. Nevertheless, the protoconch miscrosculpture of Atenia (Martínez–Ortí, 2006) is apparently identical to that of Darderia, probably indicating phylogenetic proximity. Indeed, the low angular tooth of Darderia, a feature absent from other helicodontids, could be homologous to the parietal lip of Atenia. The latter feature is a homoplasy (Gittenberger, 1968) shared with Trissexodon Pilsbry, 1895, which belongs to a different subfamily, the Trissexodontinae (Nordsieck, 1987). However, the parietal lip of Trissexodon is continuous with and can be interpreted as a prolongation of its flaring peristome.

Thus, the mere presence of a parietal tooth or lip may have a low phylogenetic value; yet, the existence of such an armature extending from the angular area, in addition to the protoconch characters, may indicate a common ancestry of Atenia and Darderia within the Lindholmiolinae.

The biogeographic position of Darderia bellverica in Mallorca, and of D. dentata in older sites in Eivissa, Menorca and (if it is the same species) Sardinia, may not be as puzzling as previously thought. Their probable relatedness to the living Lindholmiolinae might fill a geographic gap between the two genera currently placed in this subfamily and living at opposite ends of the Mediterranean basin. If this systematic position is correct, Darderia may have its origin in the continental fauna present in the Balearic Promontory when it became detached from the Corso–Sardinian block. This area was located 30 My ago between the Iberian eastern edge and the Alps, prior to the formation of the current complex geography of the eastern Mediterranean. This biogeographic centrality would be in accordance with the patterns observed in other ancient taxa with limited dispersal abilities (Paul & Altaba, 1992; Oosterbroek & Arntzen, 1992; Altaba, 1998; De Jong, 1998).

Whether Darderia bellverica is still extant is open to further explorations. In spite of intense searches throughout the Balearics during the last 30 years, it has not been found live anywhere.

However, the profound ecological changes that have taken place in Mallorca during the Holocene and especially in recent decades (Altaba & Ponsell, 2001) may have pushed it into remote refugia. It is conceivable that this little snail followed the path of the ferreret, or Balearic midwife toad (Alytes muletensis Sanchiz & Adrover, 1977), an endemic with a long history of isolation that was first discovered as a fossil and survives only in a few inaccessible canyons (Hemmer & Alcover, 1984; Altaba, 1997). To date D. bellverica has been found only in rugged terrain, and Paul (1984) considered the traits of D. dentata to indicate a humid environment.

Acknowledgements I am indebted to Francesc Uribe and all the staff at the Museu de Ciències Naturals de la Ciutadella in Barcelona for allowing me to study their malacological collection. José Ramón Arrébola Burgos kindly answered questions about Iberian and North African helicodontids.

References Alcover, J. A., McMinn, M. & Altaba, C. R., 1994.

Eivissa: A Pleistocene Ocean–like Island in the Mediterranean. National Geographic Research and Exploration, 10: 236–248.

Altaba, C. R., 1991. Mol.luscs. In: Història Natural dels Països Catalans, vol. 8: Invertebrats no artròpodes: 375–416, 427–470 (C. R. Altaba & J. Ros, Eds.). Enciclopèdia Catalana, Barcelona.

– 1993. Els caragols i llimacs terrestres (Mollusca: Gastropoda). In: Història natural de l’Arxipèlag de Cabrera: 409–426 (J. A. Alcover, J. Fornós & E. Ballesteros, Eds.). Editorial Moll & C.S.I.C., Palma de Mallorca.

– 1997. Phylogeny and biogeography of midwife toads (Alytes, Discoglossidae): a reappraisal.

Contributions to Zoology, 66: 257–262.

– 1998. Testing vicariance: melanopsid snails and Neogene tectonics in the Western Mediterranean. Journal of Biogeography, 25: 541–551.

– 2004. La biodiversitat de les Illes Balears: un paradigma per a la conservació. Biodiversity of the Balearic Islands: A paradigm for conservation. In: Jornades sobre biodiversitat i conservació biològica / Seminar on biodiversity and conservation: 169– 188, 371–389 (M. Vilà, F. Rodà & J. Ros, Eds.).

Institut d’Estudis Catalans, Barcelona.

– In press. A new genus and species of Enidae (Gastopoda: Pulmonata) from the Quaternary of the Balearic Islands (Western Mediterranean).

Zootaxa.

Altaba, C. R. & Ponsell, C., 2001. Tourism and biodiversity: the Balearic experience. In: Calpe 2000: Linking the fragments of paradise: 125– 132 (J. Cortes, Ed.). Gibraltar Ornithological and Natural History Society & UK Overseas Territories Conservation Forum.

Arrébola, J. R., Prieto, C., Puente, A. I. & Ruiz, A., 2006. Hatumia, a new genus for Oestophora riffensis Ortiz de Zárate, 1962, Oestophora cobosi Ortiz de Zárate, 1962 and Hatumia pseudogasulli n. sp. (Pulmonata: Helicoidea: Trissexodontidae).

Journal of Conchology, 3: 119–134.

Bouchet, P. & Rocroi, J.–P., 2005. Classification and nomenclator of gastropod families.

Malacologia, 47: 1–397.

Cela–Conde, C. & Altaba, C. R., 2002. Multiplying genera versus moving species: a new taxonomic proposal for the family Hominidae. South African Journal of Science, 98: 1–4.

Cuerda Barceló, J., 1959. Presencia de Mastus pupa, Bruguière en el tirreniense de las Baleares

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orientales. Boletín de la Sociedad de Historia Natural de Baleares, 5: 45–50, lám. iv.

Cuerda, J., 1989. Los tiempos cuaternarios en Baleares. 2nd ed. Conselleria de Cultura, Educació i Esports, Govern Balear, Palma de Mallorca.

De Jong, H., 1998. In search of historical biogeographic patterns in the western Mediterranean terrestrial fauna. Biological Journal of Linnean Society, 65: 99–164.

Esu, D., 1978. La malacofauna continentale pliopleistocenica della formazione fluvio–lacustre di Nuraghe Su Casteddu (Sardegna orientale) e sue implicazioni paleogeografiche. Geologica romana, 17: 1–34 Gasull, L., 1963. Un nuevo molusco terrestre fósil para la fauna cuaternaria de Baleares. Oestophora (id.) Barbula Charp. Boletín de la Sociedad de Historia Natural de Baleares, 9: 81–82.

– 1964. Las Helicella (Xeroplexa) de Baleares (Gasteropoda Pulmonata). Boletín de la Sociedad de Historia Natural de las Baleares, 10: 3–70, láms. i–ix.

– 1972. L’insularité des îles Baléares du point de vue de la malacologie terrestre. Rapports et Communications internationaux sur la Mer Méditérranéenne, 20: 553–557.

– 1975. Fauna malacológica terrestre del sudeste ibérico. Boletín de la Sociedad de Historia Natural de Baleares, 20: 1–155.

Germain, L., 1930. Mollusques terrestres et fluviatiles. Première partie. Faune de France, 21: 1–477.

Gittenberger, E., 1968. Zur Systematik der in die Gattung Trissexodon Pilsbry (Helicidae, Helicodontinae) gerechneten Arten. Zoologische Mededelingen, 43: 165–172.

Hemmer, H. & Alcover, J. A. (Eds.), 1984. Història biològica del ferreret. Moll, Ciutat de Mallorca.

Hesse, P., 1918. Die subfamilia Helicodontidae.

Nachrichtsblatt der Deutsche Malakolozoologische Gessellschaff, 50: 99–110.

Hidalgo, J. G., 1875. Catálogo iconográfico y descriptivo de los moluscos terrestres de España, Portugal y las Baleares, IV. S. Martínez, Madrid.

Martínez–Ortí, A., 2006. New anatomical data on the Iberian endemic Atenia quadrasi (Hidalgo, 1885) (Pulmonata, Helicodontidae). Journal of Conchology, 39: 55–60.

Martínez–Ortí, A. & Robles, F., 2003. Moluscos continentales de la Comunidad Valenciana.

Conselleria de Territori i Habitatge, Generalitat Valenciana, València.

Nordsieck, H., 1987. Revision des Systems der Helicoidea (Gastropoda: Stylommatophora).

Altaba

Archiv für Molluskenkunde, 118: 9–50.

Ortiz de Zárate, A., 1962. Observaciones anatómicas y posición sistemática de varios Helícidos españoles. V. Género Oestophora Hesse, 1907.

Boletín de la Real Sociedad Española de Historia Natural (Biología), 60: 81–104.

Oosterbroek, P. & Arntzen, J. W., 1992. Area– cladograms of Circum–Mediterranean taxa in relation to Mediterranean palaeography. Journal of Biogeography, 19: 3–20.

Paul, C. R. C., 1984. Pleistocene non–marine molluscs from Cova de Ca Na Reia, Eivissa. Bolletí de la Societat d’Història Natural de les Balears, 28: 95–114.

Paul, C. R. C. & Altaba, C. R., 1992. Els mol.luscs terrestres fòssils de les Illes Pitiüses. Bolletí de la Societat d’Història Natural de les Balears, 34: 141–170.

Prieto, C. E., 1986. Estudio sistemático y biogeográfico de los Helicidae sensu Zilch, 1959–1960 (Gastropoda: Pulmonata: Stylommatophora) del País Vasco y regiones adyacentes. Tesis doctoral, Univ. del País Vasco.

Prieto, C. E., Puente, A. I., Altonaga, K. & Gómez, B. J., 1993. Genital morphology of Caracollina lenticula (Michaud, 1831), with a new proposal of classification of Helicodontoid genera (Pulmonata: Hygromioidea). Malacologia, 35: 63–77.

Puente, A. I., 1996. El género Oestophora Hesse 1907 en la Península Ibérica. Archiv für Molluskenkunde, 126: 81–107.

Puente, A. I., Altonaga, K., Prieto, C. E. & Ruiz, J. C., 1998. Los géneros Gasulliella Gittenberger 1980, Mastigophallus Hesse 1918, Oestophorella Pfeffer 1929 y Trissexodon Pilsbry 1894 en la Península Ibérica (Gastropoda: Pulmonata: Helicoidea: Hygromiidae: Trissexodontinae).

Archiv für Molluskenkunde, 127: 43–55.

Quintana, J., 1995. Fauna malacológica asociada a Cheirogaster gymnesica (Bate, 1914).

Implicaciones biogeográficas. Bolletí de la Societat d’Història Natural de les Balears, 38: 95–119.

Riedel, A. & Norris, A., 1987. An undescribed species of Zonites from the Island of Santorini, Greece. Journal of Conchology, 32: 377–378, Schileyko, A. A., 1991. Taxonomic status, phylogenetic relations and system of the Helicoidea sensu lato (Pulmonada). Archiv für Molluskenkunde, 120: 187–236.

Steinke, D., Albrecht, C. & Pfenninger, M., 2004.

Molecular phylogeny and character evolution in the western Palaearctic Helicidae s. l.

(Gastropoda: Stylommatophora). Molecular Phylogenetics and Evolution, 32: 724–734.

Animal Biodiversity and Conservation 29.2 (2006)

I

Animal Biodiversity and Conservation

Manuscrits

Animal Biodiversity and Conservation (abans Miscel·lània Zoològica) és una revista inter­disciplinària publicada, des de 1958, pel Museu de Zoologia de Bar­ celona. Inclou articles d'inves­tigació empírica i teòrica en totes les àrees de la zoologia (sistemàtica, taxo­nomia, morfo­logia, biogeografia, ecologia, etologia, fisiologia i genètica) procedents de totes les regions del món amb especial énfasis als estudis que d'una manera o altre tinguin relevància en la biología de la conservació. La revista no publica catàlegs, llistes d'espècies o cites puntuals. Els estudis realitzats amb espècies rares o protegides poden no ser acceptats tret que els autors disposin dels permisos corresponents. Cada volum anual consta de dos fascicles.

Animal Biodiversity and Conservation es troba registrada en la majoria de les bases de dades més importants i està disponible gratuitament a internet a http://www.bcn.cat/ABC, de manera que permet una difusió mundial dels seus articles.

Tots els manuscrits són revisats per l'editor execu­ tiu, un editor i dos revisors independents, triats d'una llista internacional, a fi de garantir–ne la qualitat. El procés de revisió és ràpid i constructiu. La publicació dels treballs acceptats es fa normalment dintre dels 12 mesos posteriors a la recepció.

Una vegada hagin estat acceptats passaran a ser propietat de la revista. Aquesta es reserva els drets d’autor, i cap part dels treballs no podrà ser reproduïda sense citar–ne la procedència.

Els treballs seran presentats en format DIN A­–4 (30 línies de 70 espais cada una) a doble espai i amb totes les pàgines numerades. Els manus­crits han de ser complets, amb taules i figures. No s'han d'enviar les figures originals fins que l'article no hagi estat acceptat.

El text es podrà redactar en anglès, castellà o català. Se suggereix als autors que enviïn els seus treballs en anglès. La revista els ofereix, sense cap càrrec, un servei de correcció per part d'una persona especialitzada en revistes científiques. En tots els casos, els textos hauran de ser redactats correctament i amb un llenguatge clar i concís. La redacció del text serà impersonal, i s'evitarà sempre la primera persona.

Els caràcters cursius s’empraran per als noms científics de gèneres i d’espècies i per als neologis­ mes intraduïbles; les cites textuals, independentment de la llengua, seran consignades en lletra rodona i entre cometes i els noms d’autor que segueixin un tàxon aniran en rodona.

Quan se citi una espècie per primera vegada en el text, es ressenyarà, sempre que sigui possible, el seu nom comú.

Els topònims s’escriuran o bé en la forma original o bé en la llengua en què estigui escrit el treball, seguint sempre el mateix criteri.

Els nombres de l’u al nou, sempre que estiguin en el text, s’escriuran amb lletres, excepte quan precedeixin una unitat de mesura. Els nombres més grans s'escriuran amb xifres excepte quan comencin una frase.

Les dates s’indicaran de la forma següent: 28 VI 99; 28, 30 VI 99 (dies 28 i 30); 28–30 VI 99 (dies 28 a 30).

S’evitaran sempre les notes a peu de pàgina.

Normes de publicació Els treballs s'enviaran preferentment de forma electrònica (abc@bcn.cat). El format preferit és un document Rich Text Format (RTF) o DOC que inclo­ gui les figures (TIF). Si s'opta per la versió impresa, s'han d'enviar quatre còpies del treball juntament amb una còpia en disquet a la Secretaria de Redacció.

Cal incloure, juntament amb l'article, una carta on es faci constar que el treball està basat en investiga­ cions originals no publicades anterior­ment i que està sotmès a Animal Biodiversity and Conservation en exclusiva. A la carta també ha de constar, per a aquells treballs en que calgui manipular animals, que els autors disposen dels permisos necessaris i que compleixen la normativa de protecció animal vigent.

També es poden suggerir possibles assessors.

Quan l'article sigui acceptat, els autors hauran d'enviar a la Redacció una còpia impresa de la versió final acompanyada d'un disquet indicant el progra­ ma utilitzat (preferiblement en Word). Les proves d'impremta enviades a l'autor per a la correcció, seran retornades al Consell Editor en el termini de 10 dies. Aniran a càrrec dels autors les despeses degudes a modificacions substancials introduïdes per ells en el text original acceptat.

El primer autor rebrà 50 separates del treball sense càrrec a més d'una separata electrònica en format PDF. ISSN: 1578–665X

Format dels articles Títol. El títol serà concís, però suficientment indicador del contingut. Els títols amb desig­nacions de sèries numèriques (I, II, III, etc.) seran acceptats previ acord amb l'editor.

Nom de l’autor o els autors.

Abstract en anglès que no ultrapassi les 12 línies mecanografiades (860 espais) i que mostri l’essència del manuscrit (introducció, material, mètodes, resultats i discussió). S'evitaran les especulacions i les cites bibliogràfiques. Estarà encapçalat pel títol del treball en cursiva.

Key words en anglès (sis com a màxim), que orientin sobre el contingut del treball en ordre d’importància.

Resumen en castellà, traducció de l'Abstract. De la traducció se'n farà càrrec la revista per a aquells autors que no siguin castellano­parlants.

Palabras clave en castellà.

Adreça postal de l’autor o autors.

(Títol, Nom, Abstract, Key words, Resumen, Pala­ bras clave i Adreça postal, conformaran la primera pàgina.)

© 2006 Museu de Ciències Naturals

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Introducción. S'hi donarà una idea dels antecedents del tema tractat, així com dels objectius del treball.

Material y métodos. Inclourà la informació pertinent de les espècies estudiades, aparells emprats, mèto­ des d’estudi i d’anàlisi de les dades i zona d’estudi.

Resultados. En aquesta secció es presentaran úni­ cament les dades obtingudes que no hagin estat publicades prèviament.

Discusión. Es discutiran els resultats i es compa­ raran amb treballs relacionats. Els sug­geriments de recerques futures es podran incloure al final d’aquest apartat.

Agradecimientos (optatiu).

Referencias. Cada treball haurà d’anar acompanyat de les referències bibliogràfiques citades en el text.

Les referències han de presentar–se segons els models següents (mètode Harvard): * Articles de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe­ cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Llibres o altres publicacions no periòdiques: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Treballs de contribució en llibres: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva­ tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.).

Oxford University Press, Oxford. * Tesis doctorals: Merilä, J., 1996. Genetic and quantitative trait vari­ ation in natural bird populations. Tesis doctoral, Uppsala University. * Els treballs en premsa només han d’ésser citats si han estat acceptats per a la publicació: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

La relació de referències bibliogràfiques d’un treball

serà establerta i s’ordenarà alfabè­ticament per autors i cronològicament per a un mateix autor, afegint les lletres a, b, c,... als treballs del mateix any. En el text, s’indi­caran en la forma usual: “...segons Wemmer (1998)... ”, “...ha estat definit per Robinson & Redford (1991)...”, “...les prospeccions realitzades (Begon et al., 1999)...”

Taules. Les taules es numeraran 1, 2, 3, etc. i han de ser sempre ressenyades en el text. Les taules grans seran més estretes i llargues que amples i curtes ja que s'han d'encaixar en l'amplada de la caixa de la revista.

Figures. Tota classe d’il·lustracions (gràfics, figures o fotografies) entraran amb el nom de figura i es numeraran 1, 2, 3, etc. i han de ser sempre ressen­ yades en el text. Es podran incloure fotografies si són imprescindibles. Si les fotografies són en color, el cost de la seva publicació anirà a càrrec dels au­ tors. La mida màxima de les figures és de 15,5 cm d'amplada per 24 cm d'alçada. S'evitaran les figures tridimensionals. Tant els mapes com els dibuixos han d'incloure l'escala. Els ombreigs preferibles són blanc, negre o trama. S'evitaran els punteigs ja que no es repro­dueixen bé.

Peus de figura i capçaleres de taula. Els peus de figura i les capçaleres de taula seran clars, concisos i bilingües en la llengua de l’article i en anglès.

Els títols dels apartats generals de l’article (Intro­ ducción, Material y métodos, Resultados, Discusión, Conclusiones, Agradecimientos y Referencias) no aniran numerats. No es poden utilitzar més de tres nivells de títols.

Els autors procuraran que els seus treballs originals no passin de 20 pàgines (incloent–hi figures i taules).

Si a l'article es descriuen nous tàxons, caldrà que els tipus estiguin dipositats en una insti­tució pública.

Es recomana als autors la consulta de fascicles recents de la revista per tenir en compte les seves normes.

Animal Biodiversity and Conservation 29.2 (2006)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (antes Miscel·lània Zoològica) es una revista inter­ disciplinar, publicada desde 1958 por el Museo de Zoología de Barcelona. Incluye artículos de investigación empírica y teórica en todas las áreas de la zoología (sistemática, taxo­nomía, morfología, biogeografía, ecología, etología, fisiología y genéti­ ca) procedentes de todas las regiones del mundo, con especial énfasis en los estudios que de una manera u otra tengan relevancia en la biología de la conservación. La revista no publica catálogos, listas de especies sin más o citas puntuales. Los estudios realizados con especies raras o protegidas pueden no ser aceptados a no ser que los autores dispongan de los permisos correspondientes. Cada volumen anual consta de dos fascículos.

Animal Biodiversity and Conservation está re­ gistrada en todas las bases de datos importantes y además está disponible gratuitamente en internet en http://www.bcn.cat/ABC, lo que permite una difusión mundial de sus artículos.

Todos los manuscritos son revisados por el editor ejecutivo, un editor y dos revisores independientes, elegidos de una lista internacional, a fin de garan­ tizar su calidad. El proceso de revisión es rápido y constructivo, y se realiza vía correo electrónico siem­ pre que es posible. La publicación de los trabajos aceptados se realiza con la mayor rapidez posible, normalmente dentro de los 12 meses siguientes a la recepción del trabajo.

Una vez aceptado, el trabajo pasará a ser propie­ dad de la revista. Ésta se reserva los derechos de autor, y ninguna parte del trabajo podrá ser reprodu­ cida sin citar su procedencia.

Normas de publicación Los trabajos se enviarán preferentemente de forma electrónica (abc@bcn.cat). El formato preferido es un documento Rich Text Format (RTF) o DOC, que incluya las figuras (TIF). Si se opta por la versión im­ presa, deberán remitirse cuatro copias juntamente con una copia en disquete a la Secretaría de Redacción.

Debe incluirse, con el artículo, una carta donde conste que el trabajo versa sobre inves­tigaciones originales no publi­cadas an­te­rior­mente y que se somete en exclusiva a Animal Biodiversity and Conservation.

En dicha carta también debe constar, para trabajos donde sea necesaria la manipulación de animales, que los autores disponen de los permisos necesa­ rios y que han cumplido la normativa de protección animal vigente. Los autores pueden enviar también sugerencias para asesores.

Cuando el trabajo sea aceptado los autores de­ berán enviar a la Redacción una copia impresa de la versión final junto con un disquete del manuscrito preparado con un pro­cesador de textos e indicando el programa utilizado (preferiblemente Word). Las pruebas de imprenta enviadas a los autores deberán ISSN: 1578–665X

III

remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Los gastos debidos a modifica­ ciones sustanciales en las pruebas de im­pren­­ta, intro­ ducidas por los autores, irán a ­cargo de los mismos.

El primer autor recibirá 50 separatas del trabajo sin cargo alguno y una copia electrónica en formato PDF. Manuscritos Los trabajos se presentarán en formato DIN A–4 (30 líneas de 70 espacios cada una) a doble espacio y con las páginas numeradas. Los manuscritos deben estar completos, con tablas y figuras. No enviar las figuras originales hasta que el artículo haya sido aceptado.

El texto podrá redactarse en inglés, castellano o catalán. Se sugiere a los autores que envíen sus trabajos en inglés. La revista ofre­ce, sin cargo ningu­ no, un servicio de corrección por parte de una persona especializada en revistas científicas. En cualquier caso debe presentarse siempre de forma correcta y con un lenguaje claro y conciso. La redacción del texto deberá ser impersonal, evitán­dose siempre la primera persona.

Los caracteres en cursiva se utilizarán para los nombres científicos de géneros y especies y para los neologismos que no tengan traducción; las citas textuales, independientemente de la lengua en que estén, irán en letra redonda y entre comillas; el nombre del autor que sigue a un taxón se escribirá también en redonda.

Al citar por primera vez una especie en el trabajo, deberá especificarse siempre que sea posible su nombre común.

Los topónimos se escribirán bien en su forma original o bien en la lengua en que esté redactado el trabajo, siguiendo el mismo criterio a lo largo de todo el artículo.

Los números del uno al nueve se escribirán con letras, a excepción de cuando precedan una unidad de medida. Los números mayores de nueve se escribirán con cifras excepto al empezar una frase.

Las fechas se indicarán de la siguiente forma: 28 VI 99; 28, 30 VI 99 (días 28 y 30); 28–30 VI 99 (días 28 al 30).

Se evitarán siempre las notas a pie de página.

Formato de los artículos Título. El título será conciso pero suficientemente explicativo del contenido del trabajo. Los títulos con designaciones de series numéricas (I, II, III, etc.) serán aceptados excepcionalmente previo consen­ timiento del editor.

Nombre del autor o autores.

Abstract en inglés de 12 líneas mecanografiadas (860 espacios como máximo) y que exprese la esencia del manuscrito (introducción, material, métodos, resulta­ dos y discusión). Se evitarán las especulaciones y las citas bibliográficas. Irá encabezado por el título del trabajo en cursiva.

Key words en inglés (un máximo de seis) que especifiquen el contenido del trabajo por orden de importancia. © 2006 Museu de Ciències Naturals

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Resumen en castellano, traducción del abstract. Su traducción puede ser solicitada a la revista en el caso de autores que no sean castellano hablan­tes.

Palabras clave en castellano.

Dirección postal del autor o autores.

(Título, Nombre, Abstract, Key words, Resumen, Palabras clave y Dirección postal conformarán la primera página.)

Introducción. En ella se dará una idea de los ante­ cedentes del tema tratado, así como de los objetivos del trabajo.

Material y métodos. Incluirá la información referente a las especies estudiadas, aparatos utilizados, me­ todología de estudio y análisis de los datos y zona de estudio.

Resultados. En esta sección se presentarán úni­ camente los datos obtenidos que no hayan sido publicados previamente.

Discusión. Se discutirán los resultados y se compara­ rán con otros trabajos relacionados. Las sugerencias sobre investigaciones futuras se podrán incluir al final de este apartado.

Agradecimientos (optativo).

Referencias. Cada trabajo irá acompañado de una bibliografía que incluirá únicamente las publicaciones citadas en el texto. Las referencias deben presentarse según los modelos siguientes (método Harvard): * Artículos de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe­ cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773 * Libros y otras publicaciones no periódicas: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Trabajos de contribución en libros: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva­ tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.).

Oxford University Press, Oxford. * Tesis doctorales: Merilä, J., 1996. Genetic and quantitative trait vari­ ation in natural bird populations. Tesis doctoral, Uppsala University.

* Los trabajos en prensa sólo se citarán si han sido aceptados para su publicación: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

Las referencias se ordenarán alfabética­men­te por autores, cronológicamen­te para un mismo autor y con las letras a, b, c,... para los tra­bajos de un mismo autor y año. En el texto las referencias bibliográficas se indicarán en la forma usual: "... según Wemmer (1998)...", "...ha sido definido por Robinson & Redford (1991)...", "...las prospecciones realizadas (Begon et al., 1999)..."

Tablas. Las tablas se numerarán 1, 2, 3, etc. y se reseñarán todas en el texto. Las tablas grandes deben ser más estrechas y largas que anchas y cortas ya que deben ajustarse a la caja de la revista.

Figuras. Toda clase de ilustraciones (gráficas, figuras o fotografías) se considerarán figuras, se numerarán 1, 2, 3, etc. y se citarán todas en el texto. Pueden incluirse fotografías si son imprescindibles. Si las fotografías son en color, el coste de su publicación irá a cargo de los autores. El tamaño máximo de las figuras es de 15,5 cm de ancho y 24 cm de alto.

Deben evitarse las figuras tridimen­sionales. Tanto los mapas como los dibujos deben incluir la escala.

Los sombreados preferibles son blanco, negro o trama. Deben evitarse los punteados ya que no se reproducen bien.

Pies de figura y cabeceras de tabla. Los pies de figura y cabeceras de tabla serán claros, concisos y bilingües en castellano e inglés.

Los títulos de los apartados generales del artículo (Introducción, Material y métodos, Resultados, Discusión, Agradecimientos y Referencias) no se numerarán. No utilizar más de tres niveles de títulos.

Los autores procurarán que sus trabajos originales no excedan las 20 páginas incluidas figuras y tablas.

Si en el artículo se describen nuevos taxones, es imprescindible que los tipos estén depositados en alguna institución pública.

Se recomienda a los autores la consulta de fascículos recientes de la revista para seguir sus directrices.

Animal Biodiversity and Conservation 29.2 (2006)

V

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an inter­­dis­c i­p li­n ary journal which has been published by the Zoologi­ cal Museum of Bar­c elona since 1958. It includes empirical and theoretical research in all aspects of Zoology (Systematics, Taxo­n omy, Morphology, Bio­geography, Ecology, Etho­logy, Physio­logy and Genetics) from all over the world with special emphasis on studies that stress the relevance of the study of Conservation Biology. The journal does not publish catalogues, lists of species (with no other relevance) or punctual records. Studies about rare or protected species will not be accep­ ted unless the authors have been granted all the relevant permits. Each annual volume consists of two issues.

Animal Biodiversity and Conservation is registered in all principal data bases and is freely available online at http://www.bcn.cat/ABC, thus assuring world–wide access to articles published therein.

All manuscripts are screened by the Executive Edi­ tor, an Editor and two independent reviewers in order to guarantee the quality of the papers. The process of review is rapid and constructive. Once accepted, papers are published as soon as practicable, usually within 12 months of initial submission.

Upon acceptance, manuscripts become the prop­ erty of the journal, which reserves copyright, and no published material may be reproduced without quoting its origin.

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Number all pages. Manuscripts should be complete with figures and tables. Do not send original figures until the paper has been accepted.

The text may be written in English, Spanish or Catalan. Authors are encouraged to send their con­ tributions in English. The journal provides a FREE service of correction by a professional translator specialized in scientific publications. Care should be taken in using correct wording and the text should be written concisely and clearly. Wording should be impersonal, avoiding the use of the first person.

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Quotations in whatever language used must be typed in ordinary print between quotation marks. The name of the author following a taxon should also be written in small print.

The common name of the species should be writ­ ten in capital letters. When referring to a species for the first time in the text, both common and scientific names must be given when possible.

Place names may appear either in their original form or in the language of the manuscript, but care should be taken to use the same criteria throughout the text.

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Information for authors Electronic submission of papers is encouraged (abc@ bcn.cat). The preferred format is a document Rich Text Format (RTF) or DOC, including figures (TIF). In the case of sending a printed version, four copies should be sent together with a copy on a computer disc to the Editorial Office. A cover letter stating that the article reports on original research not published elsewhere and that it has been submitted exclusively for consi­ deration in Animal Biodivers­ity and Conservation is also necessary. When animal manipulation has been necessary, the cover letter should also especify that the authors follow current norms on the protection of animal species and that they have obtained all relevant permissions. Authors may suggest referees for their papers.

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The first author will receive 50 reprints free of charge and an electronic version of the article in PDF format.

ISSN: 1578–665X

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Summaries of articles by non­–Spanish speaking authors will be trans­lated by the journal on request.

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© 2006 Museu de Ciències Naturals

VI

Material and methods. This section should provide relevant information on the species studied, materials, methods for collecting and analysing data and the study area.

Results. Report only previously unpublished results from the present study.

Discussion. The results and their comparison with related studies should be discussed. Sug­gestions for future research may be given at the end of this section.

Acknowledgements (optional).

References. All manuscripts must include a bibliogra­ phy of the publications cited in the text. References should be presented as in the following examples (Harvard method): * Journal articles: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe­ cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Books or other non–periodical publications: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Contributions or chapters of books: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva­ tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.).

Oxford University Press, Oxford. * Ph. D. Thesis: Merilä, J., 1996. Genetic and quantitative trait vari­ ation in natural bird populations. Ph. D. Thesis, Uppsala University. * Works in press should only be cited if they have been accepted for publication: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim.

Biodivers. Conserv.

References must be set out in alphabetical and

chronological order for each author, adding the letters a, b, c,... to papers of the same year. Biblio­graphic citations in the text must appear in the usual way: "... according to Wemmer (1998)...", "...has been defined

by Robinson & Redford (1991)...", "...the pros­pec­tions that have been carried out (Begon et al., 1999)..."

Tables. Tables must be numbered in Arabic numerals with reference in the text. Large tables should be narrow (across the page) and long (down the page) rather than wide and short, so that they can be fitted into the column width of the journal.

Figures. All illustrations (graphs, drawings or photographs) must be termed as figures, num­ bered consecutively in Arabic numerals (1, 2, 3, etc.) and with re­ference in the text. Glossy print photographs, if essential, may be included. Colour photographs may be published but its publication will be charged to authors. Maximum size of figures is 15.5 cm width and 24 cm height. Figures will not be tridimen­sional. Both maps and drawings must include scale. The preferred shadings are white, black and bold hatching. Avoid stippling, which does not reproduce well.

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Main headings (Introduction, Material and methods, Results, Discussion, Acknowled­ge­ments and Refe­ rences) should not be number­ed. Do not use more than three levels of headings.

Manuscripts should not exceed 20 pages including figures and tables.

If the article describes new taxa, type material must be deposited in a public institution.

Authors are advised to consult recent issues of the journal and follow its conventions.

VII

Animal Biodiversity and Conservation 29.2 (2006)

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"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 29.2 (2006)

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"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 29.2 (2006)

XI

Arxius de Miscel·lània Zoològica vol. 4 (2006) 2006 Museu de Ciències Naturals de la Ciutadella ISSN: 1698–0476

Índex/Índice/Contents Bros, V., 2006. Cargols terrestres (Gastropoda, Stylommatophora) del Parc Natural de la Muntanya de Montserrat (Barcelona, NE península Ibèrica). Arxius de Miscel·lània Zoològica, vol 4: 1–41.

Abstract Land snails (Gastropoda, Stylommatophora) in the Natural Park of Montserrat (Barcelona, NE Iberian Peninsula).— The inventory of 73 land snails in the Natural Park of Montserrat was updated following the review of 130 publications. Planned field study was also conducted in areas of different habitats on the Montserrat mountain to provide a preliminary description of the communities of land snails in the study area. A total of 342 samples of land snails were studied and 50 species were identified. The most frequent were Pomatias elegans, Helicigona lapicida, Pseudotachea splendida, Abida polyodon and Otala punctata. In this region of the prelittoral Catalan mountain range, the level of endemism was high for Abida secale bofilli, Montserratina bofilliana and Xerocrassa montserratensis. The results of the field work extend the faunistic catalogue of the Natural Park of Montserrat to include references to Hygromia cinctella, Microxeromagna lowei, Paralaoma servilis and Punctum pygmaeum in the area. Finally, investigation and conservation programmes are suggested for the endemic species Xerocrassa montserratensis, protected by the Plan for Areas of Natural Interest (PEIN) approved by Decree 328/1992.

Key words: Mollusk, Natural Park of Montserrat, Biodiversity, Land mollusks, Land snails, Conservation.

Al–Ghzawi, A., Zaitoun, S., Mazary, S., Schindler, M. & Wittmann, D., 2006. Diversity of bees (Hymenoptera, Apiformes) in extensive orchards in the highlands of Jordan. Arxius de Miscel·lània Zoològica, vol. 4: 42–48.

Abstract Diversity of bees (Hymenoptera, Apiformes) in extensive orchards in the highlands of Jordan.— Bees visiting the blossoms of fruit trees were surveyed for the first time in Jordan. A transect was determined in Ebbin village in Ajlun (32° 22" N, 35° 49" E) where the bees were collected from blossoms of stone fruit trees.

Most of the specimens were identified up to the species level and few specimens were identified up to the genus level only. A total of 1461 specimens were collected during the study period and 53 bee species were identified and recorded for the first time in Jordan. The collected species represented five families: Apidae, Megachilidae, Halictidae, Andrenidae and Colletidae. The results showed that Apidae and Megachilidae were the largest in terms of diversity, while Halictidae showed the highest abundance.

Key words: Pollinators, Stone fruit trees, Wild bees, Insects, Jordan.

Fresneda, J. & Fadrique, F., 2006. Datos de distribución de los Cholevinae de Marruecos (Coleoptera, Leiodidae). Arxius de Miscel.lània Zoològica, vol. 4: 49–57.

Abstract Distribution data of the Cholevinae from Morocco (Coleoptera, Leiodidae).— The author’s given a new data of the distribution of Speonemadus maroccanus (Jeannel, 1936), Nargus (Demochrus) rufipennis (Lucas, 1846), Choleva (Choleva) kocheri Henrot, 1962 and Catops fuscus fuscoides Reitter, 1909.

Key words: Cholevinae, New data, Morocco.

web: http://www.bcn.cat/arxiusMZ

All works are licensed under a Creative Commons Attribution­–NonCommercial 2.5 License

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain

Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Les cites o els abstracts dels articles d’Animal Biodiversity and Conservation es resenyen a / Las citas o los abstracts de los artículos de Animal Biodiversity and Conservation se mencionan en / Animal Biodiversity and Conservation is cited or abstracted in: Abstracts of Entomology, Agrindex, Animal Behaviour Abstracts, Anthropos, Aquatic Sciences and Fisheries Abstracts, Behavioural Biology Abstracts, Biological Abstracts, Biological and Agricultural Abstracts, Current Primate References, Directory of Open Acces Journals (DOAJ), Ecological Abstracts, Ecology Abstracts, Entomology Abstracts, Environmental Abstracts, Environmental Periodical Bibliography, Genetic Abstracts, Geographical Abstracts, índex de Sumaris Electrònics del Consorci de Biblioteques de Catalunya, Índice Español de Ciencia y Tecnología, International Abstracts of Biological Sciences, International Bibliography of Periodical Literature, International Developmental Abstracts, Marine Sciences Contents Tables, Oceanic Abstracts, Recent Ornithological Literature, Red de Revistas Científicas Españolas (REVICIEN), Referatirnyi Zhurnal, Science Abstracts, Serials Directory, Ulrich’s International Periodical Directory, Zoological Records.

Índex / Índice / Contents Animal Biodiversity and Conservation 29.2 (2006) ISSN 1578–665X

91–107 F. Manzoor & M. S. Akhtar Morphometric análisis of population sam­ ples of soldier caste of Odontotermes obesus (Rambur) (Isoptera, Termitidae, Macrotermitinae) 109–115 K. Emmanuvel Rajan & G. Marimuthu A preliminary examination of genetic diver­ sity in the Indian false vampire bat Megaderma lyra 117–121 J. Mateu & O. Escolà El género Antoinella Jeannel, 1937 (Coleop­ tera, Carabidae, Trechinae) tres especies nuevas de Marruecos: A. espanyoli sp. n., A. iblanensis sp. n. y A. fadriquei sp. n.

123–131 R. I. Ruiz–C. & C. Román–Valencia Aspectos taxonómicos de Cetopsorhamdia boquillae y C. nasus (Pisces, Heptapteri­ dae), con anotaciones sobre su ecología en la cuenca alta de los ríos Magdalena y Cauca, Colombia 133–148 A. Valtonen, K. Saarinen & J. Jantunen Effect of different mowing regimes on but­ terflies and diurnal moths on road verges 149–156 C. G. Majka & S. Bondrup–Nielsen Parataxonomy: a test case using beetles

157–163 G. F. Ficetola, M. Valota & F. de Bernardi Temporal variability of spawning site se­ lection in the frog Rana dalmatina: conse­ quences for habitat management 165–178 M. A. Barrett & P. Stiling Impacts of endangered Key deer herbivory on imperiled pine rockland vegetation: a conservation dilemma?

179–189 S. H. Borges Rarity of birds in the Jaú National Park, Brazilian Amazon 191–194 M. D. Bargues, R. L. Mera y Sierra, H. G. Gómez, P. Artigas & S. Mas–Coma Ribosomal DNA ITS–1 sequencing of Galba truncatula (Gastropoda, Lymnaeidae) and its potential impact on fascioliasis trans­ mission in Mendoza, Argentina 195­–200 C. R. Altaba A new land snail from the Quaternary of Mallorca (Balearic Islands, Western Me­ diterranean): Darderia bellverica n. gen., n. sp. (Gastropoda, Pulmonata, Helico­ dontidae) XI Abstracts del volum 4 (2006) d'Arxius de Miscel·lània Zoològica Abstracts del volumen 4 (2006) de Arxius de Miscel·lània Zoològica Abstracts of volume 4 (2006) of Arxius de Miscel·lània Zoològica