CICIMAR Oceánides Vol. 27 (2) 2012 by CICIMAR Oceánides

ISSN 1870-0713

Volumen 27(2)

Diciembre 2012

DIRECTORIO CENTRO INTERDISCIPLINARIO DE CIENCIAS MARINAS

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CICIMAR Oceánides Ed. Responsable: David A. Siqueiros Beltrones

ISSN: 1870-0713 Distribuida por: CICIMAR-IPN, Ave. IPN s/n, Col. Playa Palo de Sta. Rita, 23096 La Paz, B.C.S., Tels: (612)123-03-50, (612)123-46-58. Fax: (612)122- 5322.

Diciembre 2012

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CICIMAR Oceánides, 2012

VOL 27(2)

ISSN-1870-0713

CONTENIDO Changes in species composition and abundance of fish larvae from the Gulf of Tehuantepec, Mexico. LÓPEZ-CHÁVEZ, O., G. ACEVES-MEDINA, R. J. SALDIERNAMARTÍNEZ, S. P. A. JIMÉNEZ-ROSENBERG, J. P. MURAD-SERRANO, Á. MARÍNGUTIÉRREZ & O. HERNÁNDEZ-HERNÁNDEZ.

Metabolic scaling regularity in aquatic ecosystems. SALCIDO-GUEVARA, L. A., F. ARREGUÍN-SÁNCHEZ, L. PALMERI & A. BARAUSSE.

The potential effect of nitrogen removal processes on the δ15n from different taxa in the mexican subtropical north eastern Pacific. CAMALICH, J., A. SÁNCHEZ, S. AGUÍÑIGA & E. F. BALART

Proliferation of Amphidinium carterae (Gymnodiniales: Gymnodiniaceae) in Bahía de La Paz, Gulf of California. GÁRATE-LIZÁRRAGA, I.

Marine and lagoon recruitment of Litopenaeus vannamei (Boone, 1931) (Decapoda: Penaeidae) in the “cabeza de toro-la joya buenavista” lagoon system, Chiapas, Mexico. CERVANTES-HERNÁNDEZ, P., M. A. GÓMEZ-PONCE & P. TORRESHERNÁNDEZ

Additional data related to the distribution of ventrally sclerotized species of Lepido� phthalmus Holmes, 1904 (Decapoda: Axiidea, Callianassidae, Challichirinae) from the tropical eastern Pacific. HENDRICKX, M. E. & J. LÓPEZ

Coastal sea surface temperature records along the Baja California peninsula. SICARDGONZÁLEZ, M.T., M.A, TRIPP-VALDÉZ, L. OCAMPO, A.N. MAEDA-MARTÍNEZ & S.E. LLUCH-COTA.

CICIMAR Oceánides 27(2): 1-11 (2012)

CHANGES IN SPECIES COMPOSITION AND ABUNDANCE OF FISH LARVAE FROM THE GULF OF TEHUANTEPEC, MEXICO López-Chávez¹, O., G. Aceves-Medina¹, R. J. Saldierna-Martínez¹, S. P. JiménezRosenberg¹, J. P. Murad-Serrano², Á. Marín-Gutiérrez² & O. Hernández-Hernández² Departamento de Plancton y Ecología Marina, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n, col. Playa Palo de Santa Rita, La Paz, B.C.S., CP. 23096, México. Fax +52 (612) 12 2 53 22. 2Secretaría de Marina DIGAOHM. Estación de Investigación Oceanográfica de Salina Cruz, Oaxaca, CP. 70660, México. email: gaceves@ipn.mx 1

ABSTRACT. The larval fish abundance and species composition of the Gulf of Tehuantepec are described based on the analysis of samples obtained from oblique zooplankton tows during summer 2007 and spring 2008. Changes in species composition and abundance between both periods were also described. A total of 145 taxa were obtained from which 73 were identified to species level, 43 to genus and 29 to family. The larval fish assemblage of the Gulf of Tehuantepec showed distinctive characteristics from other regions of the American Pacific, such as: A) a dominance of coastal-pelagic species (mainly Bregmaceros bathymaster); B) high diversity and abundance of shallow demersal species even along the oceanic stations of the study area; and C) a low proportion of mesopelagic species, an unusual condition in areas with narrow continental shelf. The diversity estimations suggest that Gulf of Tehuantepec is one of the most diverse ecosystems of the American Pacific, even as compared with other regions considered of highest diversity such as the Gulf of California. The high abundance, as well as the presence of the larval, juvenile and adult stages of B. bathymaster, suggests the importance of this region as a reproductive, nursery and recruitment for this species.

Keywords: Fish larvae, Gulf of Tehuantepec, México. Cambios en la composición de especies y abundancia de larvas de peces en el Golfo de Tehuantepec, México RESUMEN. Se describen la composición de especies y abundancia de larvas de peces del Golfo de Tehuantepec a partir del análisis de muestras obtenidas en arrastres oblicuos de zooplancton. Así mismo, se describen los cambios en composición y abundancia entre un periodo de verano y uno de primavera. Se obtuvieron 145 taxa de los que 73 se identificaron a nivel especie, 43 a género y 29 a familia. La comunidad de larvas de peces del Golfo de Tehuantepec mostró rasgos distintivos de otras regiones similares del Pacífico Americano, tales como: A) dominancia de especies pelágico-costeras (particularmente Bregmaceros bathymaster); B) alta diversidad y abundancia de especies demersales someras aún en las estaciones mas oceánicas del área de estudio; y C) una proporción menor de especies de peces mesopelágicos, condición poco común en áreas con plataforma continental estrecha. Las estimaciones de diversidad ubican al Golfo de Tehuantepec como uno de los ecosistemas más diversos del Pacífico americano, aún comparándolo con regiones consideradas de alta diversidad a nivel mundial como es el caso del Golfo de California. La abundancia y la presencia de estadios larvales, juveniles y adultos de B. bathymaster reflejan la importancia de esta zona como área de reproducción, crianza y reclutamiento de esta especie.

Palabras clave: Larvas de peces, Golfo de Tehuantepec, México. López-Chávez, O., G. Aceves-Medina, R. J. Saldierna-Martínez, S. P. Jiménez-Rosenberg, J. P. Murad-Serrano, Á. Marín-Gutiérrez & O. Hernández-Hernández. 2012. Changes in species composition and abundance of fish larvae from the Gulf of Tehuantepec, Mexico. CICIMAR Oceánides, 27(2): 1-11.

INTRODUCTION

The Gulf of Tehuantepec is an area with intense fishery activity sustained since this is one of the three Central America areas of the eastern tropical Pacific with the highest primary productivity (Robles–Jarero & Lara–Lara, 1993; Ortega–García et al., 2000). The study area is known as a region of high diversity (Briggs, 1974), however there are few studies on the species composition of this region (Ortega–García et al., 2000), and most of them are limited to a few taxonomic groups such as copepods and euphausiids (Farber-Lorda et al., 1994; Fernández-Alamo et al., 2000). The Gulf of Tehuantepec is also a key biogeographic area. Bahía Tangolunda (Fig. 1) is a transition area between two main biogeographic regions: the Panamic and Mexican provinces (Briggs, 1974). Although these biogeographic Fecha de recepción: 7 de febrero de 2012

provinces were based mainly on fishes, the ichthyofauna of the Gulf of Tehuantepec is still not well known with only few descriptive studies in this area. The pioneer studies described a demersal fish fauna of around 292 species, and 38 more species in the coastal lagoon systems of Oaxaca and Chiapas (Anónimo, 1978; Acal & Arias, 1990; Bianchi, 1991; Tapia–García et al., 1994, Díaz–Ruiz et al., 2004), but there are no assessments of epi-, bathy- or mesopelagic species. Estimations of the species richness in the Gulf of Tehuantepec contrast with those of the Gulf of California, with an estimated 850 to 900 species (Castro–Aguirre et al., 1995). Differences between the diversity in these areas have been explained as a result of the high number of microhabitats as well as by the presence of a combined fauna from temperate, subtropical and tropical species in the relative narrower area of the Gulf of California (Briggs, Fecha de aceptación: 13 de agosto de 2012

LÓPEZ-CHÁVEZ et al.

1974, Castro-Aguirre et al., 1995) besides a more intense and systematic sampling effort in the Gulf of California. However, differences on species diversity could be related also to a lack of relevant studies of the fish species composition in the Gulf of Tehuantepec.

summer in this area corresponds with the dry season in which the Tehuano winds (which flow perpendicular to the coast) decrease significantly (Gallegos–García & Barberán–Falcón, 1998) and is characterized by a higher abundance of pelagic species (Tapia-García et al., 1994). Spring on the other hand corresponds to the rainy season and the strong Tehuano winds are almost over (Gallegos–García & Barberán– Falcón, 1998). During spring the abundance of demersal and estuarine-lacunar species increases (Tapia-García et al., 1994).

Studies on the early life stages of fish provide evidence of the adult presence, as well as their reproduction; both are key elements in the biogeographical sense, and for recognizing reproductive and nursery habitats. At the present, there is no information at the species level concerning the fish larvae of this important area. The work by Ahlstrom (1972) during the EASTROPAC surveys included only two sampling stations in an oceanic area far from the Gulf of Tehuantepe. Whilst Ayala–Duval et al. (1998) studied larval fish distribution of the coastal region of the gulf, but they identified specimens only to family and order taxonomic levels.

The objective of this work is to describe the larval fish species composition as well as the seasonal species change occurring between summer (July, 2007) and spring (May–June, 2008) in the Gulf of Tehuantepec. MATERIALS AND METHODS The Gulf of Tehuantepec is located in the southern tropical region of the Mexican Pacific. It is limited to the west by Puerto Ángel, Oaxaca and to the east by the mouth of the Suchiate river in Chiapas (Fig. 1). It has an area of 35,188 km² and a narrow continental shelf on the west side that increase toward the east side (Sosa– Hernández et al., 1980). The annual mean sea

During the summer of 2007 (July 3rd-12th) and spring 2008 (May 26th-June 8th) the Secretaria de Marina made two oceanographic surveys in which zooplankton trawls were done. Analyzes of these samples allow us to obtain data in order to describe the larval fish species composition of the Gulf of Tehuantepec. The 30

of a rni lifo Ca

Bahía Sebastián Vizcaino

lf Gu

México

Pacific Ocean 15

Gulf of Tehuantepec -115

Pto. Escondido

North latitude

Pto. Ángel

May 2008

-110

-105

-100

-95

-90

Salina Cruz Bahía Tangolunda Suchiate river

July 2007

West Longitude Figure 1. Study area and sampling stations during summer 2007 (dots) and spring 2008 (triangles). 200 m isobath is shown in dashed line.

FISH LARVAE FROM THE GULF OF TEHUANTEPEC

surface temperature ranges between 25º and 30º C (Gallegos–García & Barberán-Falcón, 1998). Two oceanographic surveys were conducted, one in summer (July 3rd to 12th, 2007) and one in spring (May 26th –June 8th, 2008). Zooplankton oblique tows were performed at 32 sampling stations in summer and 36 in spring (Fig. 1) using the Smith and Richardson (1979) standard method. Almost all the tows were done at a 200 m depth with an average towing time of 30 min but, in case stations were shallow, tows were then done 10 m above the sea floor. Nytex Bongo nets with 333 and 505-µm of mesh, 0.6 m in diameter, and flexible collectors were used. Each net was equipped with a digital flowmeter in the mouth to estimate the water volume filtered (in average 346 m³ in July and 297 m³ in spring). The zooplankton obtained with the 505-µm mesh net was preserved in a 4% formalin solution buffered with sodium borate, and that obtained with the 333-µm mesh net was preserved in 96% alcohol. Only the specimens collected with the 505-µm mesh net were used. Fish larvae were sorted from all samples and identified to species when possible following Moser (1996). Identified organisms were counted and their abundance was standardized on each sampling station to 10 m² of sea surface (Smith & Richardson, 1979). When specimens could not be identified to species level in the absence of descriptions, they were identified to family or genus and the meristic and morphometric characteristics of each specimen were used to assign a type to each taxon. In this way, Syacium sp. 1 and Syacium sp. 2 for example, should be considered as different species. Percent abundance of families and taxa for each survey were calculated after adding adjusted numbers (organisms/10 m²). Due to the difference in the numbers of sampling stations as well as the non normal distribution in the ichthyoplankton data, we calculated de geometric mean of the larval abundance with its standard deviation in order to compare the larval abundance between both surveys as in Lavaniegos and Hereu (2009). The species list was done according to Nelson (2006) and includes biogeographic affinity (tropical, transitional), habitat of adult distribution (shallow demersal, deep demersal, epipelagic, mesopelagic or bathypelagic) based on Eschmeyer (2009). All specimens were preserved in borosilicate vials and included in the “Larval fish collection of the Mexican Pacific” of the Plankton and Marine Ecology Department of Centro Interdisciplinario de Ciencias Marinas (CICIMAR–IPN).

In order to do a comparative analysis of the species richness of the Gulf of Tehuantepec with other areas of the Mexican Pacific with high fish diversity, we performed cumulative species curves (Soberón & Llorente, 1993). For this propose the cumulative species adjusted curves of the Gulf of California (Aceves–Medina, 2003) and the raw data of Bahía Sebastián Vizcaino obtained from Jiménez-Rosenberg et al. (2007) and Jiménez-Rosenberg (2008) were used. Cumulative curves were performed until 68 samples were completed in order to make comparable the sampling efforts of both regions and the Gulf of Tehuantepec. RESULTS A total of 145 taxa were found, 73 were identified to species, 43 to genus and 29 to family (Table 1). From the 55 identified families, 15 represented at least 1% of the catches, totaling 92% of the collected larvae (Table 2). In the same way, 19 species had abundance ≥ 1% at least in one of both surveys, representing 84% of the total ichthyoplankton in July and 89% in May-June (Table 3). The number of species was highest during spring 2008 (Table 4) and the number of shared species for both seasons was only 62 (44%). Of the 19 most abundant species for all the study period, only Opisthonema sp. 1 and Eucinos� tomus dowii were not present during summer. In both seasons most abundant species were Bregmaceros bathymaster and Vinciguerria lu� cetia (Table 3), which suggests a similar composition in the dominant fraction of the larval fish for both summer and spring. The main differences between the larval fish assemblage of summer 2007 and spring 2008 were: a) The fish larvae abundance was almost twice in the spring survey (Table 4). b) The increase in the abundance of coastal pelagic species during spring (Table 4) was mainly an increase in the abundance of B. bathymas� ter and Opisthonema sp. 3 and sp.1 (Table 3). c) There was an increase during the spring in both the abundance and the number of taxa of shallow demersal species (Table 4), particularly species of Syacium and Symphurus (Table 3). d) A decrease in the abundance of mesopelagic species occurred during the spring. The adjusted cumulative curve for the Gulf of Tehuantepec (Fig. 2), shows an expected value of 120 species from 68 samples, which indicates a higher species richness compared with the curves from the Gulf of California

LÓPEZ-CHÁVEZ et al.

Table 1. Fish larvae collected in the Gulf during July 2007 and May 2008 showing percent abundance. Order (O); Sub Order (S.O.); Family (F). Habitat (HA): shallow demersal (sd); deep demersal (dd); coastal pelagic (cp); ocean epipelagic (op); mesopelagic (mp); and bathypelagic (bp). Taxon O. Anguiliformes S. O. Congroidei F. Ophichthidae Myrophis vafer Jordan and Gilbert, 1883 Ophichthus sp. 1 Ophichthus triserialis (Kaup, 1856) Ophichthus zophochir Jordan and Gilbert, 1882 Ophichthus sp. 2 F. Congridae Ariosoma gilberti (Ogilby, 1898) Bathycongrus varidens (Garman,1899) Congridae sp. 1 Paraconger californiensis Kanazawa, 1961 O. Clupeiformes S.O. Clupeoidei F. Clupeidae Etrumeus teres (DeKay, 1842) Harengula thrissina (Jordan and Gilbert, 1882) Opisthonema sp. 1 Opisthonema sp. 3 F. Engraulidae Cetengraulis mysticetus (Günther, 1867) O. Argentiniformes S.O. Argentinoidei F. Microstomatidae Bathylagoides nigrigenys (Parr, 1931) Bathylagoides wesethi (Bolin, 1938) O. Stomiiformes S.O. Phoschthyoidei F. Phosichthyidae Vinciguerria lucetia (Garman, 1899) F. Stomiidae Idiacanthus antrostomus Gilbert, 1890 O. Aulopiformes S.O. Synodontoidei F. Synodontidae Synodus sp. 1 Synodus sp. 2 S.O. Alepisauroidei F. Scopelarchidae Scopelarchoides nicholsi (Parr, 1929) F. Paralepididae Lestidiops neles (Harry, 1953) Lestidiops sp. 1 Paralepididae sp. 1 O. Myctophiformes F. Myctophidae Benthosema panamense (Tåning, 1932) Diaphus pacificus Parr, 1931 Diogenichthys laternatus (Garman, 1899) Hygophum atratum Garman, 1899 Lampanyctus parvicauda Parr, 1931 O. Lampriformes F. Trachipteridae Trachipterus altivelis Kner, 1859 O. Gadiformes F. Bregmacerotidae Bregmaceros bathymaster Jordan & Bollman 1889 Bregmaceros sp. 1 O. Ophidiiformes S.O. Ophidioidei F. Ophidiidae Cherublemma emmelas (Gilbert, 1890) Ophidion sp. 1

% HA

<0.1 <0.1 <0.1 <0.1 <0.1

sd sd sd sd sd

<0.1 <0.1 <0.1 <0.1

sd sd sd sd

<0.1 <0.1 2.7 4.2

cp cp cp cp

1.8

<0.1 bp <0.1 bp

14.3 mp <0.1 mp

<0.1 sd <0.1 sd <0.1 bp <0.1 op <0.1 op <0.1 2.3 1.8 <0.1 <0.1 <0.1

mp mp mp mp mp

<0.1 cp 35.9 cp <0.1 cp

<0.1 dd <0.1 sd

Taxon Ophidion sp. 2 O. Lophiiformes S.O. Lophioidei F. Lophiidae Lophiodes sp. 1 F. Melanocetidae Melanocetidae sp. 1 Melanocetidae sp. 2 O. Mugiliformes F. Mugilidae Mugil cephalus Linnaeus, 1758 O. Beloniformes F. Exocoetidae Cheilopogon sp. 1 Cheilopogon sp. 2 Cheilopogon sp. 3 Fodiator rostratus (Günther, 1866) Prognichthys tringa Breder, 1928 F. Hemiramphidae Oxyporhamphus micropterus (Valenciennes, 1847) O. Stephanoberyciformes F. Melamphaidae Melamphaes sp. 1 Melamphaidae sp. 1 Melamphaidae sp. 2 Scopelogadus mizolepis (Günther 1878) O. Beryciformes S.O. Holocentroidei F. Holocentridae Myripristis leiognathos Valenciennes, 1846 O. Scorpaeniformes S.O. Scorpaenidae F. Scorpaenidae Pontinus sp. 1 Scorpaenodes xyris (Jordan and Gilbert, 1882) F. Triglidae Prionotus sp. 1 O. Perciformes S.O. Percoide F. Serranidae Cephalopholis panamensis (Steindachner, 1877) Diplectrum sp. 1 Diplectrum sp. 3 Epinephelus sp.1 Paralabrax nebulifer (Girard 1854) Paralabrax maculatofasciatus Steindachner, (1868) Serranus sp. 1 Serranus sp. 3 F. Apogonidae Apogon sp. 1 F. Coryphaenidae Coryphaena hippurus Linnaeus, 1758 F. Carangidae Caranx caballus Günther, 1868 Caranx sexfasciatus Quoy and Gaimard, 1825 Chloroscombrus orqueta Jordan and Gilbert, 1883 Decapterus sp. 1 Naucrates ductor (Linnaeus, 1758) Oligoplites saurus (Bloch and Schneider, 1801) Selar crumenophthalmus (Bloch, 1793) Selene peruviana (Guichenot, 1866) F. Bramidae Bramidae sp. 1 F. Lutjanidae

% HA <0.1 sd

<0.1 dd <0.1 bp <0.1 bp <0.1 sd <0.1 <0.1 <0.1 <0.1 <0.1

cp cp cp cp cp

<0.1 cp <0.1 <0.1 <0.1 <0.1

mp mp mp mp

<0.1 sd

3.3 sd <0.1 sd sd

<0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1

sd sd sd sd sd sd sd sd

<0.1 sd <0.1 op <0.1 1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1

cp cp cp cp cp cp cp cp

<0.1 op

FISH LARVAE FROM THE GULF OF TEHUANTEPEC

Table 1. Continued. Order (O); Sub Order (S.O.); Family (F). Habitat (HA): shallow demersal (sd); deep demersal (dd); coastal pelagic (cp); ocean epipelagic (op); mesopelagic (mp); and bathypelagic (bp). Taxon Lutjanus peru (Nichols & Murphy, 1922) Lutjanus sp.1 F. Lobotidae Lobotes surinamensis (Bloch, 1790) F. Gerreidae Eucinostomus currani Zahuranec, 1980 Eucinostomus dowii (Gill, 1863) Eucinostomus gracilis (Gill, 1862) F. Haemulidae Haemulidae sp. 1 Haemulidae sp. 2 Haemulidae sp. 3 Haemulidae sp. 4 Haemulidae sp. 5 F. Haemulidae Haemulon sp. 1 F. Polynemidae Polydactylus approximans (Lay & Bennett, 1839) F. Sciaenidae Sciaenidae sp. 1 Sciaenidae sp. 2 Sciaenidae sp. 3 Sciaenidae sp. 4 Sciaenidae sp. 5 Sciaenidae sp. 6 Sciaenidae sp. 7 Sciaenidae sp. 8 F. Kyphosidae Kyphosidae sp. 1 S.O. Labroidei F. Pomacentridae Abudefduf troschelii (Gill, 1862) Stegastes sp. 1 F. Labridae Thalassoma sp. 1 S.O. Zoarcoidei F. Stichaeidae Stichaeidae sp. 1 S.O.Trachinoidei F. Uranoscopidae Uranoscopidae sp. 1 S.O. Blennioidei F. Blenniidae Hypsoblennius sp. 1 Ophioblennius steindachneri Jordan & Evermann, 1898 S.O. Gobioidei F. Eleotridae Dormitator latifrons (Richardson, 1844) Eleotridae sp. 1 Erotelis armiger (Jordan & Richardson, 1895) F. Gobiidae Ctenogobius manglicola (Jordan & Starks, 1895) Ctenogobius sagittula (Günther, 1862) Gobiidae sp. 1 Microgobius sp. 1 Microgobius sp. 2

% HA Taxon <0.1 sd F. Microdesmidae <0.1 sd Clarkichthys bilineatus (Clark, 1936) S.O. Acanthuroidei <0.1 sd F. Ephippidae Chaetodipterus zonatus (Girard, 1858) <0.1 sd Ephippidae sp. 1 <0.1 sd F. Luvaridae <0.1 sd Luvarus imperialis (Rafinesque, 1810) S.O. Scombroidei <0.1 sd F. Sphyraenidae <0.1 sd Sphyraena ensis Jordan & Gilbert, 1882 <0.1 sd F. Scombridae <0.1 sd Auxis sp. 1 <0.1 sd Euthynnus lineatus Kishinouye, 1920 F. Istiophoridae <0.1 sd Kajikia audax (Philippi, 1887) S.O. Stromateoidei <0.1 sd F. Stromateidae Peprilus sp. 1 <0.1 sd F. Nomeidae <0.1 sd Cubiceps pauciradiatus Günther, 1872 <0.1 sd Nomeidae sp. 1 <0.1 sd Psenes sio Haedrich 1970 <0.1 sd O. Pleuronectiformes <0.1 sd S.O. Pleuronectoidei <0.1 sd F. Paralichthyidae <0.1 sd Cyclopsetta panamensis (Steindachner, 1876) Etropus sp. 1 <0.1 sd Paralichthyidae sp. 1 Syacium sp. 1 Syacium sp. 2 <0.1 sd F. Pleuronectidae <0.1 sd Pleuronectidae sp. 1 F. Bothidae <0.1 sd Bothus leopardinus (Günther, 1862) Bothus sp. 1 Monolene asaedai Clark, 1936 <0.1 dd F. Cynoglossidae Symphurus atramentatus Jordan & Bollman, 1890 Symphurus callopterus Munroe & Mahadeva, 1989 <0.1 sd Symphurus chabanaudi Mahadeva & Munroe, 1990 Symphurus elongatus (Günther, 1868) Symphurus melanurus Clark, 1936 <0.1 sd Symphurus sp. 1 <0.1 sd Symphurus sp. 4

<0.1 sd <0.1 sd <0.1 sd <0.1 <0.1 <0.1 <0.1 <0.1

sd sd sd sd sd

(Aceves–Medina, 2003) and Bahía Sebastián Vizcaíno on the west coast of Baja California Sur (Jiménez–Rosenberg et al., 2007; Jiménez–Rosenberg, 2008). The mode in the number of species by sampling station (18 taxa per sample) also shows a higher alpha diversity compared with other re-

Symphurus sp. 5 Symphurus sp. 6 Symphurus sp. 7 Symphurus sp. 8 Symphurus sp. 9 Symphurus williamsi Jordan & Culver, 1895 O. Tetraodontiformes S.O. Balistoidei F. Balistidae Balistes polilepis Steindachner, 1876 Sufflamen verres (Gilbert & Starks, 1904)

<0.1 sd <0.1 sd <0.1 sd <0.1 sd <0.1 cp 1.7 op <0.1 op <0.1 op <0.1 sd <0.1 op <0.1 <0.1 op

<0.1 <0.1 <0.1 3.5 2.9

sd sd sd sd sd

<0.1 sd 1.8

sd sd <0.1 sd <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1

dd dd sd sd sd sd sd

<0.1 <0.1 <0.1 <0.1 <0.1 <0.1

sd sd sd sd sd sd

<0.1 sd <0.1 sd

gions of the Eastern Pacific (Table 5). DISCUSSION This is the first descriptive work on the larval fish assemblage of the Gulf of Tehuantepec which includes 145 taxa from the Eastern Tropical Pacific.

LÓPEZ-CHÁVEZ et al.

Table 2. Taxonomic list of families collected as larvae in the Gulf of Tehuantepec during July 2007 and May 2008, ordered by their relative abundance (%) and the number of taxa identified in each family (NT).

Family Bregmacerotidae Phosichthyidae Clupeidae Paralichthyidae Myctophidae Scorpaenidae Sciaenidae Bothidae Carangidae Engraulidae Cynoglossidae Scombridae Gerreidae Lutjanidae Nomeidae Hemiramphidae Microstomatidae Haemulidae Gobiidae

% 40 14.3 7.2 7 5.4 3.4 2.1 2.1 2 1.8 1.8 1.7 1.4 1.2 1 0.9 0.6 0.4 0.4

NT 2 1 4 5 5 2 8 3 8 1 13 2 3 2 3 1 2 6 5

Family Eleotridae Coryphaenidae Sphyraenidae Paralepididae Balistidae Melamphaidae Ophichthidae Ophidiidae Congridae Exocoetidae Serranidae Synodontidae Stomiidae Pomacentridae Polynemidae Ephippidae Mugilidae Scopelarchidae Blenniidae

Only 50 % of the taxa (73) were identified to species, although almost all the specimens could be assigned to an equivalent category (types), using pigmentation patterns as well as meristic and morphometric characteristics. This allowed us to do a general description of the larval fish composition of this area, as well as a series of comparisons with other better known areas of the Eastern Pacific. The larval fish assemblage of the Gulf of Tehuantepec consists of a group of dominant species found in both, summer and spring seasons. Contrasting with other areas of the Mexican Pa-

% NT Family 0.4 3 Melanocetidae 0.3 1 Triglidae 0.3 1 Trachipteridae 0.3 3 Bramidae 0.3 2 Microdesmidae 0.2 4 Labridae 0.2 5 Istiophoridae 0.2 3 Lobotidae 0.2 4 Stromateidae 0.2 5 Kyphosidae 0.1 8 Pleuronectidae 0.1 2 Uranoscopidae 0.1 1 Apogonidae 0.1 2 Luvaridae 0.1 1 Holocentridae 0.1 2 Stichaeidae 0.1 1 Lophiidae <0.1 1 <0.1 2

% <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1 <0.1

NT 2 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

cific Ocean, one of the dominant components is of coastal–pelagic species, the most abundant and frequent of which was B. bathymaster. In the California Current B. bathymaster is found in low abundances (Moser & Smith, 1993) and in the Gulf of California it constituted only 0.2% of the total abundance (Aceves–Medina et al., 2003). Abundance of this species increases off the coasts of Jalisco and Colima, México, where they represent more than 80% of the ichthyoplankton all year round (Franco–Gordo et al., 2001; Siordia-Cermeño et al., 2006). The abundance of the tropical–subtropical species

Table 3. Total collected fish larvae after the standardized routine and relative abundance by cruise (%) of the most abundant taxa collected in the Gulf of Tehuantepec during July 2007 and May 2008. Geometric mean (G.M) and standard deviation (S.D.) per sample.

Species Bregmaceros bathymaster Vinciguerria lucetia Syacium sp. 1 Pontinus sp. 1 Syacium sp. 2 Diaphus pacificus Auxis sp. 1 Bothus leopardinus Opisthonema sp. 3 Benthosema panamense Oxyporhamphus micropterus Diogenichthys laternatus Lutjanus peru Psenes sio Symphurus elongatus Caranx sexfasciatus Opisthonema sp. 1 Cetengraulis mysticetus Eucinostomus dowii

jul-07 4462 3427 539 625 212 488 517 361 170 412 107 98 167 93 61 191 0 29 0

(%) 31.4 24.1 3.8 4.4 1.5 3.4 3.6 2.5 1.2 2.9 0.8 0.7 1.2 0.7 0.4 1.3 0 0.2 0

may-08 10453 1926 788 623 868 185 135 335 1426 481 227 263 170 206 215 208 1014 663 255

(%) 45.2 8.3 3.4 2.7 3.8 1 0.6 1.5 6.2 2.1 1 1.1 0.7 1 1 0.9 4.4 2.9 1.1

G.M. 41 22.3 7.5 4.6 3.7 3.1 3.1 2.9 2.2 2.2 2.1 2.1 2 1.9 1.9 1.7 1.5 1.5 1.4

S.D. 10.1 7.8 4.7 5.5 5.5 4.4 4.4 4.3 4.8 4.5 3.3 3.4 3.3 3.2 3.2 3.4 3.9 3.3 2.6

FISH LARVAE FROM THE GULF OF TEHUANTEPEC

Table 4. Total collected larvae and number of species by adult habitat: shallow demersal (sd); deep demersal (dd); coastal pelagic (cp); ocean epipelagic (op); mesopelagic (mp); bathypelagic (bp); (nd) not determined; (CS) Taxa present in both months. Number in parentheses is the percentage by respective oceanographic survey. Bold numbers represent the geometric mean of the larval abundance by sample ± standard deviation. survey July-07 may-08 survey July-07 may-08 Total CS

cp mp 5399(37.9) 4571(32.2) 30 ± 8.5 63 ± 6.1 14253(61.6) 2972(12.9) 187 ± 3.6 29 ± 6.5 sd 57 (58.8) 68 (61.8) 91 34

cp 19 (19.6) 19 (17.3) 25 13

Larval abundance sd op bp 3205(22.6) 791(5.6) 146(1.0) 56 ± 3.1 13 ± 3.9 2 ± 3.3 5216(22.6) 504(2.1) 143(0.6) 91 ± 2.9 5 ± 4.5 2 ± 3.1 Number of species mp op bp 10 (10.1) 5 (5.2) 3 (3.1) 9 (8.2) 5 (4.5) 5 (4.5) 12 6 5 7 4 3

B. bathymaster decreases south of the Jalisco and Colima area in the Gulf of Tehuantepec, where they represent between 31 to 45% of the total catches. There are no previous studies describing the seasonal or spatial variations in the abundance of this species. However, Aceves– Medina et al. (2003) found that B. bathymaster larvae were less abundant in the Gulf of California during the warm regime registered in the Pacific Ocean after 1975 than during the cold regime 1950–1975 Moser et al. (1974). Distribution of B. bathymaster in the American Pacific Ocean has been determined from adult records in the Gulf of California and Panama (http://www.fishbase.org; Bianchi, 1991; Tapia–García et al., 1994; Castro–Aguirre et al., 1999; Fröese & Pauly, 2009), and by the presence of larvae between both areas (Franco–Gordo et al., 2001; Siordia-Cermeño et al., 2006). In our surveys, several juveniles of B.

dd 58(0.4) 1.2 ± 2.3 28(0.1) 1 ± 1.8

nd 38(0.3) 1±2 9(0.03) 1.1 ± 1.4

Total 14208 280 ± 3 23125 452 ± 2.4

dd 1 (1) 3 (2.7) 3 1

nd 2 (2.1) 1 (0.9) 3

Total 97 110 145 62

bathymaster were collected in the Bongo nets from the coastal sampling stations off Bahía Tangolunda and Salina Cruz. In addition to these juvenile records, during the spring survey an adult specimen of 7 cm LP with a Petersen drag of 5 K off Puerto Escondido (15° 50’ N; 97° 9’ W) was collected at a 160 m depth (Bastida– Zavala, com. pers). Although the juveniles were not included in the larval abundance data, because the ichthyoplankton protocol analysis excludes them (Smith & Richardson, 1979), the high abundance of B. bathymaster and the presence of juvenile and adults suggest the importance of the Gulf of Tehuantepec as a reproduction, nursery and recruitment area for this species, which although it has no commercial value, it is ecologically relevant in the oceanic trophic webs (Zavala–García & Flores–Coto, 1994; Siordia–Cermeño et al., 2006).

Figure 2. Cumulative curves for Bahía Sebastián Vizcaino (BSV; dashed-dot line); Gulf of California (GC; dashed line); observed data for the Gulf of Tehuantepec (GT Obs; dotted line) and adjusted curve for the Gulf of Tehuantepec (GT Calc; continuous line).

LÓPEZ-CHÁVEZ et al.

Table 5. Comparative list of species richness (R) and families (NF) by sampling region in the northern hemisphere of the Eastern Pacific including the total number of samples collected (NS) and the mode (M) of the number of taxa by positive station. (ND) = No available data.

California Current Sebastián Vizcaíno Gulf of California Jalisco-Colima Gulf of Tehuantepec Eastern Tropical Pacific Costa Rica Dome

NS 31,214 377 464 132 68 482 ND

R 249 208 283 102 145 ND ND

M 6 8 4 ND 18 ND ND

Other coastal pelagic species also included between the most abundant species of the Gulf of Tehuantepec, were Opisthonema sp. 1, Opisthonema sp. 3 and Cetengraulis mystice� tus; all of them have commercial and/or ecological relevance. The Opisthonema morpho-types (sp. 1 and sp. 2) were identified according to Funes–Rodríguez et al. (2004) and based on the number of miomers and the pigmentation pattern in the cephalic region as well as in the caudal region below the notochord. During the identification processes of fish larvae from the Gulf of Tehuantepec, we observed a number of larvae different from Opisthonema sp. 1 and Opisthonema sp. 2, because of the presence of a group of pigments in the anal region. These specimens were designated as Opisthonema sp. 3. Opisthonema sp. 1 was present only during the spring survey, while Opisthonema sp. 3 was found in both seasons. Three Opistho� nema species are distributed in the area (O. lib� ertate, O. bulleri and O. medirastre) However, until now it is not possible to assign the species name to any of the three types found (Funes– Rodríguez et al., 2004). The finding of a third morphotype of Opisthonema offers a possibility to obtain meristic and morphometric data useful in future work in the description of these larvae at species level. The second most abundant species in the Gulf of Tehuantepec was Vinciguerria lucetia, which together with other mesopelagic species such as Benthosema panamense, Diaphus pacificus and Diogenichthys laternatus are characteristics of the oceanic ecosystem of the Gulf of Tehuantepec and other regions of the Pacific Ocean (Moser & Smith, 1993; Aceves– Medina et al., 2004; Funes–Rodríguez et al., 2006). An important characteristic of the larval fish assemblage of the Gulf of Tehuantepec is the high larval abundance of shallow demersal species such as Syacium, Bothus and Pontinus along with many others, which together represented 22 % of the abundance. This feature,

NF. ND 78 53 ND 55 56 37

Source Moser & Smith, 1993 Jiménez-Rosenberg et al., 2007 Aceves-Medina 2003 Franco-Gordo et al., 1999 This work Ahlstrom, 1971; Ahlstrom, 1972 Aguilar-Ibarra & Vicencio-Aguilar, 1994

along with the lower abundance of larvae of mesopelagic species during spring, is relevant since in other regions of the Eastern Pacific, including the Gulf of California, the abundance as well as the number of species from demersal environments is lower than that of mesopelagic species. That is the case off the west coast of the Baja California Peninsula, where larvae of demersal species are the most abundant, reaching 18% of the total (Jiménez–Rosenberg et al., 2000). In the Gulf of California demersal species larvae may represent 16 % of the total catches (Aceves–Medina et al., 2003). High abundance of shallow demersal species is remarkable since most of the sampling stations are far from the continental shelf in the Gulf of Tehuantepec. Presence of this kind of larvae in the oceanic region suggests oceanographic processes that transport fish larvae of neritic species off the Gulf of Tehuantepec, and could explain also the lower abundance of larvae of mesopelagic species. These processes may play a key role in the recruitment to the adult fish populations and should be studied in a multidisciplinary context. Cumulative curves show that with the same sampling effort it is possible to obtain larvae of almost 33% more species than in the Gulf of California (Aceves–Medina et al., 2003), and 60% more species than in Bahía Sebastián Vizcaíno (Jiménez–Rosenberg et al., 2007). Alpha diversity is also higher since the number of species per sample in the Gulf of Tehuantepec is more than twice than in any other region studied in the Eastern Pacific. These results indicate that the Gulf of Tehuantepec is an important reproduction area, mainly of species of coastal pelagic and demersal environments. Even to family level, the Gulf of Tehuantepec has a higher diversity than that found in the Domo de Costa Rica and is quite similar to that found in the whole area of the Eastern Tropical Pacific between 20º N and 20º S (Table 5). The species richness found showes the importance of this region, and diversity indices suggest that the area could be considered one of the areas

FISH LARVAE FROM THE GULF OF TEHUANTEPEC

of highest diversity in the Mexican Pacific, even when compared with the Gulf of California, considered one of the most diverse ecosystems in the Eastern Pacific (Walker, 1960; Thompson et al., 1979; Castro–Aguirre et al., 1995; Aceves–Medina et al., 2003). Although the primary production of the Gulf of Tehuantepec is lower than that found in the upwelling ecosystems of middle latitudes of the Eastern Pacific (Ortega–García et al., 2000), this region, together with the Gulf of Papagayo and the Domo de Costa Rica, represents the only known source of enrichment by nutrients supply to the surface along the entire area of the Central America Pacific coast (Ortega–García et al., 2000). This together with the high species richness found, make the Gulf of Tehuantepec a key area in the understanding of the oceanic ecosystems from low latitudes, which are poorly studied. ACKNOWLEDGEMENTS We thank the Instituto Politécnico Nacional, Secretaria de Investigación y Posgrado IPN and Consejo Nacional de Ciencia y Tecnología for the funding through the projects SIP-20090303; SIP-20090421; SIP-20120878 and CONACYT 90331. We also thank to the Secretaría de Marina- Dirección General Adjunta de Oceanografía, Hidrografía y Meteorología; Jefatura de la Estación de Investigación Oceanográfica of Salina Cruz, the survey chief José Paul Murad Serrano and the crew of the Hydrographic Vessel ARM BI-03 “ALTAIR”. Many thanks to Dr. Donald W. Johnson for the English edition on the manuscript. GAM, RJSM and SPAJR are EDI, COFAA and SNI fellows. REFERENCES Acal, D. E. & A. Arias. 1990. Evaluación de los recursos demerso-pelágicos vulnerables a redes de arrastre de fondo en el sur del Pacífico de México. Cienc. Mar., 16: 93-129. Aceves-Medina, G. 2003. Grupos de larvas de peces recurrentes en la costa de Baja California Sur y región central del Golfo de California. Doctoral thesis. CICIMAR-IPN, La Paz. B.C.S. México. 132 p. Aceves–Medina, G., S. P. A Jiménez–Rosenberg, A. Hinojosa-Medina, R. Funes–Rodríguez, R. J. Saldierna, D. Lluch–Belda, P. E. Smith & W. Watson. 2003. Fish larvae from the Gulf of California. Sci. Mar., 67: 1-11. Aceves–Medina, G., S. P. A. Jiménez–Rosenberg, A. Hinojosa–Medina, R. Funes– Rodríguez, R. J. Saldierna & P. E. Smith. 2004. Fish Larvae assemblages in the Gulf

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CICIMAR Oceánides 27(2): 13-26 (2012)

METABOLIC SCALING REGULARITY IN AQUATIC ECOSYSTEMS Salcido-Guevara, L. A.1, F. Arreguín-Sánchez1,*, L. Palmeri2 & A. Barausse2 Centro Interdisciplinario de Ciencias Marinas del IPN, Apartado Postal 592, La Paz, Baja California Sur, México LASA, Dip. di Processi Chimici dell’Ingegneria, Università di Padova via Marzolo 9, 35131 Padova, Italy. email: salcidog@gmail.com 1 2

ABSTRACT. We tested the hypothesis that ecosystem metabolism follows a quarter power scaling relation, analogous to organisms. Logarithm of Biomass/Production (B/P) to Trophic Level (TL) relationship was estimated to 98 trophic models of aquatic ecosystems. A normal distribution of the slopes gives a modal value of 0.64, which was significantly different of the theoretical value of 0.75 (p<0.05). After correction for transfer efficiency among trophic levels a modal value of 0.726 was obtained through a least squares algorithm which was not significantly different from the theoretical one (p>0.05). We also tested for error in both variables, Log (B/P) and TL, through a Reduced Major Axis regression with similar results, with a modal value of 0.756 (p>0.05). We also explored a geographic distribution showing no significant relation (p>0.05) to latitude and between different regions of the world. We conclude that: a) ecosystem metabolism follows the quarter-power scaling rule; b) transfer efficiency between TL plays a relevant role characterizing local attributes to ecosystem metabolism; and c) there is neither latitudinal nor geographic differences. These findings confirm the existence of a metabolic scaling regularity in aquatic ecosystems.

Keywords: Ecosystem, metabolism, scaling factor, transfer efficiency Regularidad del escalamiento metabólico en ecosistemas acuáticos RESUMEN. Se contrastó la hipótesis de que el metabolismo de un ecosistema sigue una relación de escalamiento análoga a la existente en los organismos. La relación entre el logaritmo de la razón Producción/ Biomasa (B/P) y el nivel trófico (TL) se estimó para 98 modelos tróficos de los ecosistemas acuáticos. Una distribución normal de las pendientes de esta relación produjo un valor modal de 0.64 que es significativamente diferente del valor teórico de 0.75 (p<0.05). Después de realizar una corrección considerando la eficiencia de transferencia entre niveles tróficos, se obtuvo un valor modal de 0.726, el cual fue obtenido a través de un algoritmo de mínimos cuadrados, que generó un valor significativamente (p>0.05) similar al teórico esperado. También se contrastó la hipótesis de existencia de error en ambas variables, logaritmo (B/P) y TL, a través de la técnica de regresión denominada “Reduced Major Axis”, con resultados similares según el valor modal de 0.756, sin diferencia estadísticamente significativa (p>0.05) del valor teórico. Se exploró la existencia de algún patrón en la distribución geográfica, sin obtenerse relación significativa (p>0.05) con la latitud, o con diferentes regiones del mundo. Las conclusiones son: a) el metabolismo del ecosistema sigue la regla de escalamiento metabólico de 3/4; b) la eficiencia de la transferencia entre TL desempeña un papel relevante, representando los atributos locales del metabolismo del ecosistema; c) no hay una diferencias latitudinal o geográfica. Estos resultados confirman la existencia de una regularidad en el escalamiento metabólico en ecosistemas acuáticos.

Palabras clave: Ecosistema, metabolismo, factor de escalamiento, eficiencia de transferencia. Salcido-Guevara, L. A., F. Arreguín-Sánchez, L. Palmeri & A. Barausse. 2012. Metabolic scaling regularity in aquatic ecosystems. CICIMAR Oceánides, 27(2): 13-26.

INTRODUCTION Mass and size of organisms are key attributes associated to metabolism and consequently of great interest for managing natural resources. A number of contributions discuss metabolic regularities in a wide range of living organisms, from unicellular to higher complex living systems, including plants and animals, individuals and populations (West et al., 2001; Savage et al., 2004; Brown et al., 2004). The concept has also been extended to ecosystems accounting for the metabolism of individual organisms with different life histories (Ernest et al., 2003; West & Brown, 2004; Brown et al., 2002). Such metabolic regularities are represented by the allometric relation Y Mb, where Y=metabolic rate, M=body mass and b= 0.75. The concept behind the slope value is referred as “quarter-power” scaling or “3/4-power law” (Savage et al., 2004) and represents the scaling factor between metabolic rate and indiFecha de recepción: 8 de marzo de 2012

vidual mass, where the quarter scaling, instead of 2/3 derived from size dimensions, is associated to network constrains for energy transport and their assimilation within the living systems which are characterized by having a hierarchical branching structure through which energy flows (West & Brown, 2004; West et al., 1997; Banavar et al., 2002). A similar process has been suggested at ecosystem level where trophic relationships are arranged like a branching structure with a source of energy represented by primary producers on the base of the trophic pyramid, and the prey-predator relations as the branches or pathways through which energy flows; such structures representing the food web. In an ecosystem context the 3/4-power law is also expected to represent metabolism as a process analogous to that of individual organisms (West & Brown, 2005). Fecha de aceptación: 30 de julio de 2012

SALCIDO-GUEVARA et al.

Some authors (West & Brown, 2004; 2005) present an allometric relation representing several species for different levels of complexity suggesting metabolic regularity at ecosystem level such as that observed for individuals and populations. MATERIALS AND METHODS The information used comes from 98 trophic models for aquatic ecosystems worldwide (see list of models in Annex) comprising lakes, oceanic waters, continental shelf, coral reefs, coastal lagoons, rivers, bays, reservoirs and insular systems (Figure 1), most of them exploited and few unexploited. It is not possible to know the quality of the data in most models, because it does not have an estimate of the pedigree index. However, only eight models have an average pedigree index of 0.53, which indicates that they possess an acceptable quality. Trophic models were constructed using Ecopath with Ecosim suite of programs (Christensen & Pauly, 1992), which is based in one master equation that represents the balance between production and losses for each functional groups and the whole ecosystem:

where Bi is biomass of group i ; is production/biomass ratio of i, which is equal to the total mortality coefficient (Z) under steady-state conditions (Allen, 1971; Merz & Myers, 1998); EEi is ecotrophic efficiency which is the part of the total production that is consumed by predators or exported out of the system; Bj is the biomass of predator j; is the consumption/ biomass ratio of predator j; DCji is the proportion of prey i in the diet of predator j; EXi is the export of group i, which in this study consists of fisheries catch when a group is exploited; Ei is net migration and BAi is biomass accumulation. To test for metabolic regularity at ecosystem level, we used the relationship between metabolic rate, expressed by , in respect to size, represented by trophic level of group i (TLi). This assumes that a trophic level has a direct and negative relationship with the biomass of the compartment according to the pyramid of biomass (Lindeman, 1942). Biomass/Production ratio (B/P) reflects the proportion of production (P) sustaining a given biomass (B), related to organisms size and longevity (Pauly & Christensen, 1993) reflecting attributes related to metabolism. For a given population, energy is gained through assimilation stored as biomass and removed by respi-

ration and biomass mortality (Allen, 1971). In a stable population mortality equals production, meaning sustained biomass through metabolism. Evidently, for consumers, energy gained comes from preys and in an ecosystem this is represented by trophic relationships between individuals and the food web as a structural attribute. as:

In our case, the trophic level is estimated

where TLj is the trophic level of predator j, DCji represents the proportion of preys i in the diet of predator j, TLi is the trophic level of prey i; and the sum represents diet composition of predator. In addition, transfer efficiency (TEi), between TL’s was also considered since this process can be different for similar groups between ecosystems depending of the topological and functional configuration of each system. TEi is computed as follows:

TEi being the proportion of energy transferred by predation and export. Correction of the exponent We used the slope (βTE) of the relationship Log TEi vs. TLi to correct the slope (β0) of the relationship vs. TLi as = α0 + β0 TLi, where β0= βBP (1+βTE), where bBP and βTE are the slopes in figure 2 of and Log TEi changes with TLi, and α0, is a normalization constant independent of TLi. RESULTS AND DISCUSSION vs. TLi expresses a linear equation (Figure 2A), where the slope represents the exponential rate of change of with TLi, meaning how production is used to sustain biomass when flowing through the food web in a process that reflects ecosystem metabolism; and TLi linearly relates to logarithm of biomass (Jennings et al., 2001). Based on literature (West et al., 1997; West & Brown, 2005; Banavar et al., 1999), it is expected as null hypothesis (metabolic regularity) a slope value of b=0.75, while the ordinate is assumed normalization constant.

METABOLIC SCALING REGULARITY

Figure 1 Ecosystem distribution of 98 models used in this paper (see annex for details). Numbered areas indicate regions used to look for geographic patterns. Black dots indicates models used for computations, white dots not used models.

Distribution of β values for the 98 ecosystems (see Annex) is shown in figure 3A, with a mean of b=0.64 (standard deviation of d=0.19) significantly different to the expected 0.75 value (p<0.05). b<2/3 has been interpreted as that the network is not fully representing a real ecosystem (Bendoricchio & Palmeri, 2005); or that differences from 0.75 are stemming from network inefficiencies (Banavar et al., 2002). Taking into account the process shown in figure 2A, the slope may approach 0.75 if , increases for higher TLi’s or diminishes for lower TLi’s. In theory this could happen with biomass changes accumulated within respective TLi’s, process,

which is inherent to Transfer Efficiencies (TEi) between TLi’s. It has been demonstrated that changes in TEi would alter scaling exponent of abundance (i.e. as biomass) with mass (Jennings et al., 2002; Jennings & Mackinson, 2003), and particularly that changes in TEi from 0.05 to 0.30 would alter scaling exponent by ±0.2 (25% of the exponent theoretical value of 0.75). TEi’s in ecosystem models, as estimated by Ecopath, vary between TL’s, despite of the 10% reported as average value, and between ecosystems (Pauly & Christensen, 1995). The 3/4-power law assumes distribution of energy

Figure 2. A) Trend of Biomass / Production ratio over trophic level, and B) Trend of transfer efficiency with trophic level for the Central Pacific ecosystem (Kitchell et al., 2002).

SALCIDO-GUEVARA et al.

Figure 3. Slope distribution of log (B/P) versus TL for ecosystem models showing a normal-type distribution with (A) a modal value b =0.64 and δ=0.19, (B) modal value b0=0.726 and δ =0.25 after TE correction, both solved by a least squares algorithm, (C) a modal value of b0=0.756 and δ =0.193, solved by Reduced Major Axis regression. First modal value was significantly different of the theoretical value of 0.75 (p<0.05), other were not significantly different (p>0.05).

along living systems having the same efficiency (in circulatory system it is expressed as maintenance of a constant nutrient deliverable rate per unit volume of body; Banavar et al., 2002). This assumption is not fulfilled in many trophic webs represented by biomass flows, where TEi tends to decrease with TLi (Figure 2B). For this reason the slopes (β0) were corrected obtaining a new set of vs. TLi for 95 ecosystems (Figure 3B) with a mean value of β0=0.726 (d=0.25), showing a non-significant difference from the 0.75 value (p>0.05). Since ecosystem models used here come from different parts of the world, we searched for geographic patterns of β0 values; specifically for latitudinal changes. Figure 1 shows ecosystems locations, and areas drawn indicate latitudinal groups for selected regions to explore for patterns. Values for β0 (Table 1) did not show statistical differences between them (p>0.05) nor with zero, which means there is not latitudinal gradient and confirm existence of a global pattern. Previous references to scaling regularity for ecosystem metabolism have used information

of specific species (West & Brown, 2004; 2005) and their masses not belonging to the same food web. Here we used information of 95 aquatic ecosystems of different regions of the world where their TLi’s were estimated through diet composition data. Slopes of and Log TEi, with TLi, represent ecosystem attributes related to ecosystem structure and function. In contrast with some previous analysis (Garlaschelli et al., 2003) our results confirm the hypothesis that ecosystems metabolism follows the 3/4-power law, transfer efficiency being a key process. Considering the quantitative analysis, ordinary least squares regression assumes that Table 1. Results for the relationships between β0 (slope of the relationship Log(B/P) vs. TL corrected by βTE) vs. Latitude for selected regions of the world shown in figure 1. No one slope was significantly different of b=0 (p>0.05) around b0=0.75. C.I. is the confidence interval of the β0 and r the coefficient of correlation. Region

β0

βTE

1 2 3 4 5 6

0.6786 0.7763 1.2897 0.9550 0.8250 0.6495

-0.0016 -0.0043 -0.0083 -0.0083 -0.0082 -0.0031

+/-95% C.I. 0.0052 0.0072 0.0253 0.0154 0.0243 0.0038

r 0.15 0.27 0.21 0.36 0.18 0.35

METABOLIC SCALING REGULARITY

error exists only in the dependent variable, resulting potentially in biased results when the assumption is not met. In our data trophic level was probably also measured with error. To test for this effect in our estimates of β0, we alternatively applied the Reduced Major Axis (RMA) analysis (Sokal & Rohlf, 1981; Bohonak & van der Linde, 2004) on both, and Log TEi, with TLi relationships. RMA assumes both variables are measured with error. Results indicate an estimation of β0=0.756 (δ=0.193) and, after the same consideration with respect to TEi, results shows a non-significant difference from the 0.75 value (p>0.05), which confirm the 3/4-power law (Figure 3C). Results provide evidence of regularity of aquatic ecosystems metabolism. Such regularity is maintained independently of the type of ecosystem or the region of the world. Despite of their emergent metabolism regularity, there are particularities for individual ecosystems given by specific transfer efficiencies, attribute that could be of relevance for local considerations. As conclusion, our findings confirm the concept that complex living systems also follow the 3/4-metabolism scaling rule as a global regularity (West & Brown, 2005; Brown et al., 2007; Banavar et al., 2010). ACKNOWLEDGMENTS Authors thank Luis Capurro, Steve Mackinson and Daniel Pauly for their valuable comments and suggestions to an early versions of this manuscript. Authors also thank partial support through projects CONACyT (SEP-CONACYT 104974 and ANR-CONACyT 111465); GEF-UNIDO-SEMARNAT LME-Gulf of Mexico, Incofish (EC-003739); and also to the National Polytechnic Institute through SIP-20121444, EDI and COFAA. REFERENCES Allen, K.R. 1971. Relation between production and biomass. J. Fish. Res. Board Can., 28(10): 1573-1581. DOI: 10.1139/f71-236 Bohonak, A.J. & K. van der Linde. 2004. RMA: Software for Reduced Major Axis regression, Java version. Available from: http:// www.kimvdlinde.com/professional/rma. html [Accessed 3 February 2012]. Banavar, J.R., A. Maritan & A. Rinaldo.1999. Size and form in efficient transportation networks. Nature, 399: 130-132. DOI 10.1038/20144 Banavar, J.R., A. Maritan & A. Rinaldo.2002. Supply-demand balance and metabolic

scaling. PNAS, 99(16): 10506-10509. DOI: 10.1073/pnas.162216899 Banavar, J.R., M.E. Moses, J.H. Brown, J. Damuth, A. Rinaldo, R.M. Sibly & A. Maritan. 2010. A general basis for quarter-power scaling in animals. PNAS. 107(36): 1581615820. Bendoricchio, G. & L. Palmeri. 2005. Quo vadis ecosystem? Ecol. Model., 184(1): 5-17. DOI: 10.1016/j.ecolmodel.2004.11.005 Brown, J.H., K.V. Gupta, B.L. Li, B.T. Milne, C. Restrepo & G.B. West. 2002. The fractal nature of nature: power laws, ecological complexity and biodiversity. Philos. T. Roy. Soc. B., 357: 619-626. DOI: 10.1098/ rstb.2001.0993 Brown, J.H., J.G. Gillooly, A.P. Allen, V.M. Savage & G.B. West. 2004. Towards a metabolic theory of ecology. Ecology, 85(7): 1771-1789. DOI: 10.1890/03-9000 Brown, J.H., A.P. Allen & J.F. Gillooly. 2007. The metabolic theory of ecology and the role of body size in marine and freshwater ecosystems, 1-10. In: Hildrew A.G., Raffaelli D.G. & R. Edmonds-Brown (Eds.) Body Size: the structure and function of aquatic ecosystems. Cambridge University Press, New York, 356 p. Christensen, V. & D. Pauly, 1992. ECOPATH II – a software for balancing steady-state ecosystem models and calculating network characteristics. Ecol. Model., 61: 169-185 (www.ecopath.org) DOI: 10.1016/03043800(92)90016-8 Ernest, S.K.M., B.J. Enquist, J.H. Brown, E.L. Charnov, J.F. Gillooly, V.M. Savage, E.P. White, F.A. Smith, E.A. Hadly, J.P. Haskell, S.K. Lyons, B.A. Maurer, K.J. Niklas & B. Tiffney. 2003. Thermodynamic and metabolic effects on the scaling of production and population energy use. Ecol. Lett., 6: 990-995. DOI: 10.1046/j.14610248.2003.00526.x Garlaschelli, D., G. Caldarelli & L. Pletonero. 2003. Universal scaling relations in food webs. Nature, 423: 165-168. DOI: 10.1038/ nature01604 Jennings, S., K.J. Warr & S. Mackinson. 2002. Use of size-based production and stable isotope analyses to predict trophic transfer efficiencies and predator-prey body mass ratios in food webs. Mar. Ecol. Prog. Ser., 240, 11-20. DOI: 10.3354/meps240011

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Pauly, D. & V. Christensen. 1995. Primary production required to sustain global fisheries. Nature, 374: 255-257. DOI: 10.1038/374255a0

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Kitchell, J.F., T.E. Essington, C.H. Boggs, D.E. Schindler & C.J. Walters. 2002. The role of sharks and longline fisheries in a pelagic ecosystem of the Central Pacific. Ecosysďż˝ tems, 5(2): 202-216. DOI: 10.1007/s10021001-0065-5 Lindeman, R.L. 1942. The trophic-dynamic aspect of ecology.Ecology, 23(4): 399-417. Available from: ftp://brd1.ucsc.edu/Bio293/ week2/Lindeman%201942.pdf [Accessed 7 June 2012] Merz, G. & R.A. Myers. 1998. A simplified formulation for fish production. Can. J. Fish. Aquat. Sci., 55(2): 478-484 Pauly, D. & V. Christensen. 1993. Graphical representation of steady-state trophic ecosystem models, 20-28. In: Trophic models of aquatic ecosystems, Christensen, V. & D. Pauly (Eds.). Philippines, ICLARM Conf. Proc. 26. ISBN: 971-1022-84-2

Sokal, R.R. & F.J. Rolf. 1981. Biometry. 2nd ed., San Francisco, California, W.H. Freeman. ISBN: 0716712547 West, G.B. & J.H. Brown. 2004. Lifeâ&#x20AC;&#x2122;s universal scaling laws. Phys. Today, 57(9): 36-42. DOI: 10.1063/1.1809090 West, G.B. & J.H. Brown. 2005. The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J. Exp. Biol., 208: 15751592. DOI: 10.1242/jeb.01626 West, G.B., J.H. Brown & B.J. Enquist. 1997. A general model for the origin of allometric scaling laws in biology. Science, 276(5309): 122-126. DOI: 10.1126/science.276.5309.122 West, G.B., J.H. Brown & B.J. Enquist. 2001. A general model for ontogenic growth. Nature, 413: 628-631. DOI: 10.1038/35098076

Region I Prince William Sound Ecosystem, Alaska Prince William Sound old model, Alaska North British Columbia 1750, Canada North British Columbia 1900, Canada Alto Golfo de California, Mexico Central Gulf of California, Mexico Southern of Gulf California, Mexico Gulf of Nicoya, Costa Rica Golfo Dulce, Costa Rica Monterey Bay, United States La Paz Bay, Mexico Rivers Inlet 1950, Canada Rivers Inlet 1990, Canada Huizache-Caimanero, Mexico Sharks in Central Pacific Region II Campeche Sound, Mexico Northern Gulf of St. Lawrence, Canada Seagrass in St. Marks, United States Bahia Ascencion, Mexico Celestun Mangrove, Mexico Terminos Lagoon, Mexico Looe Key National Marine Sanctuary, United States Coral Reef Mexican Caribbean Lake Ontario, Canada Upwelling Gulf of Salamanca, Colombia Weat Greenland Campeche Sound, Mexico Terminos Lagoon, Mexico Mandinga Lagoon, Mexico Tampamachoco Lagoon, Mexico Celestun Lagoon, Mexico

Ecosystem name 61 61 52 52 30.5 29.5 22.3667 10.0167 8.5 37 24.5 51.3333 51.3333 23 40 19 48.5 30 19.75 20.75 18.3333 24.5333 21 43.5 11.0833 64 20 18.5 19 21 21

-146 -136 -136 -113.5 -112.5 -105.8333 -85 -83.2667 -122 -110.5 -128 -128 -106.05 -150 -93 -63 -84.5 -87.5 -90.25 -91.1667 -81.4 -86 -78.5 -74.5 -55 -91.5 -91.5 -96 -97.5 -90.5

Latitude

-146

Longitude

Continental shelf Continental shelf Continental shelf Coastal lagoon Coastal lagoon Coastal lagoon

Coral reef Lake Continental shelf

Coral reef

Bay Coastal lagoon Coastal lagoon

Bay

Continental shelf

Continental shelf Continental shelf Bay Bay River River Coastal lagoon Oceanic

Continental shelf

Continental shelf Continental shelf

Continental shelf

12 19 20 20 23 16

18 14 18

19 19 16

21 21 16 22 32 32 26 22

29 27

Number of Type of ecosystem functional groups

1 (1) 1 (1) 2 (1) 1 (1) 2 (1) 2 (1)

2 (1) 1 (1) 2 (1)

2 (1)

2 (1) 2 (1) 2 (1)

5 (1)

1 (1)

2 (1)

3 (1) 2 (1) 3 (1) 2 (1) 2 (1) 2 (1) 2 (1) 1 (1)

2 (1)

2 (1) 1 (1)

2 (1)

4 (2)

Number of PP (incluiding detritus)

0.5034 0.6469 0.8613 0.8523 0.4242 0.6187

0.4518 0.6086 0.6006

0.4467

0.763 0.4079 0.7912

0.2889

0.5911

0.5152

0.5492 0.7867 0.7021 0.5318 0.5562 0.5626 0.6528 0.6132

0.3416

0.7674 0.578

0.2583

0.2598

0.7354

0.6517

βPB

0.0797 -0.0796 0.0245 -0.5165 -0.1662 0.0195

-0.2789 -0.0626 0.0441

-0.1969

-0.0879 -0.1576 0.0949

-0.2218

-0.0183

-0.0876

0.0615 0.1285 -0.071 -0.0263 -0.174 -0.1461 -0.0754 -0.2244

0.0172

0.0322 -0.0044

-0.1091

-0.1032

-0.0637

-0.0662

βTE

0.5435 0.6984 0.8824 1.2925 0.4947 0.6307

0.5778 0.6467 0.6271

0.5347

0.83 0.4722 0.8663

0.353

0.6019

0.5603

0.583 0.8878 0.752 0.5458 0.653 0.6448 0.702 0.7508

0.3475

0.7921 0.5805

0.2865

0.2866

0.7823

0.6949

β0

0.657 0.736 1.047 0.481 0.484 0.808

0.562 0.752 0.637

0.721

0.853 0.663 1.047

0.686

0.575

0.657

0.905 0.932 0.725 0.612 0.597 0.602 0.686 0.484

0.548

0.748 0.79

0.648

0.642

0.809

0.727

β0,RMA

(24) (25) (26) (27) (28) (29)

(21) (22) (23)

(20)

(17) (18) (19)

(16)

(15)

(14)

(7) (8) (9) (10) (11) (11) (12) (13)

(6)

(4) (5)

(3)

(2)

(1)

Reference

Annex. Names and some attributes for the ecosystems used in this contribution. For more details about models and documentation related please visit www.ecopath.org. PP = primary producers; βBP = slope relationship Log(B/P) vs. TL; βTE = slope relationship Log(TE) vs. TL; β0 = slope of the relationship Log(B/P) vs. TL corrected by βTE. (least squares regression); β0,RMA = slope of the relationship Log(B/P) vs. TL corrected by βTE (Reduced Major Axis regression).

METABOLIC SCALING REGULARITY 19

Region III Iceland 1950 Seine Estuary, France Lagoon of Venice, Italy Gironde Estuary, France Etang de Thau, France Orbetello Lagoon, Italy Garonne River, France Lake Aydat, France Ria Formosa lagoonal system, Portugal Baltic Sea Region IV Lake Kinneret, Israel Lake Turkana 1973, Kenya Lake Turkana 1987, Kenya Lake George, Uganda Lake Victoria, Kenya Lake Tanganyica, Africa Lake Kariba, Zimbabwe Lake Malawi Sri Lankan Reservoir, Sri Lanka Region V Brunei Darussalam, Philippines Coast of Sarawak, Malaysia Coast of Sabah, Malaysia Kuosheng Bay, Taiwan San Miguel Bay, Philippines San Pedro Bay, Philippines Bolinao Coral Reef, Philippines Laguna de Bay 1820, Philippines Laguna de Bay 1920, Philippines Laguna de Bay 1950, Philippines Laguna de Bay 1968, Philippines Laguna de Bay 1980, Philippines Laguna de Bay 1990, Philippines Region VI Brunei Darussalam, Philippines Coast of Sarawak, Malaysia Coast of Sabah, Malaysia Peninsula Malaysia, Malaysia North Coast of Central Java, Indonesia Kuosheng Bay, Taiwan San Miguel Bay, Philippines San Pedro Bay, Philippines Bohai Sea, China

Ecosystem name

Annex. Continued.

62 49.4417 45.5 45 43.5 43 44 45.5 37.0333 60 33 4.5 4.5 0 -1 -7 -16.5 -9.5 10.75 5 4.8333 4.8333 25.2167 14 11.0917 16.4167 14.5 14.5 14.5 14.5 14.5 14.5 5 4.8333 4.8333 1 -6.5 25.2167 14 11.0917 39

20 35.5 36.5 36.5 30.2 34.5 30 29 35 35.3333 114 112.5 112.5 121.6667 123 125 119.9167 121.5 121.5 121.5 121.5 121.5 121.5 114 112.5 112.5 98 109 121.6667 123 125 120

Latitude

-11 0.1667 12.5 0 3.5 10.5 1.5 6 -7.8

Longitude

Bay Bay Bay Bay

Continental shelf

Continental shelf Continental shelf Continental shelf Continental shelf

Continental shelf Continental shelf Continental shelf Bay Bay Bay Coral reef Lake Lake Lake Lake Lake Lake

Lake Lake Lake Lake Lake Lake Lake Lake Reservoir

Oceanic

Continental shelf Coastal lagoon Coastal lagoon Coastal lagoon Coastal lagoon Coastal lagoon River Lake Reservoir

Type of ecosystem

17 16 16 13

13 29 29 15

13 29 29 17 16 16 26 30 26 21 16 17 20

14 8 8 14 16 7 10 9 17

24 15 16 18 11 12 10 11 14

Number of functional groups

2 (1) 1 (1) 2 (1) 1 (1)

2 (1)

1 (1) 2 (1) 2 (1) 1 (1)

1 (1) 2 (1) 2 (1) 2 (1) 1 (1) 2 (1) 3 (1) 2 (1) 2 (1) 2 (1) 2 (1) 2 (1) 2 (1)

2 (1) 1 (1) 1 (1) 2 (1) 2 (1) 1 (1) 3 (1) 1 (1) 4 (1)

2 (1)

2 (1) 2 (1) 2 (1) 2 (1) 2 (1) 2 (1) 2 (1) 2 (1) 1 (1)

Number of PP (incluiding detritus)

0.2796 0.6384 0.3798 0.5968

0.4502

0.6865 0.6245 0.5432 0.4885

0.6865 0.6245 0.5432 0.2796 0.6384 0.3798 0.2825 0.8666 0.8694 0.8308 0.6789 0.8196 0.7523

0.585 0.7669 0.7675 0.6739 0.6889 0.8654 0.6669 1.1651 0.6517

0.782

0.808 0.5473 0.5443 0.9351 0.4755 0.6486 0.8197 0.787 1.2186

βPB

-0.1168 0.0361 0.1122 -0.0097

0.0663

-0.1483 -0.0914 -0.0659 0.0257

-0.1483 -0.0914 -0.0659 -0.1168 0.0361 0.1122 0.0242 -0.1297 0.1759 0.0136 0.1975 0.2024 0.2787

-0.2667 -0.2898 -0.3224 0.0406 -0.166 -0.028 -0.2188 -0.5119 0.1129

-0.1419

-0.0876 -0.2172 -0.1148 0.0223 0.1567 -0.1473 -0.8516 0.0473 -0.0686

βTE

0.3123 0.6615 0.4224 0.6026

0.4801

0.7883 0.6816 0.579 0.5011

0.7883 0.6816 0.579 0.3123 0.6615 0.4224 0.2893 0.979 1.0223 0.8421 0.813 0.9855 0.962

0.741 0.9892 1.015 0.7012 0.8033 0.8896 0.8128 1.7615 0.7253

0.893

0.8788 0.6662 0.6068 0.956 0.55 0.7442 1.5178 0.8242 1.3022

β0

1.138 0.755 0.546 0.626

0.961

0.732 0.741 0.658 0.62

0.732 0.741 0.658 1.138 0.755 0.546 0.614 0.652 0.874 0.719 0.548 0.763 0.801

1.008 0.643 0.604 0.958 0.782 0.846 0.917 0.658 1.267

0.816

0.777 0.829 0.836 1.502 0.777 0.693 0.093 0.669 0.894

β0,RMA

(50) (51) (52) (57)

(56)

(48) (49) (49) (55)

(48) (49) (49) (50) (51) (52) (53) (54) (54) (54) (54) (54) (54)

(40) (41) (41) (42) (43) (44) (45) (46) (47)

(39)

(30) (31) (32) (33) (34) (35) (36) (37) (38)

Reference

20 SALCIDO-GUEVARA et al.

Bay of Bengal, Bangladesh Bolinao Coral Reef, Philippines Northern Great Barrier Reef, Australia Central Great Barrier Reef, Australia Uvea Atoll Loyalty Islands, New Caledonia Central Pacific Ocean Subantarctic water Plateau, New Zeland Laguna de Bay 1990, Philippines Models used for BP vs TL but not for latitudinal analysis Central Chile 1992, Chile Central Chile 1998, Chile Iceland’s fisheries, Iceland South Orkneys/Georgia, British Antarctic Territory Northern Benguela, Namibia Eastern Bering Sea, United States Western Bering Sea, United States Venezuela shelf, Venezuela Southern Brazil, Brzil Barents Sea 1990 Barents Sea 1995 Southwest coast of India, India Tongo Bay, Chile Bay of Somme, France Maputo bay, Mozambique Sandy Barrier Lagoon Chiku, Taiwan Sakumo Lagoon, Ghana Mangrove in Celestun Lagoon, Mexico

Ecosystem name

Annex. Continued.

21 16.4167 -16 -18 -20.5 20 -50 14.5 -33 -33 62.5 -50 -22 52 65 10 -32.5 80 80 13 -30.2417 50.2333 -26 23.1333 5.6167 20.75

147 166.5 170 170 121.5 -73 -73 -25 -34 12 -163.5 -179.5 -62 -51 40 40 75 -71.5 1.55 33 124.0667 0.0333 -90.25

Latitude

91 119.9167 150

Longitude

Coastal lagoon Coastal lagoon

Continental shelf Continental shelf Continental shelf Continental shelf Continental shelf Bay Bay Bay Coastal lagoon

Continental shelf Continental shelf Continental shelf

Continental shelf Continental shelf Continental shelf Continental shelf

Lake

Oceanic Oceanic

Coral reef

Bay Coral reef Coral reef

Type of ecosystem

13 19

16 13 41 41 11 17 9 10 13

24 38 36

21 21 21 30

26 19

1 (1) 2 (1)

2 (1) 1 (1) 2 (3) 2 (3) 1 (1) 2 (1) 2 (1) 2 (1) 2 (1)

1 (2) 1 (3) 1 (3)

1 (1) 1 (1) 1 (1) 1 (1)

2 (1)

1 (1) 1 (2)

3 (2)

2 (1)

Number of Number of functional PP (incluiding groups detritus) 15 1 (1) 26 3 (1) 25 2 (1)

0.8797 0.4059

0.7141 0.7557 0.669 0.672 0.6101 0.606 0.7796 0.7397 0.9072

0.0269 0.7134 0.7002

0.6288 0.5728 0.9818 0.7456

0.7523

0.6399 0.7164

0.7128

0.6869

0.6806 0.2825 0.6528

βPB

-0.079

-0.108 0.1855 -0.138 -0.119 0.2447 0.0074 -0.275 0.1296

-0.05 -0.194 -0.147

-0.165 -0.183 -0.147 -0.131

0.2787

-0.0207 -0.103

-0.102

-0.131

0.1966 0.0242 -0.133

βTE

0.438

0.7909 0.8959 0.7613 0.752 0.7594 0.6105 0.9431 1.0247

0.0282 0.852 0.8031

0.7326 0.6778 1.126 0.8436

0.962

0.6532 0.7902

0.7853

0.7771

0.8144 0.2893 0.7397

β0

0.545

0.732 0.989 0.813 0.788 0.815 0.9 0.719 1.491

0.705 0.707 0.812

0.607 0.701 1.009 0.682

0.801

0.7 0.705

0.743

0.899

0.533 0.614 0.913

β0,RMA

(76) (77

(69) (70) (71) (71) (72) (73) (74) (75) (78)

(67) (68) (68)

(64) (64) (65) (66)

(54)

(62) (63)

(61)

(60)

(58) (53) (59)

Reference

METABOLIC SCALING REGULARITY 21

SALCIDO-GUEVARA et al.

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CICIMAR Oceánides 27(2): 27-35 (2012)

THE POTENTIAL EFFECT OF NITROGEN REMOVAL PROCESSES ON THE δ15N FROM DIFFERENT TAXA IN THE MEXICAN SUBTROPICAL NORTH EASTERN PACIFIC Camalich, J.1*, A. Sánchez1, S. Aguíñiga1 & E. F. Balart2 Centro Interdisciplinario de Ciencias Marinas - Instituto Politécnico Nacional. Av. Instituto Politécnico Nacional s/n Col. Playa Palo de Santa Rita Apdo. Postal 592. C.P. 23090, La Paz, B.C.S., México. 2 Centro de Investigaciones Biológicas del Noroeste. Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur; La Paz, B.C.S. México. C.P. 23096 * Corresponding author. Present address: IMARES Wagening UR, Zuiderhaaks 5 1797 SH ’t Horntje, Texel, Netherlands. 1

ABSTRACT. The sub-tropical north eastern Pacific is one of the major zones in the ocean where nitrogen is removed by bacterial processes which are enhanced by low oxygen concentrations commonly found in the water column along the Pacific coast upwelling areas. It is well established that the nitrogen isotopic signal (δ15N) increases in relation to trophic levels but little is known about the transfer of this δ15N signal from the dissolved fraction to higher trophic levels in oceanic regions with low oxygen. The objectives of this study are: 1) to report δ15N values from different abiotic and biotic components collected in the low-oxygen oceanic region in front of Bahía Magdalena (Mexican subtropical north-eastern Pacific); 2) to compare the δ15N of different trophic levels with analogous organisms in regions where nitrogen fixation is the dominating process, which will allow us to evaluate the actual transfer of δ15N enriched in 15N through the trophic web up to top predators. The δ15N was higher in both abiotic and biological compared to those reported from zones where N fixation is the dominating process. Oxygen concentrations in the oceanic area in front of Bahía Magdalena are low (< 2ml/l) at shallow water depths (< 100m) but not anoxic. Despite this we found that the δ15N signal reflects denitrification and this signal is transferred up though the food web.

Keywords: Subtropical north eastern Pacific, nitrogen cycle, δ15N, oxygen minimum zone. Efecto potencial del proceso de remoción de nitrógeno sobre el δ15N de distintos taxa en el Pacífico noreste mexicano subtropical RESUMEN. El Pacífico subtropical noroeste es una de las zonas más importantes del océano en las cuales el nitrógeno es utilizado por procesos bacterianos que se intensifican bajo condiciones bajas de oxígeno como las que se encuentran comúnmente en las zonas de surgencia a lo largo de las costas del Pacifico. El incremento en la señal isotópica de N con respecto al nivel trófico (δ15N) es bien conocido, sin embargo su transferencia desde la fracción disuelta hasta niveles tróficos altos no ha sido estudiada a profundidad en zonas del océano en las cuales las concentraciones de oxígeno son bajas. Los objetivos de este estudio son: 1) reportar valores de δ15N de diferentes compartimentos (abióticos y bióticos) recolectados en la zona oceánica de baja concentración de oxígeno frente a Bahía Magdalena (Pacifico subtropical noreste Mexicano); 2) comparar δ15N de diferentes niveles tróficos con organismos análogos de regiones en las cuales la fijación de nitrógeno es el procesos dominante; esto nos permitirá evaluar la transferencia real de δ15N enriquecido en 15N a través de la red trófica hasta depredadores tope. El δ15N de los componentes abióticos y abióticos fue más alto que los reportados en regiones con una alta tasa de fijación de N. Las concentraciones de oxígeno en la zona de estudio son bajas (< 2ml/l) a profundidades superficiales (< 100m) aunque no anóxicas. No obstante, la señal de δ15N refleja desnitrificación y esta señal es transferida a lo largo de la cadena trófica.

Palabras clave: Pacifico nororiental subtropical, ciclo del nitrógeno, δ15N, zona de mínimo oxígeno. Camalich, J., A. Sánchez, S. Aguíñiga & E. F. Balart. 2012. The potential effect of nitrogen removal processes on the δ15N from different taxa in the mexican subtropical north eastern Pacific. CICIMAR Oceánides, 27(2): 27-35.

INTRODUCTION Upwelling areas, where nutrient rich water is transferred from the deep ocean to the productive surface layers, have an important role in coastal fisheries around the world as they enhance primary productivity, which in turn allows for a higher secondary production. However, in some areas a combination of high productivity and poor water exchange can create large areas in the water column with very low oxygen concentrations (0.5 ml/l) called oxygen minimum zones (OMZ, Levin et al., 2002). Within these OMZ, processes take place which transfer nitrogen, one of the most important nutrients in the ocean, to a form which cannot be used by phytoplankton and thus result in a loss of biologically available nitrogen. The major niFecha de recepción: 9 de mayo de 2012

trogen removal processes behind this are denitrification, in which heterotrophic bacteria convert nitrate (NO3 ) to dinitrogen gas (N2), and anaerobic ammonium oxidation (anammox), where microbes use ammonium (NH4+) and nitrite (NO2 ) to produce N2 (Lam et al., 2009, Fig. 1). Although OMZ represent less than the 1% of the ocean volume worldwide, it has been estimated that as much as 20 - 40% (or approximately 200 x106 ton/year) of the oceanic nitrogen is lost in the Arabian Sea and the North and South Eastern Tropical Pacific (Codispoti et al., 2001; Devol, 2008). With the alleged warming of the oceans due to climate change, a substantial expansion of OMZ is predicted to occur (Stramma et al., 2008). Another emerging proFecha de aceptación: 5 de julio de 2012

CAMALICH et al.

0 0

[O2] ml/l 2

Upper OMZ – BM oceanic region

200 400

Upper OMZ

NO2-

Nitrification

Depth (m)

Assim.

NO3-

Norg

Lower OMZ

Remin. DNRA

Nitrate reduction

NH4+

N2 fix a tio n

Anammox

NO2-

Figure 1.The N cycle at the OMZ. The processes nitrate reduction (denitrification) and anammox can potentially increase the isotopic signal at the dissolved phase. Nitrate reduction and anammox are considered as loss of N (modified from Lam et al., 2009).

blem is the increase of coastal areas not connected to OMZ with low oxygen conditions (hypoxia), which is considered to be one of the major emerging anthropogenically induced problems (Vaquer-Sunyer & Duarte, 2008). These expansions will lead to an increase in nitrogen removal processes (Stramma et al., 2008) and could therefore cause a significant imbalance in the global budget of this important nutrient (Zehr & Ward, 2002; Zehr, 2009). Furthermore, oxygen minimum zones are inhospitable to many species and therefore serve as biogeographic barriers (Helly & Levin, 2004; Rogers, 2000) possibly causing ecological modification as some species are displaced or removed. Nitrogen is found in two stable isotopic forms in nature, the lighter 14N (99.6%) and the heavier 15N (<0.4%). Due to their difference in mass the heavier isotope reacts at a slightly slower rate compared to 14N, thereby causing chemical fractionation (Devol, 2008). In addition there are many biological reactions that can alter the ratio of heavy-to -light isotopes (Peterson & Fry, 1987), as 15N is selectively discriminated and therefore accumulates in the residual nitrogen pool. Several studies have used the stable isotopic composition of nitrogen (δ15N) to trace nitrogen removal processes. Water column denitrification in the OMZ and the incorporation of NO3 by phytoplankton in the ocean surface leads to an increase in nitrate δ15N. For

example, Brandes et al. (1998) showed that as a result of intense denitrification within the water column in the OMZ of the Arabian Sea and the eastern tropical North Pacific Ocean (ETNP), there is- a marked increase in the δ15N signal of NO3 from the deep water to the surface. In addition, a significant difference between the δ15N of nitrate measured in the North Eastern Pacific (15 ‰) and the average open ocean (5‰) has been detected due to the N removal processes in OMZ waters (Altabet et al., 1999; Brandes et al., 1998; Cline & Kaplan, 1975). Although this process is commonly known, the transference of this relatively high δ15N signal from the dissolved fraction up through the trophic web has not previously been reported in this region. Our objectives with this study are: 1) to report the δ15N from different abiotic (sediment and NO3) and biological components (phytoplankton, zooplankton, cephalopods: Dosidicus gigas, bentho-pelagic crustaceans: Pleuroncodes planipes, demersal fishes, sea lions: Zalophus californianus and dolphins: Tursiops truncatus) from the low-oxygen oceanic region in front of Bahía Magdalena, Mexico (Fig 2); 2) to highlight the potential effect of nitrogen removal process in the δ15N values from the base of the food web through top predators. Low water column oxygen concentrations favor bacterial nitrogen removal processes leaving a pool of nitrate high on δ15N. Since this signal is transferred trough the food web, our hypothesis is that higher trophic levels including

EFFECT OF NITROGEN REMOVAL PROCESSES ON δ15N

top predators are considerably more enriched in 15N than similar taxa living in regions were the δ15N at the base of the food web is lower. MATERIAL AND METHODS Samples of water, sediments, phytoplankton, zooplankton, bentho-pelagic crustaceans and demersal fishes were collected on board the research vessel BIP XII during four campaigns (March and November, 2006 and 2007) at the oceanic region in front of the Bahía Magdalena-Almejas lagoon complex (Fig. 2). Phytoplankton and zooplankton were collected simultaneously using a bongo net towed from the surface (61 cm diameter, 200 and 500 µm mesh respectively), stored in conical tubes and kept cold (4 °C) for later analysis. Sediment samples were collected at different depths (from 40 to 400 m) using a Smith-McIntyre grab and stored in clean plastic bags at -20°. Water samples were collected at 50 m and 200 m (only during November 2007) using a Niskin bottle, filtered through pre-combusted GF/F filters (0.45 µm) and stored in cleaned Nalgene bottles. The demersal fishes and the red crab (P. planipes) were collected using a bottom-trawl net with a head rope of 34 m and a 50-mm mesh size and preserved by freezing for later analysis (no P. planipes samples were collected in November 2006). Portions of muscle from stranded sea mammals were acquired by continuous patrolling along Isla Margarita (Fig 2).

Oxygen profiles The world ocean atlas is the result of a global collection of samples supported by different programs including the World Ocean Data Base (WOD) and the Global Oceanographic Data Archaeology and Rescue (GODAR). In the case of oxygen concentrations, values have in most cases been obtained by instruments mounted on oceanographic rosettes and in some cases obtained from a modified Winkler titration (ocean discrete samples in the WOD) (García et al., 2010). The data was downloaded from http://www.nodc.noaa.gov/OC5/WOA09/ woa09data.html and the profiles constructed using Ocean Data View (Schlitzer, 2011). The selection of profiles from WOA09 correspond to those closest available for our sampling stations. Stable isotope analysis Nitrogen stable isotopes from water samples were analyzed following the ammonia diffusion method from by Sigman et al. (1997) at the Facultad de Ciencias del Mar y Limnologia (UNAM-Mazatlán). Sediments were dried and approximately 20 mg were weighed and packed into tin capsules and sent to the University of Davis for the isotopic analysis. The phytoplankton and zooplankton samples were freeze-dried and set under acid environment (1N HCl) using a glass desiccator during 24 h following Lorrain et al. (2003). After

Figure 2. Map of sampling sites (•) and points selected (Δ) offshore Bahía Magdalena for the O2 profiles using WOA09 data

CAMALICH et al.

decalcification, approximately 1 mg of sample was weighed and packed into tin capsules for analysis. Samples from the giant squid (Dosidi� cus gigas) mantle were freeze-dried and 1 mg packed into tin capsules. Samples of muscle of bentho-pelagic (22 – 32 mm) red crab were scraped from the exoskeleton, freeze-dried and 1 mg packed into tin capsules for analysis. For demersal fishes a portion of dorsal muscle was freeze dried and 1mg packed into tin capsules. In the case of marine mammals the biopsies were dissected to remove the adipose tissue and rinsed in methanol before being freezedried and packed into tin capsules. The analysis reproducibility was 0.1‰ for δ15N (n = 19, UC Davis internal standard). The highest standard deviation from duplicates was 0.3‰. Literature data comparison We used the concept of N* proposed by Gruber and Sarmiento (1997) to distinguish between regions in the ocean with contrasting N processes such as removal (denitrification) and fixation. The N* concept and its mathematical development are based on a large collection of samples which describes the stoichiometry behind the Redfield ratio. Based on Gruber (2008) we thus selected regions of the Atlantic ocean with positive N* value (Caribbean, West coast of the Iberian Peninsula, Brazilian coast, Bay of Biscay France, coast of Island, coast of Virginia U.S., North Sea U.K) as a criterion for N fixation and searched the literature for species of similar taxa to those collected at the northeastern subtropical Pacific to use in a comparison of δ15N transfer in N-fixing and N-removing environments. The intense denitrification around the studied area is evidenced by N* value of -4 (at 300 m) (Gruber, 2008). On the other hand, values of N* from Alaska and the Atlantic Ocean (-1 to 4 respectively, Table 1), were large cyanobacteria blooms constantly occur (e.g. Zehr & Ward, 2002) reveal N fixation (Carpenter & Capone, 2008) RESULTS Oxygen profiles The oxygen profiles constructed for the studied area show a fast reduction in O2-concentration in the first two hundred meters at all stations (Fig. 3). Hypoxic conditions ([O2] < 2.1 ml/l) starts between 50-150 m for all stations. N stable isotopes -

The analysis of δ15N-NO3 ranged from 6‰ to 7.6‰ at 50 m and from11‰ to 13.4‰ at 300 m. The sediment values ranged from 6.3‰ to 9.3‰. The phytoplankton values ranged from

8‰ to 9‰ and zooplankton values from 12.9‰ to 13.9‰. The cephalopod values ranged from 15.1‰ to 17.7‰, red crab values from 12.6‰ to 16.6‰, demersal fish from 13.8‰ to 18‰, dolphins from to 16.8‰ to 17.8‰ and sea lion values from 18.4‰ to 20.7‰. Literature data comparison Nitrogen stable isotope data (δ15N) from taxa similar to those found in front of Bahía Magdalena were obtained from ten different studies from regions in the Atlantic Ocean with positive N* values, with the exception of Hobson et al. (2002) which is from Alaska and has a negative N* (Table 1). Aguilar et al. (2008) used stable isotopes in marine fish from the Atlantic Ocean and Caribbean to compare different levels of human impacts. The study of Bode et al. (2007) was conducted on the Iberian Atlantic shelf and described the temporal variations of the pelagic food web using stable isotopes. Corbisier et al. (2006) used stable isotopes to determine food sources and reconstruct the food web in a coastal area in Brazil. Hobson et al. (2002) used stable isotopes to model the Arctic food web from particulate organic matter (POM) to top predators. Le Loc’h et al. (2008) described the benthic food web using stable isotopes from the continental shelf in the north eastern Atlantic. Although the article of Logan and Lutcavage (2008) was not focused on ecological descriptions, important values from fish species were found for this comparison. Petursdottir et al. (2008) described trophic routes from benthic and pelagic crustaceans to mesopelagic fish species using stable isotopes and fatty acids. Stowasser et al. (2009) analyzed stable isotopes and fatty acids from deep sea fishes collected in the North Atlantic. Sigmanet al. (1997) described the method for δ15NO3 analysis using samples from the Sargasso Sea, a region of the ocean commonly known for intense N2 fixation. The mean and standard deviations of each component are summarized in Table 1. DISCUSSION In the present study our purpose was to highlight the utility of δ15N as a tracer of N removal processes along the food web in front of Bahía Magdalena. Therefore the results presented are averaged values of four season samplings. Details regarding seasonal changes and specific species can be found in Camalich (2011). The data comparison of analogous biotic components from the studied region and the Atlantic Ocean shows the transfer of dissolved nitrogen, and its progressive- enrichment, along the food web. The δ15N-NO3 found in this study were higher compared to those reported as av-

EFFECT OF NITROGEN REMOVAL PROCESSES ON δ15N

Table 1. Average values and standard deviations of δ15N from different components in areas where nitrogen fixation is the dominating process. N* Gruber 2008 3

d15N (‰) Mean ± S.D. 5

3-4

5.6 ± 1.7

Crustaceans*

10 ± 0.5

Cephalopods*

2-3

11 ± 1.3

Compartment NO3

POM

Demersal species*

1-2

12.5 ± 0.1

Delphinus delphis Pusa hispida

3 -1

13.1 17.5

Citation Sigman et al., 1997 Bode et al., 2007; Corbisier et al., 2006 Corbisier et al., 2006; Petursdottir et al., 2008 Bode et al., 2007; Corbisier et al., 2006 Aguilar et al., 2008; Bode et al., 2007; Corbisier et al., 2006; Le Loc’h et al., 2008; Logan & Lutcavage, 2008; Logan & Lutcavage, 2010; Petursdottir et al., 2008; Stowasser et al., 2009 Bode et al., 2007 Hobson et al., 2002

*A detailed description of the species and values used for this comparison can be found in Camalich (2011).

erage for open oceans were N fixation is the dominant process (Table 1), and are consistent with the range of values reported by Liu and Kaplan (1989), Brandes et al. (1998) and Voss et al. (Voss et al., 2001) from the Eastern tropical north Pacific OMZ (8‰ to 16‰). In addition we found that the δ15N of the sedimentary organic matter in the study area were higher compared to areas in the Atlantic Ocean. The sediment underlying oxygen minimum zones are a good register of the δ15N sinking particles since the low oxygen enhance the preservation of surface organic matter (Altabet et al., 1999). Although the O2-concentration in the water column in the area is potentially not low enough (~2 ml/l) for denitrification, the record of 15Nenriched particles in the sediments appear to confirm the presence of nitrogen removal processes in the overlying water column. Both phytoplankton and zooplankton in the study area were enriched in 15N compared to the Atlantic regions (Fig. 4). Zooplankton δ15N in the Bahía Magdalena oceanic region fit into the values measured at the southern end of the Baja California peninsula reported by LopezIbarra (2008) and Olson et al. (2010). In addition, the giant squid and the red crab had higher values compared to the Atlantic cephalopods and crustaceans (Fig. 4). Following the same trend, marine mammals (dolphins and sea lions) off Bahía Magdalena were enriched in 15N even though they maintained similar diets as those found for the Atlantic (Table 1). Both the jumbo squid and the red crab were sampled at depths from 50 to 400m. Gilly (2006) showed that jumbo squid migrate vertically in the Gulf of

California and the north eastern Pacific, probably hunting one of its preferred prey species, Pleuroncodes planipes. . In the case of higher trophic levels the average δ15N values showed a 15N enrichment compared to those reported in the literature living on the Atlantic (Table 1). Some demersal fishes and marine mammals of the region have been suggested as a good monitor of biogeochemical processes since they observed a strong spatial and temporal fidelity (Camalich, 2011). In the study of Ménard et al. (2007) conducted at the Arabian Sea, migratory tuna (Thunnus albacares) and sword fish (Xiphias gladius) recorded a change in the δ15N signal corresponding to a change in N dynamics. As they found the highest δ15N values in fishes in areas with high N removal rates, their results suggest that top predators can be used as monitors of water column denitrification. Our finding of a cascading effect in the δ15N-signal from the base of the food web to top predators in the area supports that conclusion. However, it is not clear if the enhanced signal is caused by denitrification as the O2-concentration in the more shallow parts of the study area is too high (~2 ml/l) to cause extensive denitrification (Gruber, 2008; Knowles, 1982). It is possible that the high δ15N signal has been transferred into the area from deeper waters or carried northward from the more O2-depleted regions such as the Mazatlán area (Brandes et al., 1998) or the Gulf of Tehuantepec (Kienast et al., 2002). Another possible explanation is that the high δ15N is due to anammox in the water column. Anammox is triggered at O2-concentration of ~ 2 ml/l as in the

CAMALICH et al.

Figure 3. Oxygen concentration (ml/l) profiles at the oceanic region in front of BahĂa Magdalena (data from WOA09).

Figure 4. Comparison of d15N from abiotic (nitrate and sediments) and biological samples from the northern ETP (Camalich, 2011) compared to the Atlantic Ocean (Bode et al., 2007; Corbisier et al., 2006; Gruber & Sarmiento, 1997; Hobson et al., 2002; Knapp et al., 2008; Le Locâ&#x20AC;&#x2122;h et al., 2008; Stowasser et al., 2009).

EFFECT OF NITROGEN REMOVAL PROCESSES ON δ15N

shallower parts of the study area and in recent years it has become clear that in addition to denitrification, anammox may be an important nitrogen removal process (Kuypers et al., 2003; Lam et al., 2009). Just as for denitrification the signal of this process could thus be printed on the water column nitrates and transferred to the base of the food web (Holtappels et al., 2010; Song & Tobias, 2011). Elucidating the contribution of denitrification and anammox to the enrichment of 15N in low oxygen areas and determining the potential transfer of the δ15N signal from anammox processes throughout the food web is important in future studies. ACKNOWLEDGEMENTS This study was supported by the grants SEP-CONACYT (project C01-46806, 20052008), SAGARPA-CONACYT (project 200302-019) and project EP2 of CIBNOR. We are grateful to the crew of the R/V BIP XII and Arturo Tecuapetla for their assistance during the field work. The first author is grateful to CONACyT and COFAA for the scholarships provided during his doctoral work. Thanks to Elisabeth Svensson for her help in improving the final manuscript. REFERENCES Aguilar, C., G. González-Sansón, I. Faloh & R.A. Curry. 2008. Spatial variation in stable isotopes (d13C and d15N) in marine fish along the coast of Havana City: Evidence of human impacts from harbor and river waters. J. Coast. Res., 24(5): 1281-1288. Altabet, M.A., C. Pilskaln, R. Thunell, C. Pride, D. Sigman, F. Chavez, & R. Francois. 1999. The nitrogen isotope biogeochemistry of sinking particles from the margin of the Eastern North Pacific. Deep Sea Res. Part I, 46(4): 655-679. Bode, A., M.T. Alvarez-Ossorio, M.E. Cunha, S. Garrido, J.B. Peleteiro, C. Porteiro, L. Valdés & M. Varela. 2007. Stable nitrogen isotope studies of the pelagic food web on the Atlantic shelf of the Iberian Peninsula. Prog. Oceanogr., 74(2-3): 115-131. Brandes, J.A., A.H. Devol, T. Yoshinari, D.A. Jayakumar & S.W.A. Naqvi. 1998. Isotopic composition of nitrate in the central Arabian Sea and eastern tropical North Pacific: A tracer for mixing and nitrogen cycles. Lim� nol. Oceanogr., 43(7): 1680-1689. Camalich, J. 2011. The register of oceano� graphic variability on demersal fishes and top predators at the oceanic front off Bahia Magdalena México, PhD. Thesis. Centro

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EFFECT OF NITROGEN REMOVAL PROCESSES ON δ15N

Schlitzer, R. 2011. Ocean Data View, http://odv. awi.de. Sigman, D.M., M.A. Altabet, R. Michener, D.C. McCorkle, B. Fry & R.M. Holmes. 1997. Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar. Chem., 57(3-4): 227-242. Song, B. & C.R. Tobias. 2011. Molecular and stable isotope methods to detect and measure anaerobic ammonium oxidation (anammox) in aquatic ecosystems. Meth� ods Enzymol., 496: 63-89. Stowasser, G., R. McAllen, G.J. Pierce, M.A. Collins, C.F. Moffat, I.G. Priede & D.W. Pond. 2009. Trophic position of deep-sea fish-Assessment through fatty acid and stable isotope analyses. Deep Sea Res. Part I. 56, 812-826.

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CICIMAR Oceánides 27(2): 37-49 (2012)

PROLIFERATION OF Amphidinium carterae (GYMNODINIALES: GYMNODINIACEAE) IN BAHÍA DE LA PAZ, GULF OF CALIFORNIA Gárate-Lizárraga, I. Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Departamento de Plancton y Ecología Marina, Apartado postal 592, La Paz, Baja California Sur 23096, México. Email: igarate@ipn.mx ABSTRACT. During a sampling on 15 December 2011 in Bahía de La Paz, a bloom of the benthic dinoflagellate Amphidinium carterae was detected. Its abundance ranged from 28.2 to 64.8 × 103 cells L–1. Cells of A. carterae varied in length from 18 to 28 µm and 13 to 18 µm in wide (n = 30). The presence of A. carterae and benthic species of diatoms and dinoflagellates at the surface could be an indicator of upwelling water generated by northwestern winds. Seawater temperature during the bloom was 20 °C. Also, new records of dinoflagellates for the Mexican coast of the Pacific are here reported: Amphidiniopsis hirsuta, Amphidiniopsis sp., Amylax buxus, Cochlodinium pulchellum, Cochlodinium virescens, Durinskia cf. baltica, Gyrodinium sp., Thecadinium sp., and Prorocentrum minimum var. triangulatum.

Keywords: Proliferation, Amphidinium carterae, benthic dinoflagellates, Gulf of California Proliferación de Amphidinium carterae (Dinophyceae: Gymnodiniales) en Bahía de La Paz, Golfo de California RESUMEN. Durante un muestreo realizado el 15 de Diciembre de 2011 en Bahía de La Paz se detectó un florecimiento del dinoflagelado bentónico Amphidinium carterae. Los valores de abundancia variaron de 28.2 a 64.8 × 103 céls L–1. Los especímenes de A. carterae presentaron un intervalo de tallas de 18 a 28 µm de longitud y de 13 a 18 µm de ancho (n = 30). La presencia de A. carterae, así como de especies bentónicas de diatomeas y dinflagelados en superficie podrían indicar aguas de surgencia debido a la influencia de los vientos del noroeste en esta temporada. La temperatura del agua durante el florecimiento fue de 20 °C. También se reportan nuevos registros de dinoflagelados para la costa pacífica de México: Amphidiniopsis hirsuta, Amphidiniopsis sp., Amylax buxus, Cochlodinium pulchellum, Cochlodinium virescens, Durinskia cf. baltica, Gyrodinium sp., Thecadinium sp. y Prorocentrum minimum var. triangulatum.

Palabras claves: Proliferación, Amphidinium carterae, dinoflagelados bentónicos, Golfo de California. Gárate-Lizárraga, I. 2012. Proliferation of Amphidinium carterae (Gymnodiniales: Gymnodiniaceae) in Bahía de La Paz, Gulf of California. CICIMAR Oceánides, 27(2): 37-49.

INTRODUCTION Microalgae blooms are frequent and periodic throughout the year in Bahía de La Paz, at the southwestern part of the Gulf of California. Harmful blooms cause negative impacts to marine fauna through poisoning, mechanical damage, or other media (Gárate-Lizárraga et al., 2001). Naked dinoflagellates that form red tides have only recently received attention (Gárate-Lizárraga et al., 2004; 2006, 2009a; 2011). Many of these have been underestimated because they are normally deformed or destroyed by sampling nets, storage, and by traditional preservation solutions used in routine phytoplankton sampling (Okolodkov & GárateLizárraga, 2006; Gárate-Lizárraga et al., 2011). Gymnodiniales are unarmored dinoflagellates that lack cellulose plates, but have a membranous outer covering of small vesicles. Most of the studies of gymnodinioid dinoflagellates focus on the species responsible for harmful algal blooms, which are abundant in coastal waters (Gárate-Lizárraga et al., 2001; 2009a; 2011). The genus Amphidinium Claparède and Lachmann emend. Flø Jørgensen, Murray & Fecha de recepción: 7 de febrero de 2012

Daugbjerg belongs to the order Gymnodiniales Lemmermann, 1910, although the placement of Amphidinium in the Gymnodiniales was not supported by the molecular analyses done by Flø Jørgensen et al. (2004). Amphidinium definition was emended by Flø Jørgensen et al. (2004) as follows: Athecate benthic or endosymbiotic dinoflagellates with minute irregular triangular- or crescent- shaped epicones. Epicone overlays anterior ventral part of hypocone. Epicone deflected to the left. Cells are dorsoventrally flattened, with or without chloroplasts. Members of Amphidinium are among the most abundant and diverse benthic dinoflagellates worldwide (Fukuyo, 1981; Dodge, 1982; Sampayo, 1985; Ismael et al., 1999; Hoppenrath, 2000; Okolodkov et al., 2007; Steidinger et al., 2009; Hallegraeff et al., 2010). Twelve species of Amphidinium have been found in Pacific coastal waters of Mexico (Okolodkov & Gárate-Lizárraga, 2006; Gárate-Lizárraga et al., 2007). According to Murray et al. (2004), there are several distinct genotypes. This report describes the first proliferation of Amphidinium carterae Claparède and Lachmann, 1859 in the southwestern Gulf of California. The stages of sexual fusion are also reported, and the microFecha de aceptación: 13 de agosto de 2012

GÁRATE-LIZÁRRAGA

algae community present during this bloom is also described.

24.4

MATERIAL AND METHODS Bahía de La Paz is the largest bay on the peninsular side of the Gulf of California. It has constant exchange of water with the Gulf of California via a northern and a southern broad channel (Gómez-Valdés et al., 2003). The main northern channel is wide and deep (up to 300 m), while the southern mouth is shallow and associated with a shallow basin about 10 m deep. There is a shallow lagoon, the Ensenada de La Paz, connected to the bay by a narrow inlet (1.2 km wide and 4 km long) with an average depth of 7 m. The sampling station (24.23°N; 110.34°W; 25 m depth) is located in the shallow basin of the southernmost region of Bahía de La Paz. Phytoplankton bottle samples were collected at sampling station 1 (off PEMEX) in Bahía de La Paz (Fig. 1) December 15, 2011.Samples were fixed with Lugol´s solution. Identification and cell counts were made in 5 ml settling chambers under an inverted Carl Zeiss phasecontrast microscope (Germany). Surface and vertical tows from 15 m were made with a 20 μm phytoplankton net mesh. A portion of each tow was immediately fixed with acid Lugol´s solution and later preserved in 4% formalin. These samples were used to properly identify some uncommon species found in the bottle samples. Sea surface temperature was measured with a bucket thermometer (Kahlsico International Corp., El Cajon, CA, USA). Scientific names of microalgae species were updated using the algae data base (http://www.algaebase.org/) (Guiry & Guiry, 2012). An Olympus CH2 compound microscope (Japan) was used to measure cells, and a digital Konus camera and a SONY Cyber shot camera (8.1MP) were used to record the phytoplankton images. RESULTS AND DISCUSSION A total of 107 microalgae taxa were identified: 56 were diatoms, 46 dinoflagellates, 2 silicoflagellates, 1 raphydophyte, 1 cyanobacteria and 1 coccolithophorid. This survey revealed the presence of benthic diatoms and dinoflagellates, as well as dinoflagellate cysts in the surface water samples, which is an indicator of upwelled water generated by northwest winds (Gárate-Lizárraga & Muñetón, 2008; GárateLizárraga et al., 2009a). The species list and abundance are summarized in Table 1. Microphytoplankton was numerically more important than nano-phytoplankton, and diatoms were the most important group followed by dinoflagellates; in this last group Amphidinium cart�

24.3

24.2

110.7

110.6

110.5

110.4

110.3

Figure 1. Sampling station (●) in the Bahía de La Paz, Gulf of California.

erae was the most abundant. The abundance of A. carterae in three samples was 28.2, 42.0, and 64.8 × 103 cells L–1. These are the highest quantitative data of A. carterae recorded for the Gulf of California, with a seawater temperature of 20 oC. Although this is the first recorded bloom of A. carterae in the Gulf of California, it was registered in Bahía de La Paz by Núñez-Vázquez (2005) and Okolodkov & Gárate-Lizárraga (2006). Only a few specimens were found in February 12, March 24, April 28 and May 24 of 2011, in the net phytoplankton samples (unpublished data). Cells of A. carterae were oval from the ventral side and flattened dorsoventrally, as shown in Figs. 2–5. Cells range from 18 to 28 µm in length and 13 to 18 µm in wide (n = 30). The epitheca is asymmetric and directed to the left (Fig. 2). Girdle is v-shaped ventrally and runs higher on the dorsal side of the cell. The cell contains one large, multilobed chloroplast (Fig. 3) with a central pyrenoid structure (Fig. 4). The chloroplast is located at the cell periphery and can be obscured by other organelles. The nucleus is large and ovoid and located in the posterior part of the cell. When live phytoplankton samples were examined vegetative cells or gametes of A. carterae were swimming close to each other, simulating recognition (Fig. 4). Gametes of A. carterae were described to have the same size and shape as vegetative cells (Cao Vien, 1967). This occurred about one hour after the samples were collected and, about a half hour later, specimens of A. carterae were surrounded by a mucilaginous membrane. Inside this membrane the cells swam close to each other (Figs. 5, 6) until they fused (Figs. 6, 8). In most of these cases four cells of A. carterae were aggregated (Figs. 7, 8), while in a few cases, 12 cells were aggregated (Fig. 9). Inside another mucilaginous membrane, four cells were joined (Fig. 10).

PROLIFERATION OF Amphidinium carterae

The term “pellicle” is more appropriately used to describe single-layered-wall stages (Bravo et al., 2010). Kofoid and Sweezy (1921) mentioned that encystment of Amphidinium members occurs within a thin-walled membrane and that binary fission takes place within a cyst or in freely-swimming forms. Fusion of A. carterae cells have been observed as mentioned by Cao Vien (1967), at the same time, zygotes germination in culture was detected (Cao Vien, 1968). This author mentioned that

only the act of fusion between gametes reveals their role in sexual recombination. Barlow and Triemer (1988) observed formation of cysts as part of the life cycle in A. klebsii Carter, 1937. These cysts contain 2-8 cells and are sites of multiple vegetative divisions. An encysted stage has important implications for species ecology because they survive conditions that would destroy the motile stage, enabling the species to repeatedly occur in a local region year after year (Sampayo, 1985).

Figures 2–10. Two specimens of Amphidinium carterae; Ventral view; arrow indicates the epicone (2) and Dorsal view; arrows indicate the multilobed chloroplast (3). Two cells of Amphidinium carterae swimming near each other; arrows indicate the pyrenoid (4). Two cells of Amphidinium carterae inside a just made pellicle. (5). Two clearly joined (matched) cells (6). A sequence of four cells of Amphidinium carterae recognizing each other (7) and later they matched (8). Two pellicicles with 16 cells of Amphidinium carterae (9, 10).

GÁRATE-LIZÁRRAGA

Table 1. Abundance of microalgae species recorded in Bahía de La Paz, Gulf of California during the proliferation of Amphidinium carterae in December 2011. Microalgae species Sample A Sample B Sample C Diatoms cells L−1 cells L−1 cells L−1 Actinoptychus adriaticus Grunow, 1863 200 0 0 Asterionellopsis glacialis (Castracane) Round, 1990 3000 1400 600 Asteromphalus heptactis (Brébisson) Ralfs, 1861 0 400 400 Auliscus coelatus Bailey, 1854 0 200 0 Azpeitia nodulifer (Schmidt) Fryxell &Sims, 1986 200 0 0 Bacillaria paxillifera (O.F.Müller) T. Marsson, 1901 0 200 4200 Bellerochea malleus (Brightwell) Van Heurck, 1885 1600 1200 0 Biddulphia aurita (Lyngbye) Brébisson, 1838 200 0 0 Biddulphia bidulphiana (J.E.Smith) Boyer, 1900 0 1200 0 Biddulphia tuomeyii (Bailey) Roper, 1859 0 600 0 Cerataulina pelagica (Cleve) Hendey, 1937 0 200 200 Cerataulus californicus Schmidt,1888 200 0 0 Chaetoceros affinis H.S. Lauder, 1864 92800 101200 41600 Chaetoceros atlanticus P.T. Cleve, 1873 14600 14200 21400 Chaetoceros coarctatus H.S. Lauder, 1864 4000 1400 3000 Chaetoceros compressus H.S. Lauder,1864 10000 12200 6000 Chaetoceros curvisetus P.T. Cleve, 1889 36800 21400 42600 Chaetoceros didymus Ehrenberg, 1845 1400 0 800 Chaetoceros lorenzianus Grunow, 1863 0 1600 1800 Chaetoceros messanensis Castracane, 1875 400 600 800 Chaetoceros rostratus H.S. Lauder, 1864 4200 1200 600 Chaetoceros socialis H.S. Lauder, 1864 8200 15200 4400 Chaetoceros sp. 23200 18400 16600 Coscinodiscus asteromphalus Ehrenberg, 1844 200 0 200 Coscinodiscus radiatus Ehrenberg, 1839 0 400 200 Coscinodiscus sp. 200 0 0 Cylindrotheca closterium (Ehrenberg) Reimann & J.C. Lewin, 1964 200 400 1800 Detonula pumila (Castracane) Gran,1900 800 5200 400 Ditylum brightwellii (T.West) Grunow in Van Heurck, 1885 400 200 200 Eucampia cornuta (Cleve) Grunow in Van Heurck, 1883 0 200 200 Eucampia zodiacus Ehrenberg, 1840 400 800 200 Eupodiscus radiatus J.W.Bailey, 1851 200 200 0 Fallacia nummularia (Greville) D.G.Mann, 1990 0 400 0 Fragilariopsis doliolus (Wallich) Medlin & P.A.Sims, 1993 0 1200 800 Grammatophora marina (Lyngbye) Kützing, 1844 0 0 400 Guinardia flaccida (Castracane) H.Peragallo, 1892 0 1400 400 Guinardia striata (Stolterfoth) Hasle, 1997 400 1200 400 Helicotheca tamesis Ricard, 1987 0 400 0 Lauderia annulata Cleve, 1873 0 600 0 Lioloma pacifica (Cupp) Hasle, 1996 1600 2000 4200 Lithodesmium undulatum Ehrenberg 1839 0 400 1200 Paralia fenestrata Sawai and Nagumo, 2005 800 800 600 Pleurosigma sp. A 200 200 0 Pleurosigma sp. B 400 0 200 Proboscia alata (Brightwell) Sundström, 1986 200 0 400 Pseudosolenia calcar-avis (Schultze) B.G.Sundström, 1986 0 200 800 Pseudo-nitzschia spp. 3600 4200 5600 Rhizosolenia bergonii H.Peragallo, 1892 0 0 400 Rhizosolenia hyalina Ostenfeld, 1901 0 1600 0 Rhizosolenia imbricata Brightwell, 1858 400 200 200

PROLIFERATION OF Amphidinium carterae

Table 1. Continued Microalgae species Diatoms Rhizosolenia setigera, Brightwell 1858 Thalassionema nitzschioides (Grunow) Mereschkowsky, 1902 Thalassiosira eccentrica (Ehrenberg) Cleve, 1904 Thalassiosira rotula Meunier, 1910 Thalassiosira subtilis (Ostenfeld) Gran, 1900 Stephanopyxis palmeriana (Greville) Grunow, 1884 Total abundance of diatoms Dinoflagellates Actiniscus pentasterias (Ehrenberg) Ehrenberg, 1854 Alexandrium tamiyavanichii Balech, 1994 Amphidiniopsis hirsuta (Balech) J.D.Dodge, 1982 Amphidiniopsis sp. Amphidinium carterae Hulburt, 1957 Amphidinium sphenoides WüIff, 1916 Amylax buxus (Balech) J.D. Dodge, 1989 Cochlodinium pulchelum Lebour, 1917 Cochlodinium virescens Kofoid & Swezy, 1921 Cochlodinium sp. Coolia monotis Meunier, 1919 Dinophysis acuminata Claparède & Lachmann, 1859 Dinophysis caudata Saville-Kent, 1881 Dinophysis tripos Gourret, 1883 Dinophysis ovum Schütt, F.,1895 Dissodinium pseudolunula E.V. Swift ex Elbrächter & Drebes, 1978 Durinskia cf. baltica (Levander 1892) Carty et Cox, 1986 Gonyaulax digitale (Pouchet) Kofoid, 1911 Gymnodinium coeruleum Dogiel, 1906 Gymnodinium gracile, Bergh 1881 Gymnodinium instriatum Freudenthal & Lee, 1963 Gyrodinium sp. Katodinium glaucum (Lebour) Loeblich III, 1965 Neoceratium azoricum (Cleve) F.Gómez, D.Moreira & P.López-Garcia, 2010 Neoceratium dens (Ostenfeld & Schmidt) F.Gomez, D.Moreira & P.Lopez-Garcia, 2010 Neoceratium fusus (Ehrenberg) F.Gomez, D.Moreira & P.Lopez-Garcia, 2010 Neoceratium furca (Ehrenberg) F.Gomez, D.Moreira & P.López-García, 2010 Ornithocercus magnificus Stein, 1883 Phalacroma favus Kofoid & J.R.Michener, 1911 Prorocentrum compressum (J.W.Bailey) Abé ex Dodge, 1975 Prorocentrum emarginatum Fukuyo, 1981 Prorocentrum gracile Schütt, 1895 Prorocentrum micans Ehrenberg, 1833 Prorocentrum minimum var. triangulatum (Martin) Hulburt, 1965 Prorocentrum rhathymum Loeblich, Sherley & Schmidt,1979 Protoperidinium abei (Paulsen) Balech, 1974 Protoperidinium compressum (Abé) Balech, 1974 Protoperidinium excentricum (Paulsen, 1907) Balech, 1974 Protoperidinium oblongum (Aurivillius) Parke & Dodge, 1976 Protoperidinium pentagonum (Gran) Balech, 1974 Protoperidinium subinerme (Paulsen) Loeblich III, 1969 Ptychodiscus noctiluca Stein, 1883

Sample A cells L−1 0 0 800 1200 1600 0 214600

Sample B cells L−1 0 3000 1800 800 1200 1200 223000

Sample C cells L−1 400 1200 200 800 1400 1600 169400

200 800 0 0 28200 0 800 400 0 0 400 0 200 0 0 200 * 0 200 0 0 0 200 200 0 0 200 200 0 800 400 200 200 0 400 200 1600 400 200 0 200 200

0 200 200 200 42000 200 0 0 0 0 200 1200 400 0 400 0 * 1200 0 200 200 0 400 0 400 400 0 0 0 0 400 400 200 400 200 200 400 0 200 200 0 0

200 400 0 0 64800 0 200 200 200 200 0 400 200 200 200 200 * 1400 0 400 200 400 1600 200 200 0 200 200 400 1200 200 200 600 0 0 0 200 200 0 200 200 200

GÁRATE-LIZÁRRAGA

Table 1. Continued Microalgae species Dinoflagellates cells L−1 cells L−1 cells L−1 Pyrocystis fusiformis var. fusiformis (Wyville-Thomson ex Haeckel) V. H. Blackmann, 0 200 200 1902 Pyrocystis noctiluca Murray ex Haeckel, 1890 Pyrocystis robusta Kofoid, 1907 Thecadinium sp. Total abundance of dinoflagellates Silicoflagellates Octactis octonaria (Ehrenberg) Hovasse, 1946 Dictyocha fibula var. robusta Schrader &Murray, 1985 Rhaphydophytes Chattonella marina var. ovata (Y. Hara & Chihara) Demura & Kawachi, 2009 Cyanobacteria Trichodesmium erythraeum Ehrenberg ex Gomont, 1892 Total abundance of the other groups Micro-phytoplankton Nano-phytoplankton Total phytoplankton abundance

At least 48 species of dinoflagellates form thin-walled cysts as part of their life cycle, associated with very different conditions, both in culture and nature (Bravo et al., 2010). Pellicle cysts of Cochlodinium pulchellum Lebour, 1917 (Fig. 60), Cochlodinium virescens Kofoid & Swezy, 1921 (Fig. 61), Cochlodinium convo� lutum Kofoid & Swezy, 1921 (Fig. 64), Gyrodin� ium instriatum Freudenthal & Lee, 1963 (Fig. 65), Prorocentrum compressum (J.W.Bailey) Abé ex Dodge, 1975 (Fig. 54), and P. rhathy� mum Loeblich, Sherley & Schmidt, 1979 (not shown) were observed in our study. Other species reported to produce pellicle cysts in Bahía de La Paz are Gymnodinium falcatum Kofoid & Swezy, 1921, C. helicoides Lebour, 1925, C. helix Schütt 1895, and C. polykrikoi� des Margalef, 1961 (Gárate-Lizárraga et al., 2004; 2009a, 2011); even these encysted species can have movement. Further studies are needed to characterize the life history of Am� phidinium members. In the Sado estuary of Portugal, A. carterae blooms seasonally in fish ponds, causing fish die-offs (Sampayo, 1985). Mortality is most prevalent among caged fish which are unable to avoid algal blooms (Gárate-Lizárraga et al., 2004). Intertidal pools in the North Arabian Sea along the coast of Pakistan have blooms with concentrations of 12 × 103 cells mL−1 (Baig et al., 2006). In our study, densities were higher than in intertidal pools, however, no fish die-offs were observed. Although A. carterae is considered a benthic or epiphytic species, it makes daily upward migrations in the water column from the benthos (Kamykowski & Zentara,

400 0 200 37600

200 0 0 50800

0 200 0 76200

400 0

200 0

200 400

200

8200 8600 260800 312400 573200

4200 4400 278200 211200 489400

16800 17600 263200 245800 509000

1977) and this favors formation of blooms. The occurrence of outbreaks of A. carterae in shrimp ponds in Bahía de La Paz could pose a risk to aquaculture activities because proliferations of microalgae are common in shrimp ponds (Gárate-Lizárraga et al., 2009b). Amphidinium carterae has been recognized as a producer of powerful ichthyotoxins and hemolytic substances (Yasumoto et al., 1987; Tindall & Morton, 1998; Echigoya et al., 2005; Rhodes et al., 2010). It has a variety of deleterious effects on adults and larvae of several invertebrates and is implicated as a causative agent in human ciguatera (Baig et al., 2006). Both wild and cultured A. carterae cells were tested for ciguatera toxicity by exposure to brine shrimp nauplii and albino mice. Pharmacological effects on mice include muscle contraction in lower back area, increased respiration, immobility, and paralysis in hind limbs for 2 h. These effects appeared to be reversible and gradually disappeared within 24h. In this survey, three species of microalgae producers of okadaic acid were observed (Di� nophysis acuminata, D. caudata, and D. tripos), one produces venerupin (hepatotoxin) (Proro� centrum minimum), one generates neurotoxins and hepatotoxins (Trichodesmium erythrae� um), and one produces haemolytic toxins (P. rhathymum). Although these species occurred in low densities during this bloom, they could be a health hazard if they proliferate. Monitoring of bloom forming, and toxin-producing microalgae species in Bahía de La Paz and other coasts of the Baja California Sur is an on-going activity.

PROLIFERATION OF Amphidinium carterae

13 14

Figures 11â&#x20AC;&#x201C;26. Chaetoceros affinis (11), Chaetoceros compressus (12), Chaetoceros coarctatus (with Vorticella oceanica) (13), Chaetoceros coarctatus (with a microalgae attached; inset is the free-microalgae) (14), Chaetoceros socialis (15), Chaetoceros didymus (16), Chaetoceros curvisetus (17), Chaetoceros rostratus (18), Proboscia indica (19), Pseudosolenia calcar-avis (20), Rhizosolenia hyalina (21), Rhizosolenia imbricata (22), Guinardia striata (23), Guinardia flaccida (24), Helicotheca tamesis (25), and Thalassiosira sp. with Reticulofenestra sessilis attached to the frustule (26).

GÁRATE-LIZÁRRAGA

Figures 27–42. Thalassiosira subtilis (27), Thalassiosira rotula (28), Eucampia zodiacus (29), Eucampia cornuta (30), Asterionellopsis glacialis (31), Detonula pumila (32), Lioloma pacifica (33), Ditylum brightwelli (34), Stephanopyxis palmeriana (35), Lithodesmium undulatum (36), Fragilariopsis doliolus (37), Thalassionema nitzschioides (38) Biddulphia tuomeyii (39), Biddulphia biddulphiana (40), Bacillaria paxillifera (41), and Paralia fenestrata. (42).

PROLIFERATION OF Amphidinium carterae

Figures 43â&#x20AC;&#x201C;58. Cerataulus californicus (43), Fallacia nummularia (44), Actinoptychus adriaticus (45), Asteromphalus heptactis (46), Eupodiscus radiatus (47), Odontella aurita (48), Chattonella marina var. ovata (49) Protoperidinium abei (50), Protoperidinium excentricus (51), Protoperidinium compressum (52), Prorocentrum emarginatum (53), Four cells of Prorocentrum compressum inside a gelatinous membrane (Pellicicle) (54), Prorocentrum minimum var. triangulatum (55), Prorocentrum gracile (56), Prorocentrum micans (57), and Ptychodiscus noctiluca (58).

GÁRATE-LIZÁRRAGA

Figures 59–74. Cells of Cochlodinium pulchellum (59, 60), Pellicicle of Cochlodinium pulchellum showing the flagellum (60), Pellicicle of Cochlodinium virescens, (61), Cell Cochlodinium virescens fixed with Lugol (62), Cochlodinium convolutum (63), Cochlodinium convolutum pellicicle (64), Gyrodinium instriatum (65), Gyrodinium sp. (66), Gymnodinium gracile (67), Katodinium glaucum (68), Amphidinium sphenoides (69), Pyrocystis fusiformis var. fusiformis (70), Dissodinium pseudolunula; secondary cyst with 6 dinokont cells; arrow indicates the flagella (71), Pyrocystis robusta (72), Actiniscus pentasterias; Side view of the cell, arrow showing the two complete pentasters (73); cell showing one of the pentasters (74).

PROLIFERATION OF Amphidinium carterae

Figures 75â&#x20AC;&#x201C;90. Dinophysis ovum (75), Dinophysis acuminata (76), Dinophysis caudata (77), Dinophysis tripos (78), Phalacroma favus (79) Ornithocercus magnificus, arrow indicates the symbiotic cyanobacteria harbourd in the region of the cingular list (80), Amylax buxus (81, 82) Alexandrium tamiyanavichii (83), Gonyaulax digitale (84), Neoceratium dens (85), Amphidiniopsis hirsuta (86), Amphidiniopsis sp. (87), Thecadinium sp. (88), Coolia monotis (89), and Durinskia cf baltica, arrow indicates the bright red stigma in the sulcal area of the cell (90).

GÁRATE-LIZÁRRAGA

New records Several species of dinoflagellates shown in Figures 2-90, are new records for the Mexican Pacific coast: Prorocentrum minimum var. trian� gulatum (Martin) Hulburt, 1965 (Fig. 55), Cochlo� dinium pulchellum (Figs. 59–60), Cochlodinium virescens (Figs. 61–62), Gyrodinium sp. (Fig. 66), Amylax buxus (Balech) J.D. Dodge, 1989 (Figs. 81–82) Amphidiniopsis hirsuta (Balech) J.D.Dodge, 1982 (Fig. 86), for which the antapical row of spines was not visible under light microscopy, coinciding with those specimens collected from the French coasts (Gómez et al., 2011); Amphidiniopsis sp. (Fig. 87), Thec� adinium sp. (Fig. 88), and Durinskia cf. baltica (Levander) Carty & Cox, 1986 (Fig. 90). Some others species are new records for the Gulf of California; Ptychodiscus noctiluca Stein, 1883 (Fig. 58), Pyrocystis robusta Kofoid, 1907 (Fig. 72), Phalacroma favus Kofoid & J.R. Michener, 1911 (Fig. 79), and Coolia monotis Meunier, 1919 (Fig. 89). Two interesting findings were observed in this study: the symbiosis between the coccolithophorid Reticulofenestra sessilis (Lohmann 1912) Jordan & Young 1990 and the diatom Thalassiosira sp. (Fig. 26), as well as the presence of the diatom Paralia fenestrata (Fig. 42) in Bahía de La Paz. ACKNOWLEDGMENTS Research projects were funded by Instituto Politécnico Nacional (SIP-20110281, SIP20110590, and SIP-20121153). The author would like to thank the anonymous reviewers for their valuable comments and suggestions to improve the quality of the paper. I.G.L. is COFAA and EDI fellow. REFERENCES Baig, H.S., S.M. Saifullah & A. Dar. 2006. Occurrence and toxicity of Amphidinium cart� erae Hulburt in the North Arabian Sea. Harmful Algae, 5: 133–140. Barlow, S.B. & R.E. Triemer. 1988. Alternate life history stages in Amphidinium klebsii (Dinophyceae, Pyrrophyta). Phycologia, 27: 413–420. Bravo, I., R.I. Figueroa, E. Garcés & S.F.A. Massanet. 2010. The intricacies of dinoflagellate pellicle cysts: The example of Alexandrium minutum cysts from a bloomrecurrent area (Bay of Baiona, NW Spain). Deep Sea Research II, 57: 166–174. Cao Vien, M. 1967. Sur l’existence de phénomènes sexuels chez un Péridinien libre, l’Amphidinium carteri. C. R. Acad. Sci., Ser. D., 264: 1006-1008.

Cao Vien, M., 1968. Sur la germination du zygote et sur un mode particulier de multiplication végétative chez le péridinien libre, l’Amphidinium carteri. C. R. Acad. Sci., Ser. D., 267, 701–703. Dodge, J.D. 1982. Marine Dinoflagellates of the British Isles. Her Majesty’s Stationery Office, London, 303 p. Echigoya, R., L. Rhodes, Y. Oshima & M. Satake. 2005. The structures of five new antifungal and hemolytic amphidinol analogs from Amphidinium carterae collected in New Zealand. Harmful Algae, 4: 383–389. Flø Jørgensen, M., S. Murray & N. Daugbjerg. 2004. Amphidinium revisited. I. Redefinition of Amphidinium (Dinophyceae) based on cladistic and molecular phylogenetic analyses. J. Phycol., 40: 351–365. Fukuyo, Y. 1981. Taxonomical study on benthic dinoflagellates collected on coral reefs. Bull. Japan. Soc. Sci. Fish., 47: 967–78. Gárate-Lizárraga, I. & M.S. Muñetón-Gómez. 2008. Bloom of Peridinium quinquecorne Abé in Ensenada de La Paz, Gulf of California (July 2003). Acta Bot. Mex., 83: 33−47. Gárate-Lizárraga, I., M. L. Hernández-Orozco, C. Band-Schmidt & G. Serrano-Casillas. 2001. Red tides along the coasts of Baja California Sur, México (1984 to 2001). Oceánides, 16(2): 127–134. Gárate-Lizárraga, I., M.S. Muñetón-Gómez & V. Maldonado-López. 2006. Florecimiento del dinoflagelado Gonyaulax polygramma frente a la Isla Espíritu Santo, Golfo de California (Octubre-2004). Rev. Inv. Mar., 27(1): 31–39. Gárate-Lizárraga, I., C.J. Band-Schmidt, G. Verdugo-Díaz, M.S. Muñetón-Gómez & E.F. Félix-Pico. 2007. Dinoflagelados (Dinophyceae) del sistema lagunar MagdalenaAlmejas, 141−170. In: R. Funes-Rodríguez, J. Gómez-Gutiérrez & J.R. Palomares-García (Eds.). Estudios ecológicos en Bahía Magdalena. CICIMAR-IPN, La Paz, Baja California Sur, México. Gárate-Lizárraga, I., C.J. Band-Schmidt, F. Aguirre-Bahena & T. Grayeb-del Álamo. 2009a. A multi-species microalgae bloom in Bahía de La Paz, Gulf of California, Mexico (June 2008). CICIMAR Oceánides, 24: 1−15.

PROLIFERATION OF Amphidinium carterae

Gárate-Lizárraga, I., Band-Schmidt, C.J., López-Cortés, D.J. & M.S. Muñetón-Gómez. 2009b. Bloom of Scrippsiella trochoi� dea (Gonyaulacaceae) in a shrimp pond from the southwestern Gulf of California, Mexico. Mar. Pollut. Bull., 58: 145–149. Gárate-Lizárraga, I., F. García-Domínguez, B. Pérez-Cruz & J.A. Díaz-Ortiz. 2011. First record of Cochlodinium convolutum and C. helicoides (Dinophyceae: Gymnodiniaceae) in the Gulf of California. Rev. Biol. Mar. Oceanogr., 46: 495–498. Gómez, F., P. López-García & D. Moreira. 2011. Molecular phylogeny of the sand-dwelling dinoflagellates Amphidiniopsis hirsuta and A. swedmarkii (Peridiniales, Dinophyceae). Acta Protozool., 50: 255–262. Gómez-Valdés, J., J.A. Delgado & J.A. Dwora. 2003. Overtides, compound tides, and tidal-residual current in Ensenada de La Paz lagoon, Baja California Sur, Mexico. Geof. Inter., 42: 623–634. Guiry, M.D. & G.M. Guiry. 2012. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www. algaebase.org. Hallegraeff, G.M., C.J.S. Bolch, D.R.A. Hill, I. Jameson, J.M. LeRoi, A. McMinn, S. Murray, M.F. de Salas & K. Saunders. 2010. Algae of Australia: Phytoplankton of tem� perate coastal waters. CSIRO Publishing, Australia, 421 p. Hoppenrath, M. 2000. Taxonomische und o¨kologische Untersuchungen von Flagel� laten mariner Sande. Doctoral Thesis, Biologische Fakultät, Universität Hamburg, Germany, 311 p. Ismael, A.A., H., Y. Halim & A.G., Khalil. 1999. Optimum growth conditions for Amphidini� um carterae Hulburt from eutrophic waters in Alexandria (Egypt) and its toxicity to the brine shrimp Artemia salina. Grana, 38: 179–185. Kamykowski, D. & S.J. Zentara. 1977. The diurnal vertical migration of motile phytoplankton through temperature gradients. Limnol. Oceanogr., 22: 148–151. Kofoid, C.A. & O. Swezy. 1921. The free-living unarmored Dinoflagellata. Mem. Univ. Ca� lif., University of California Press, Berkeley. V. 5, 562 p. + 12 pl.

Murray, S., M., Flo-Joergensen, N. Daugbjerg & L. Rhodes. 2004. Amphidinium revisited. II. Resolving species boundaries in the Am� phidinium operculatum species complex (Dinophyceae), including the descriptions of Amphidinium trulla sp. nov. and Amphi� dinium gibbosum comb. nov. J. Phycol., 40: 366–382. Núñez-Vázquez, E.J. 2005. Biotoxinas marinas en peces comestibles de Baja California Sur, México: origen, identificación y cuan� tificación. Bachelor’s thesis. Centro de Investigaciones Biológicas del Noroeste, La Paz, Baja California Sur. Okolodkov, Y.B. & I. Gárate-Lizárraga. 2006. An annotated checklist of dinoflagellates from the Mexican Pacific. Acta Bot. Mex., 74: 1–154. Okolodkov, Y.B., G. Campos-Bautista, I. GárateLizárraga, J.A.G. González-González, M. Hoppenrath & V. Arenas. 2007. Seasonal changes of benthic and epiphytic dinoflagellates in the Veracruz reef zone, Gulf of Mexico. Aq. Micr. Ecol., 47: 223–237. Rhodes L.L., K.F. Smith, R. Munday, A.I. Selwood, P.S. McNabb, P.T. Holland & M.Y. Bottein. 2010. Toxic dinoflagellates (Dinophyceae) from Rarotonga, Cook Islands. Toxicon, 56: 751–758. Sampayo, M.A. 1985. Encystment and excystment of a Portugese isolate of Amphidinium carterae in cultures, 125–130. In: Anderson, D.M., A.W. White, & D.G. Baden (Eds.). Toxic Dinoflagellates, Elsevier, Amsterdam. Steidinger, K.A., A.M. Faust & D.U. HernándezBecerril. 2009. Dinoflagellates (Dinoflagellata) of the Gulf of Mexico, 131-154. In: Tunnel, J. W. Jr., D. L. Felder & S.A. Earl (Eds.). Gulf of Mexico origin, waters, and biota. Vol.1, Biodiversity. 1st ed. Harte Research Institute for Gulf of Mexico Studies Series, Texas A & M University Press, Corpus Christi, TX. Tindall, D.R. & S.L. Morton. 1998. Community dynamics and physiology of epiphytic/benthic dinoflagellates associated with ciguatera, 293–313. In: Anderson, D.M., A.D. Cembella & G.M. Hallegraeff (Eds.). Physi� ological Ecology of Harmful Algal Blooms. Proceedings of the NATO-ASI, volume 41. Springer Verlag, Heidelberg. Yasumoto, T., N. Seino, Y. Murakami & M. Murata. 1987. Toxins produced by benthic dinoflagellates. Biol. Bull., 172: 128–131.

CICIMAR Oceánides 27(2): 51-58 (2012)

MARINE AND LAGOON RECRUITMENT OF Litopenaeus vannamei (BOONE, 1931) (DECAPODA: PENAEIDAE) IN THE “CABEZA DE TORO-LA JOYA BUENAVISTA” LAGOON SYSTEM, CHIAPAS, MEXICO Cervantes-Hernández, P.1, M. A. Gómez-Ponce 2 & P. Torres-Hernández1

Instituto de Recursos e Industrias, Universidad del Mar, Ciudad Universitaria s/n, Puerto Ángel, Oaxaca 70902, México. 2Unidad de Servicio “El Carmen”, Instituto de Ciencias del Mar y Limnología. Universidad Nacional Autónoma de México. Ciudad del Carmen, Campeche 24157, México. email: pch@angel.umar.mx 1

ABSTRACT. Life cycle of the Penaeidae shrimp family is approximately 16 months and this takes place between the marine and coastal lagoon environments. Within the “Cabeza de Toro-La Joya Buenavista” lagoon system (CJB-LS) a total length value for 6116 juvenile white shrimp was recorded. Bhattacharya’s method and modal progression analysis were used in order to analyze marine (MR) and lagoon (LR) recruitment periods. The MR is the natural movement of juvenile shrimp from the interior of CJB-LS towards the marine fishing zone (MFZ) from Gulf of Tehuantepec. The LR is the natural movement of shrimp post-larvae from the MFZ towards the interior of CJB-LS. Both recruitments were separated between September and October. The MR period was delimited from April 2001 to the middle of October 2001 (during rainy season). In this period, the age at which white shrimp began to migrate towards the MFZ was recorded between 4.5 and five months old. The LR period began during the last days of October 2001 and ended in March 2002 (during “Tehuanos” season). Only in this period were shrimp cohorts observed with an approximate age of 25 days. Those shrimp cohorts were considered as recently recruited, because they continued growing after their immigration from MFZ. Reproduction period of white shrimp occurs in the MFZ from July to November with maxima in October.

Key words: shrimp, recruitment age, coastal lagoons, Gulf of Tehuantepec. RECLUTAMIENTO MARINO Y LAGUNAR DE Litopenaeus vannamei (BOONE, 1931) (DECAPODA: PENAEIDAE) EN EL SISTEMA LAGUNAR “CABEZA DE TORO LA JOYA BUENAVISTA” CHIAPAS, MÉXICO. RESUMEN. El ciclo de vida de los camarones de la Familia Penaeidae es de aproximadamente 16 meses y se desarrolla entre los ambientes marino y lagunar. En el sistema lagunar “Cabeza de Toro-La Joya de Buenavista” (CJB-SL), fue registrado el valor de la longitud total de 6116 juveniles de camarón blanco. El método de Bhattacharya y el análisis de progresión modal fueron usados para analizar los periodos de reclutamiento marino (RM) y lagunar (RL). El RM, es el movimiento natural de camarones juveniles desde el interior del CJBSL hacia la zona marina de pesca (ZMP) del Golfo de Tehuantepec. El RL, es el movimiento natural de postlarvas de camarón desde la ZMP hacia el interior del CJB-SL. Ambos periodos de reclutamiento pudieron ser separados entre septiembre y octubre. El periodo del RM fue delimitado de abril 2001 hasta la mitad de octubre 2001 (durante la estación de lluvias). En este periodo, la edad a la cual los juveniles comenzaron a emigrar hacia la ZMP fue registrada entre 4.5 y cinco meses. El periodo del RL comenzó durante los últimos días de octubre 2001 y finalizó en marzo de 2002 (durante la estación de “Tehuanos”), sólo en este período fueron observadas cohortes de camarón con una edad aproximada de 25 días. Estas cohortes de camarón fueron consideraras como recién reclutadas porque éstas continuaron creciendo después de su inmigración desde la ZMP. El periodo de reproducción del camarón blanco ocurre en la ZMP de julio a noviembre con máximos en octubre.

Palabras clave: camarón, edad de reclutamiento, laguna costera, Golfo de Tehuantepec. Cervantes-Hernández, P., M. A. Gómez-Ponce & P. Torres-Hernández. 2012. Marine and lagoon recruitment of Litopenaeus vannamei (Boone, 1931) (Decapoda: Penaeidae) in the “Cabeza De Toro - La Joya Buenavista” lagoon system, Chiapas, Mexico. CICIMAR Oceánides, 27(2): 51-58.

INTRODUCTION

In the Gulf of Tehuantepec (GT) the white shrimp Litopenaeus vannamei (Boone, 1931) is captured in a marine area called fishing zone 90, which is located between Punta Chipehua near Salina Cruz, Oaxaca (16º01´31.39´´ N and 95º22´24.56´´ W) and Puerto Chiapas, Chiapas (14º40´55.81´´ N and 92º23´44.13´´ W) (Reyna-Cabrera & Ramos-Cruz, 1998) (CervantesHernández, 2008) (Fig. 1). The marine fishing zone 90 has a total area of 8085 km2 of continental platform and it is composed of five subsectors (Reyna-Cabrera & Ramos-Cruz, 1998). In the marine fishing zone 90, the ships operate from five to 40 fathoms (i.e., 9.1 to 72.8 m) Fecha de recepción: 7 de febrero de 2012

using trawl nets with a mesh opening of 57.15 mm (INP, 2004). Throughout the GT, six lagoon systems are located along its coastline, but the most important (due to its shrimp production) are lagoon systems “Huave” in Oaxaca and “Mar Muerto” shared by the states of Oaxaca and Chiapas (Cervantes-Hernández, 2008) (Fig. 1). The complete life cycle of the Penaeidae shrimp family is approximately between 15 and 18 months (Cervantes-Hernández, 2008). The life cycle begins in the marine environment with the reproduction process that generates larvae shrimp. After post-larvae shrimp enter lagoon systems for their protection, they feed and grow Fecha de aceptación: 13 de agosto de 2012

CERVANTES-HERNÁNDEZ et al.

Figure 1. Geographic location of marine fishing zone 90 in the Gulf of Tehuantepec; sub-sectors (from S-91 to S-95); lagoon systems are: (1) “Huave”; (2) “Mar Muerto”; (3) “Cabeza de Toro-La Joya-Buenavista”; (4) “PatosSolo Dios”; (5) “Carretas-Pereyra”; (6) “Chantuto-Panzacola”; (S.C.) Salina Cruz City.

until they reach the juvenile stage (Gracia et al., 1997). Ricker (1975) indicated that recruitment is a process whereby organisms become potentially vulnerable to fishing mainly due to body length changes. These changes are biologically important because they activate emigration and immigration movements between different aquatic environments.

increase, activating then lagoon recruitment period. The author associated massive reproduction periods with maximum abundance of shrimp spawners close to and at sexual maturity age (between six/seven and 16 months). These ages were recorded during 1989-11, 1990-12, 1991-10, 1992-08, 1993-12, 1994-10, 1996-10, 1996-01 and 1997-01.

Cervantes-Hernández (2008) analyzed marine shrimp catches obtained in the marine fishing zone 90 between 1989 and 1998. Based on this information a fishery model was made to estimate marine and lagoon recruitment periods of Farfantepenaeus californiensis (Holmes, 1900). In this work the author defined the Marine Recruitment as the natural movement of juvenile shrimp from the interior lagoon systems towards the marine fishing zone 90 (Fig. 1). The author denominated recruits juvenile shrimp that were recorded at four and five months old. These ages were recorded with maximum abundance during: 1989-08, 1990-08, 1991-07, 1992-05, 1993-08, 1994-07, 1995-04, 1996-07 and 1997-09. The Lagoon Recruitment was defined as the natural movement of larvae shrimp from the marine fishing zone 90 towards the interior lagoon systems (Fig. 1). Although this author did not directly record larvae shrimp, his fishery model showed that when massive reproduction periods of F. californiensis occur in the marine fishing zone 90, larvae shrimp must

The results obtained by Cervantes-Hernández (2008), were used by Cervantes-Hernández et al. (2008 a) to demonstrate, that the marine closure system implemented from 1993 in the GT (from March/April to September) (NOM, 1993; 2002) has not functioned adequately. The main problems that these authors detected in this marine closure system were excessive protection of the juvenile and prolonged exploitation period of spawners of F. californiensis and L. vannamei. Based on these results, the authors suggested that the old marine closure system should be changed from July to October to protect both recruitment periods. The results published by CervantesHernández et al. (2008 a) were not accepted by the fishery community in Oaxaca because the author did not include lagoon recruitment information in his fishery model. Nevertheless, this type of information had not been generated. For this reason, in this work marine and lagoon recruitment periods were analyzed in the

RECRUITMENT OF Litopenaeus vannamei

“Cabeza de Toro - La Joya-Buenavista” lagoon system (CJB-LS) from GT. The results obtained in this work were compared with the results reported by CervantesHernández (2008) to determine if both recruitment periods are consistent for L. californiensis and L. vannamei. Conclusions from this work will serve to support the proposal of changing the old marine closure system in the GT. Important fishery arguments were obtained through this work to understand how both recruitment periods develop between the CJB-LS and the marine fishing zone 90. MATERIALS AND METHODS Sampling Every fifteen days between 2001-04-24 and 2002-03-28 at ten stations distributed randomly within the CJB-LS (Fig. 2), juvenile of L. van� namei samples were collected during morning between 08:00:00 and 10:00:00 using artisanal ships and atarraya nets with mesh opening of 0.9 cm. This period was chosen in order to widely cover recruitment and reproduction periods. A digital electronic vernier calliper (± 0.1 mm) was used to measure shrimp total length (LT in mm) from the rostrum tip to the telson end. Juvenile of L. vannamei were identified, using the taxonomic keys of Hendrickx (1995). Fieldwork was done by technical personnel from the

“Centro Regional de Investigación Pesquera” (CRIP-SC) from Salina Cruz, Oaxaca, México. Information generated by CRIP-SC was analyzed at the Universidad del Mar, Puerto Ángel, Oaxaca, Mexico, under project 2IR1104. Cohort’s analysis Bhattacharya’s method described by Goonetilleke and Sivasubramaniam (1987) was used in order to identify and separate shrimp cohorts in each analyzed fortnight. In this graphical method, the natural logarithm of abundance (Nt) must be estimated and its difference between successive abundances ∆Ln (Nt) is plotted against LT values. In this plot a shrimp cohort can be identified as a ∆Ln (Nt) vs. LT values group linearly ordered and separated from other cohorts using a negative lineal model. This negative lineal model is:

∆Ln (Nt) = a - b ∙ LT

(1)

According to Malcolm (2001), the parameters a and b of the function (1) were estimated using the minimum likelihood of log-normal distribution (-Ln (a, b / Nt, LT)), this is: -Ln(a, b/Nt, LT)=sum(Ln(SDƐ)+(Ln(2π)/2)+(Ɛ2/(2∙ SDƐ)) (2)

Where: Ɛ is the error structure or residual value of ∆Ln (Nt), SDƐ is the standard deviation of Ɛ estimated with SDƐ = root ((1 / n) ∙ sum

Figure 2. Geographic location of sampling station (from 1 to 10) in the Cabeza de Toro-La Joya-Buenavista lagoon system.

CERVANTES-HERNÁNDEZ et al.

(Ɛ2)), n are total records of LT of each analyzed fortnight. When parameters a and b were estimated for each shrimp cohort, the mean length (LM) was calculated using:

LM = a/b

(3)

Bhattacharya’s method was performed using the computer software BOBP/MAG/4. The function (2) was resolved using computer software Analysis Matrix Population (Pop-Tools) and with support “Solver” an Excel tool. Solver was used with a precision at 0.000001 combined tangent, progressive and Newton algorithms. To develop minimum likelihood method it was necessary to define error structure and, in this work, the Ɛ had a log-normal distribution. Malcolm (2001) indicated that the distribution of catches is often log-normally distributed in fisheries models. Modal progression analysis and age estimation Shrimp cohorts and their LM values were ordered on an ascendant criterium fortnight by fortnight to build a new plot using time as Xaxis and LM as Y-axis. This plot was used to develop a modal progression analysis according to Sparre and Venema (1995). In this analysis type, a modal progression line must be diagonally drawn between a minimum value and a maximum value of LM. Once this is done, modal progression trajectory line can be diagonally followed to see how LM values increase between fortnights until they reach the maximum value of LM. To assign an approximate age to each LM value, the criterium reported by Chávez (1979) was used. This author obtained LM records for L. vannamei in “Huave” lagoon system (Fig. 1) and, based on these records, the author indicated that when these organisms have reached between 48 and 55 mm, they are juvenile shrimp with an approximate age of one month. Organisms with a LM value between 42 and 47 mm are recently recruited younger shrimp with an approximate age of 25 days. In this work all shrimp cohorts that began with a LM value between 48 and 55 mm were assigned with an age of one month. Then, following the modal progression trajectory line diagonally, fifteen more days were added to know the approximate age of the next shrimp cohort. This additive process continued fortnight by fortnight until reaching the maximum value of LM in each modal progression lines obtained. When the modal progression lines did

not begin with aforementioned LM values (less or greater), the additive process was the same. The approximate age of the next shrimp cohort was thus estimated using the minimum value of LM recorded in these modal progression lines. Recruitment analysis To analyze marine and lagoon recruitment periods in the CJB-LS, sampling times (between 2001-04-24 and 2002-03-28) were separated into two periods on the aforementioned plot. These periods were the same as those used by Cervantes-Hernández (2008) to describe marine and lagoon recruitment periods in the marine fishing zone 90. According to this author, the first period represented marine recruitment and was delimited from April to October (during rainy season). The second period represented lagoon recruitment and was delimited between the last days of October and June (during “Tehuanos” season). Two additional criteria were considered to explain how marine and lagoon recruitment could develop between the CJB-LS and the marine fishing zone 90. a) when a shrimp cohort reached the maximum LM value in a modal progression line, this line would continue growing within the CJB-LS, but the next shrimp cohort would not be able to be observed inside the lagoon system, because it migrated toward the marine fishing zone 90, then marine recruitment had begun; and b) when a shrimp cohort began to grow in a modal progression line and this shrimp cohort was recorded with a LM value between 42 y 47 mm, then the shrimp cohort was considered as recently recruited, because they continued growing after their immigration from the marine fishing zone 90 towards the interior CJB-LS. The presence of younger shrimp within the CJB-LS suggests that lagoon recruitment had begun. RESULTS Cohort’s analysis During sampling times 6116 readings of LT were done. Figure 3 shows each analyzed fortnight and the LM values estimated for each shrimp cohort. With 23 fortnights sampled, 200 shrimp cohorts were identified and separated (Fig. 3). A higher number of shrimp cohorts were observed during June, July and October fortnights. Fewer shrimp cohorts were recorded from January to March (Fig. 3). Modal progression analysis and age estimation Marine and lagoon recruitment could clearly be separated into two periods and the separa-

RECRUITMENT OF Litopenaeus vannamei

Figure 3. Modal progression analysis for L. vannamei in the CJB-LS between 2001-04-24 and 2002-03-28. Points are shrimp cohorts and lines that connect points are the modal progression lines.

tion point between these periods was observed between September and October (Fig. 3). The first period was delimited from April 2001 to mid October 2001 (during rainy season) and 21 modal progression lines were recorded (Fig. 3). The second period began during the last days of October 2001 and ended in March 2002 (during “Tehuanos” season) and 13 modal progression lines were recorded (Fig. 3). In the first period, the modal progression lines began to grow with LM values greater than 52 mm at an approximate age between one and 1.5 months old (Fig. 3). In these modal progression lines, shrimp cohorts reached the maximum LM values between 120 and 125 mm at an approximate age between 4.5 and 4.8 months old (Fig. 3). This means that a higher shrimp cohort number at an approximated age of five months old began to emigrate from the interior the CJB-LS towards the marine fishing zone 90 (Fig. 3). In this period, shrimp cohorts with LM values between 42 and 47 mm were not observed (Fig. 3). In the second period, the modal progression lines began to grow with LM values between 42 (with an approximate age of 25 days old) and 52 mm (with an approximate age of one month old) (Fig. 3). In these modal progression lines shrimp cohorts reached maximum LM values between 105 and 110 mm at an approximate age between 3.7 and four months old (Fig. 3). Fewer shrimp cohorts were observed beginning to emigrate from the interior the CJB-LS towards the marine fishing zone 90 (Fig. 3), but

a greater number of shrimp cohorts were observed beginning to immigrate from the marine fishing zone 90 towards the interior the CJB-LS (Fig. 3). Recruitment analysis The results obtained suggest that in the CJB-LS marine recruitment continues throughout collected time, but it was higher during the first period, especially in June and July 2001. Lagoon recruitment also continues throughout collected time, but it was higher during the second period, especially in the last days of October 2001(Fig. 3). The age at which L. vannamei began to emigrate towards the marine fishing zone 90 was recorded between 4.5 and five months old (Fig. 3). We named these ages “recruitment age”. DISCUSSION Knowledge of the annual abundance variation of recruits and spawners is critical to the management of all fisheries (Penn & Caputi, 1986). For an organism whose age cannot be accurately estimated (such as penaeid shrimp), the length-cohort models can identify recruitment and spawning periods in natural populations (Watson et al., 1996). The INP (2004) described the massive egglaying periods of mature female brown shrimp in phase IV in the GT between 1982 and 2002. Phase IV in the shrimp of the genus Penaeus is characterized by dark colored mature ovaries and an empty gonadal mass (Sandoval-Quin-

CERVANTES-HERNÁNDEZ et al.

tero & Gracia, 1998). The INP (2004) reported a higher percentage of mature female brown shrimp in phase IV from October to January. In these same months Cervantes-Hernández (2008) predicted lagoon recruitment period for F. californiensis and, during this period, the author reported an increase in the spawners number of this shrimp. In the CJB-LS, 25 day old white shrimp cohorts were observed only during October 2001. Those shrimp cohorts were considered as recently recruited, because they continued growing after their migration from the marine fishing zone 90. During “Tehuanos” seasons the presence of very young shrimp suggests a flow of postlarvae shrimp from the marine fishing zone 90 towards the interior of the CJB-LS. This flow of post-larvae shrimp can be explained by a reproduction period in open sea and, according to Cervantes-Hernández et al. (2008 b), this period was recorded from July to November with maxima in October. During this period, a greater post-larvae shrimp number can be observed in the marine fishing zone 90 because food is more readily available (phytoplankton and zooplankton), according to high levels of chlorophyll a detected in the GT and INP (2004), because mature female brown shrimp in phase IV are dominant. Cervantes-Hernández et al. (2008 b) described some oceanographic conditions of the GT between 1989 and 1998. On average, chlorophyll a concentration was lower during marine recruitment in the rainy season (0.13 mg m-3) and greater during lagoon recruitment in the “Tehuanos” season (0.42-1.10 mg m-3). These authors proposed that between October and January (when the maximum abundance of spawners and the higher percentage of egglaying of mature females in phase IV occurred), larval survival was greater because food was more available. On the other hand, from July to August/September (when the maximum abundance of recruits and the lower percentage of egg-laying of mature females in phase IV occurred), larval survival was lower because food availability diminished according to the low levels of chlorophyll a observed in the GT. On the other hand, the INP (2004) reported a smaller percentage of mature female brown shrimp in phase IV from July to September. In these same months Cervantes-Hernández (2008) predicted marine recruitment period for F. californiensis and, during this period, the author reported an increase in the juvenile number of this species. For L. vannamei from the CJB-LS, a higher number of white shrimp cohorts between 4.5 and five months of age were observed within the CJB-LS, especially during

June and July. This fact was interpreted as evidence that those shrimp cohorts began to migrate towards the marine fishing zone 90. During the rainy season along the coastline between the states of Oaxaca and Chiapas, higher levels of pluvial precipitation were recorded between June and September 2001 (337-397 mm). During the “Tehuanos” season lower levels of pluvial precipitation were recorded from October to April (20-30 mm) (SMN, 2008). Several authors have reported a direct relationship between shrimp abundance and pluvial precipitation (Ruello, 1973; García & Le Reste, 1986; Cervantes-Hernández, 1999). These authors indicated that pluvial precipitation together with fluvial unloading in lagoon systems stimulate the emigration of juvenile shrimp due to diminishing salinity (chemical stimulus). Another associated factor is an increase of the water turbidity which diminishes the natural mortality rate due to depredation when shrimp leave lagoon systems. Our results indicate that between the CJBLS and the marine fishing zone 90, marine recruitment period for L. vannamei was delimited from April 2001 to mid October 2001 and recruitment in lagoons began during the last days of October 2001 and ended in March 2002. These conclusions were consistent with marine and lagoon recruitment periods predicted for F. californiensis in the marine fishing zone 90 by Cervantes-Hernández (2008), who reported a recruitment age for F. californiensis of five months. In the CJB-LS the recruitment age for L. vannamei was estimated between 4.5 and five months. The results obtained in this work show that the fishery model development by CervantesHernández et al. (2008 a) generated correct conclusions to demonstrate that the old marine closure system in the GT has not functioned adequately. The main problems detected in this marine closure system were excessive protection of the juvenile and long exploitation period of spawners of F. californiensis and L. vannamei. For this reason, we suggest that the old marine closure system should be changed from July to October to protect both recruitment periods. For details on marine closures system changes, see Cervantes-Hernández et al. (2008 a). ACKNOWLEDGMENTS We thank the CRIP at Salina Cruz, Oaxaca, México for providing the data set used in this research, and the Universidad del Mar (UMAR) for providing economic resources. Thanks to Derek J. Brockett (UMAR), Isabel Gallardo

RECRUITMENT OF Litopenaeus vannamei

Berumen (UMAR), Saul J. Serrano Guzmán (UMAR) and anonymous reviewers for their valuable time and comments regarding this article. REFERENCES Cervantes-Hernández, P. 1999. Relaciones stock-reclutamiento del camarón rosado Farfantepenaeus duorarum (Burkenroad 1939) en el Banco de Campeche. MSc thesis, Universidad Nacional Autónoma de México, 37 p. Cervantes-Hernández, P. 2008. Method to obtain abundance indices in the population of Farfantepenaeus californiensis (Holmes, 1900) from the Gulf of Tehuantepec, Oaxaca, México. Rev. Biol. Mar. Oceanogr., 43(1): 111-119. Cervantes-Hernández, P., M. I. Gallardo-Berumen, S. Ramos-Cruz, M. A. Gómez-Ponce & A. Gracia. 2008 a. Análisis de las temporadas de veda en la explotación marina de camarones del Golfo de Tehuantepec, México. Rev. Biol. Mar. Oceanogr., 43(2): 285-294. Cervantes-Hernández, P., S. Ramos-Cruz, B. Sánchez-Meraz, S. J. Serrano-Guzmán & A. Gracia. 2008 b. Variación interanual de la abundancia de Farfantepenaeus californiensis (Holmes, 1900) en el Golfo de Tehuantepec. Hidrobiológica, 18(3): 215226. Chávez, E. A. 1979. Diagnosis de la pesquería del camarón del Golfo de Tehuantepec, Pacífico Sur Occidental de México. An. Centro de Cienc. Mar y Limnol. Univ. Nal. Autón. México, 6(2): 7-14.

Goonetilleke, H. & K. Sivasubramaniam. 1987. BOBP/MAG/4 a program to Separating mixtures of normal distributions: basic pro� grams for Bhattacharya’s method and their applications to fish population analysis (ver� sion 2.20B). Available at http://www.fao.org/ DOCREP/FIELD/006/AD475E/AD475E00. HTM [Accessed 15 June 2005]. Hendrickx, M. E. 1995. Camarones, 484-508. In: FAO (Ed). Guía FAO para la identifi� cación de especies para los fines de la pesca, Pacífico Centro-Oriental, plantas e invertebrados. Food and Agriculture Organization of the United Nations, Rome, 600 p. INP (Instituto Nacional de la Pesca). 2004. Inicio de la temporada de veda 2004 para la pesquería de camarón del Océano Pacífico mexicano. Informe Técnico. Avalable at http://www.inapesca.gob.mx/.../129-iniciode-la-temporada-de-veda-2004-para-la pesqueria-de camaron-del-oceano-pacifico-mexicano [accessed 30 October de 2010]. Malcolm, H. 2001. Modelling and quantitative methods in fisheries. Chapman and Hall, London, 406 p. NOM (Norma Oficial Mexicana). 1993. Available at http://dof.gob.mx/nota_to_imagen_fs.php?cod_diario=204000andpagina =111andseccion=0 [accessed 20 June de 2010]. NOM (Norma Oficial Mexicana). 2002. Available at http://dof.gob.mx/nota_to_imagen_ fs.php?cod_diario=28724andpagina=8and seccion=1 [accessed 10 May de 2010].

García, S., & L. Le Reste. 1986. Ciclos vitales, dinámica, explotación y ordenación de las poblaciones de camarones peneidos costeros. Food and Agriculture Organization of the United Nations. Rome, 180 p.|

Penn, J. W., & N. Caputi. 1986. Spawning stock-recruitment relationships and environmental influences on the tiger prawn Penaeus esculentus fishery in Exmouth Gulf, Western Australia. Aust. J. Mar. and Fresh. Res., 37(4): 491-505.

Gracia, A., A. R. Vázquez-Bader, F. ArreguínSánchez, L. E. Schultz-Ruiz & J. A. Sánchez. 1997. Ecología de camarones peneidos, 127-144. In: Flores-Hernández D., P. Sánchez-Gil, J. C. Seijo & F. ArreguínSánchez (Ed). Análisis y diagnóstico de los recursos pesqueros críticos del Golfo de México. EPOMEX Serie Científica, Campeche, México.

Reyna-Cabrera, I.E. & S. Ramos-Cruz. 1998. La pesquería de camarón de alta mar, 163-178. En: Tapia-García, M. (Ed). El Golfo de Tehuantepec: el eco� sistema y sus recursos, Universidad Autónoma Metropolitana-Iztapalapa, México. Ricker, W. E. 1975. Computation and interpretation of biological statistics of fish populations. Bull. Fish. Res. Board Can.,191: 1-382.

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Ruello, N. 1973. The influence of rainfall on the distributions and abundance of the school prawn Metapenaeus macleayi in the Hunter River region (Australia). Marine Biology., (23): 221-228.

Sparre, P. & S. C. Venema. 1995. Introduction to tropical fish stock assessment. Part. 1: Manual. Tech. Paper 306/1 Rev. 2. Food and Agriculture Organization of the United Nations, Rome, 407 p.

Sandoval-Quintero, M. E. & A. Gracia. 1998. Stages of gonadal development in the spotted pink srhimp Penaeus brasiliensis. J. Crusta. Biol., 18(4): 610-685.

Watson, R.A., C. T. Turnbull & K. J. Derbyshire. 1996. Identifying tropical penaeid recruitment patterns. Mar. Fresh. Res., 47(1):7785.

SMN (Servicio Meteorológico Nacional). 2008. Normales climatológicas 1971-2000 Estación Tonala, Chiapas. Available at http:// smn.cna.gob.mx/productos/normales/estacion/chis/ NORMAL. [accessed 01 September de 2009].

CICIMAR Oceánides 27(2): 59-63 (2012)

ADDITIONAL DATA RELATED TO THE DISTRIBUTION OF VENTRALLY SCLEROTIZED SPECIES OF Lepidophthalmus HOLMES, 1904 (DECAPODA: AXIIDEA, CALLIANASSIDAE, CHALLICHIRINAE) FROM THE TROPICAL EASTERN PACIFIC Hendrickx, M. E.1 & J. López 2

Laboratorio de Invertebrados Bentónicos, Unidad Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México . P.O. Box 811, +52669-985-2845, fax 669-982-6133 Mazatlán, 82000 Sinaloa, México. 2CCCNPESCA, San Salvador, El Salvador. email: michel@ola.icmyl.unam. mx 1

ABSTRACT.- Specimens of the two species of “ventrally sclerotized” Lepidophthalmus currently known from the eastern tropical pacific were collected at El Salvador and Mexico. These specimens represent additional records and support the idea that L. bocourti and L. eiseni should be considered as separated species.

Keywords: Callianassidae, Lepidophthalmus, eastern tropical Pacific. Información adicional relacionada con la distribución de especies de Lepidophthalmus Holmes, 1904 (Decapoda: Axiidea, Callianassidae, Challichirnae) con esclerosis ventral en el Pacífico este tropical RESUMEN.- Especímenes de las dos especies de Lepidophthalmus con esclerosis ventral, conocidas para el Pacífico este tropical fueron recolectadas en El Salvador y México. Representan registros adicionales y apoyan la idea de que L. bocourti y L. eiseni representan dos especies distintas.

Palabras clave: Callianassidae, Lepidophthalmus, Pacifico este tropical. Hendrickx, M. E. & J. López. 2012. Additional data related to the distribution of ventrally sclerotized species of Lepidophthalmus holmes, 1904 (Decapoda: Axiidea, Callianassidae, Challichirinae) from the tropical eastern Pacific. CICIMAR Oceánides, 27(2): 59-63.

INTRODUCTION A recent review of the “Thalassinidean” families and genera from the American continent has provoked a complete reorganization of the group. New taxa have been defined or moved from one family/genus to another, some little known species have been rediscovered and sometimes redescribed, and the entire infraorder “Thalassinoidea” has been restructured in order to follow arguments in favor of dividing this paraphyletic group into two separate infraorders: Gebiidea and Axiidea. All details related to this are available in previously published literature (see Sakai & de Saint Laurent, 1989; Lemaitre & Ramos, 1992; Felder & Manning 1997; Sakai, 1999, 2005; Felder 2003; Robles et al., 2009; De Grave et al., 2009). A worldwide review of the Callianassidae was presented by Sakai (1999), followed by an updated review of the Callianassoidea (Sakai, 2005). Sakai (2005) divided the species of Callianassidae in eight subfamilies (three new) and 14 genera. Sakai concluded that the genus Lepidophthalmus (Holmes, 1904), includes in the subfamily Callichirinae (Manning & Felder, 1991) 13 species: six in the western Atlantic, four in the Indo-West Pacific, one in the eastern Atlantic and Mediterranean, and two in the eastern Pacific. Sakai (2005), however, did not follow Felder (2003) who presented a comprehensive review of material belonging to Lepidophthalmus from the eastern Pacific and Fecha de recepción: 19 de enero de 2012

withdrew L. eiseni Holmes, 1904 from the synonymy of L. bocourti (A. Milne-Edwards, 1870) (originally described as Callianassa bocourti). After reviewing numerous specimens from southern Mexico to Panama, the type material of Callianassa bocourti, and the possible types of Lepidophthalmus eiseni, Felder (2003) concluded that L. bocourti and L. eiseni were both to be considered as valid species based on the shape of the ventral abdominal sclerites (“ventrally sclerotized” species), the presenceabsence of distolateral spines on the basis of pleopods 3-5, and the shape of the terminal article of the male gonopod. Material recently obtained from coastal lagoons in Mexico and El Salvador, along the Pacific coast of America, was examined. It contained several specimens of Lepidophthal� mus. Based on the review by Felder (2003), we came to the conclusion that the examined material belongs to the two “ventrally sclerotized” species of Lepidophthalmus from the eastern Pacific. This material is reported herein. MATERIAL AND METHODS All specimens were collected by hand from coastal lagoons in El Salvador and along the Pacific coast of Mexico (coastal lagoon and shrimp ponds), fixed with a solution of formaldehyde (5-10%), washed after a few days and preserved with 70% ethanol. Illustrations were made with the help of a camera lucida mounted Fecha de aceptación: 9 de mayo de 2012

HENDRICKX & LÓPEZ.

on a Nikon SMZ-10A dissecting microscope. Specimens are deposited in Mazatlán, Mexico. Abbreviations used are: CL, carapace length; TL, total length; MCL, major cheliped length; NM, not measured; EMU, Reference Collection of Invertebrates, Mazatlán, Sinaloa, Mexico; Coll., collector. RESULTS Lepidophthalmus bocourti (A. Milne-Edwards, 1870). Figs. 1, 2 A-C-E, 3 A-C. Callianassa bocourti A. Milne-Edwards, 1870: 95. (?) Lepidophthalmus bocourti.- Sakai, 1999: 70, fig. 14c-d. Lepidophthalmus bocourti.- Felder: 2003, 431, figs. 1-19 (complete synonymy); Sakai, 2005: 149 (part, excluding treatment of L. eiseni as junior subjective synonym).

Material examined.- One female (CL/TL/ MCL: 19.8/95.0/45.0 mm), Caimanero lagoon, south of Mazatlán, Sinaloa, 1979 (EMU-172). One male (CL/TL/MCL: 17.2/75.0/47.5 mm), Estero el Verde, north of Mazatlán, Sinaloa, sandy-mud, 11 July 1979 (coll. Michel E. Hendrickx) ) (EMU-9599). Three males (CL/TL/MCL: 13.8/66.0/42.0 mm; 12.2/56.0/NM mm; 9.5/51.0/NM mm) and two females (CL/TL/MCL: 17.8/82.5/NM mm; 11.0/41.0/NM mm), Barra de Santiago (around 13o42’30”N, 90o02’W), El Salvador, intertidal in muddy-sand (about 20 cm deep), July 2003 (coll. J.L. Salazar Linares) (EMU-6484, 6487, 6486, 6488, 6489). Three females (one ovigerous), carapace length 9.6-13.1 mm, total length 41.0-58.0 mm (without first pair of chelipeds), El Salvador, intertidal in muddy-sand (about 20 cm deep), July 2003 (coll. J.L. Salazar Linares) (EMU-6543).

Figure 1. Lepidophthalmus bocourti (A. Milne-Edwards, 1870) (EMU-6484). A. Lateral view. B. Dorsal view of anterior part of cephalothorax. C. Major (right) cheliped, outer view. D. Same, inner view of carpus-manus. Scale bar, 3 mm.

Lepidophthalmus FROM THE TROPICAL EASTERN PACIFIC

Figure 2. A, C, E. Lepidophthalmus bocourti (A. Milne-Edwards, 1870) (EMU-6484). B, D, F. Lepidophthalmus eiseni Holmes, 1904 (EMU-6544). A, B. Ventral view of first and second abdominal somites of male. C, D. Dorsal view of telson. E,F, Lateral view of carapace.

One male (CL/TL/MCL: 18.0/76.0/46.5 mm), SW part of Caimanero lagoon, south of Mazatlán, Sinaloa, Mexico, intertidal in muddy-sand, 14 November 2004 (coll. X.C. Ramos Sánchez) (EMU-6485). One male, carapace length 21.0 mm, total length 81.5 mm, shrimp-farm La Astoria, Navolato, Sinaloa, in muddy bank, 14 January 2005 (coll. M. Ruiz Guerrero) (EMU-6490). One female (CL/TL/MCL: 10.9/51.0/26.0 mm), shrimp-farm, Nayarit, January 2005 (EMU9613). Remarks.- The major characters on which Felder (2003) based its re-description of L. bo� courti were all observed in our material (Figs. 1, 2). The ventral, median sclerite on the second abdominal somite is clearly hourglass-shaped (Fig. 2 A); the posterolateral lobes of telson are sharp, subtriangular, and the sulci separating

these from the rounded median lobe are moderately deep (Fig. 2 C); pleopods 3-5 feature a sharp distolateral spine on basal segment (Fig. 3 A); the male first pleopod features a small subterminal tooth, narrower than the terminal tooth (Fig. 3 C). In lateral view, the carapace features a series of short sulci forming an indefinite pattern (Fig. 2 E), while in L. eiseni this pattern is much more regular and elaborated (see infra). According to Felder (2003: 434), the material reported as L. bocourti by Lemaitre and Ramos (1992) for Colombia and by Staton et al. (2000) for Panama does not belong to any of the two sclerotized species presently known from the East Pacific but rather to an undescribed species (maybe the same species) lacking these sclerotized structures altogether. Distribution range.- According to Felder (2003), L. bocourti is known with certainty from

HENDRICKX & LÓPEZ.

Figure 3. A, C. Lepidophthalmus bocourti (A. Milne-Edwards, 1870) (EMU-6484). B, D. Lepidophthalmus eiseni Holmes, 1904 (EMU-6544). A, B. Fifth right pleopod (without setae). C, D. Male first, right gonopod.

Chiapas (Puerto Madero), Mexico to Panama, including positive records from El Salvador and Costa Rica. The material examined extends the northernmost limit to Sinaloa. Lepidophthalmus eiseni Holmes, 1904. Figs. 2 B-D-F, 3 B-D Lepidophtahlmus Eiseni Holmes, 1904: 311, Plate 35, Figs. 6-13. Lepidophthalmus eiseni.- Sakai, 1999: 70 (as junior subjective synonym of Callianassa bo� courti A. Milne-Edwards, 1870); 2005: 149 (as junior subjective synonym of Callianassa bo� courti A. Milne-Edwards, 1870).- Felder, 2003: 436, Figs. 20-29 (complete synonymy). Material examined.- One male (CL/TL: 11.8/48.0 mm) (major chelipeds missing), Barra de Santiago (about 13o42’30”N, 90o02’W), El Salvador, intertidal in muddy-sand (about 20 cm deep), July 2003 (coll. J.L. Salazar Linares) (EMU-6544).

Remark.- The male specimen of L. eiseni was collected together with three females of L. bocourti (EMU-6542), thus indicating that both species are sympatric, as noted by Felder (2003: 434) in Nicaragua. Although this male had lost major chelipeds, it was easily separated from these three females on the basis of the main diagnostic characters provided by Felder (2003), including: the quadrate shape of the ventral median sclerite on the second abdominal somite (Fig. 2 B); the posteriorly trilobate telson, with posterolateral lobes rounded and separated from the median lobe by a shallow sulcus (Fig. 2 D); the pleopods 3-5 with anterior lobe of basis rounded, without ventral spine (Fig. 3 B); the male first pleopod clearly bifid, the subterminal tooth similar in shape and size to the terminal tooth (Fig. 3 D). The posterolateral part of the carapace features a complex, indefinite honeycomb pattern of low carina (Fig. 2 F) which was noted and illustrated by Holthuis (1954: Fig. 3). The other illustrations available

Lepidophthalmus FROM THE TROPICAL EASTERN PACIFIC

for this species were published by Holmes (1904: Plate 35) for the original description, and by Bott (1955). Distribution range.- According to Felder (2003), L. eiseni is known with certainty from Nayarit, Mexico to Costa Rica, including positive records in Guatemala, Nicaragua, and El Salvador. The type locality in “San José del Cabo”, Mexico, is uncertain. ACKNOWLEDGEMENTS The authors thank the following persons who collected or donated material of species of Lepidophthalmus: J.L. Salazar Linares (El Salvador), X.C. Ramos Sanchez, L. Sanchez Osuna, and M. Ruiz Guerrero (Mexico). G. Valenzuela prepared figures 1 and 2 C. We also thank M. Cordero Ruiz for the editing of the final manuscript and preparation of electronic files (text and figures), and F. Fiers (Belgian Royal Institute of Natural Sciences) for providing literature. REFERENCES Bott, R. Von. 1955. Dekapoden (Crustacea) aus El Salvador. 2. Litorale Dekapoden, auber Uca. Senckenb. Biol., 36 (1/2): 45-72. De Grave, S., N.D. Pentcheff, S.T. Ahyong, T.Y. Chan, K.A. Crandall, P.C. Dworschak, D.L. Felder, R.M. Feldmann, C.H.J.M. Fransen, L.Y.D. Goulding, R. Lemaitre, M.E.Y. Low, J.W. Martin, P.K.L. Ng, C.E. Schweitzer, S.H. Tan, D. T. Shudy & R. Wetzer. 2009. A classification of living and fossil genera of decapod crustaceans. Raffles Bull. Zool. (Supl.) 21: 1–109. Felder, D.L. 2003. Ventrally sclerotized members of Lepidophthalmus (Crustacea: Decapoda: Thalassinidea) from the eastern Pacific. Ann. Naturhist. Mus. Wien, 104B: 429-442. Felder, D.L. & R.B. Manning. 1997. Ghost shrimps of the genus Lepidophthalmus from the Caribbean region, with description of L. richardi, new species, from Belize (Decapoda: Thalassinidea: Callianassidae). J. Crust. Biol., 17 (2): 309-331. Felder, D.L. & R.B. Manning. 1998. A new ghost shrimp of the genus Lepidophthalmus from the Pacific coast of Colombia (Decapoda: Thalassinidea: Callanassidae). Proc. Biol. Soc. Wash., 111 (2): 398-408.

Holmes, S.J. 1904. On some new or imperfectly known species of west American Crustacea. Proc. Cal. Acad. Sci. (ser. 3, Zoology), 3: 307-331. Holthuis, L.B. 1954. On a collection of decapod Crustacea from the Republic of El Salvador (Central America). Zool. Verh., 23: 1-43. Lemaitre, R. & G.E. Ramos. 1992. A collection of Thalassinidea (Crustacea: Decapoda) from the Pacific coast of Colombia, with descriptions of a new species and a checklist of Eastern Pacific species. Proc. Biol. Soc. Wash., 105 (2): 343-358. Manning, R.B. & D.L. Felder. 1991. Revision of the American Callianassidae (Crustacea: Decapoda: Thalassinidea). Proc. Biol. Soc. Wash., 104 (4): 764-792. Milne Edwards, A. 1870. Révision du genre Callianassa (Leach). Arch. Mus. Hist. Nat., Paris, 6: 75-101. Robles, R., C.C. Tudge, P.C. Dworschak, G.C.B Poore & D.L. Felder. 2009. Molecular Phylogeny of the Thalassinidea based on Nuclear and Mitochondrial Genes, 309-326. In: Martin, J.W., K.A. Crandall & D.L. Felder (eds.) Decapod Crustacean Phylogenetics. Crustacean Issues 18 CRS Press, Boca Raton, FL, USA, 616 p. Sakai, K. 1999. Synopsis of the family Callianassidae, with keys to subfamilies, genera and species, and the description of new taxa (Crustacea: Decapoda: Thalassinidea). Zool. Verh., 326: 1-152. Sakai, K. 2005. Callianassoidea of the world (Decapoda, Thalassinidea). Crustaceana Monographs 4. 285 p. Sakai, K. & M. de Saint Laurent. 1989. A check list of Axiidae (Decapoda, Crustacea, Thalassinidea, Anomura), with remarks and in addition descriptions of one new subfamily, eleven new genera and two new species. Naturalist, 3: 1-104. Staton, J.L., D.W. Foltz & D.L. Felder. 2000. Genetic variation and systematic diversity in the ghost shrimp genus Lepidophthal� mus (Decapoda: Thalassinidea: Callianassidae). J. Crust. Biol., 20 (special number): 157-169.

CICIMAR Oceánides 27(2): 65-69 (2012)

COASTAL SEA SURFACE TEMPERATURE RECORDS ALONG THE BAJA CALIFORNIA PENINSULA Sicard-González, M.T., M.A, Tripp-Valdéz, L. Ocampo, A.N. Maeda-Martínez & S.E. Lluch-Cota Centro de Investigaciones Biológicas de Noroeste (CIBNOR), Mar Bermejo 195, Playa Palo de Santa Rita, La Paz, B.C.S. 23096, México. Tel.: +52 (612) 123-8484 ext. 3302. Fax: +52 (612) 125-3625. email: tsicard@ cibnor.mx

Registros costeros de temperatura superficial del mar en la Península de Baja California

RESUMEN. El análisis de series ambientales de temperatura de alta resolución temporal en las zonas costeras permitirá caracterizar mejor las formas y escalas de variación. Las bases de datos disponibles actualmente carecen de suficiente resolución para detectar variaciones ambientales a escalas de horas y días. En este trabajo damos a conocer una colección de registros de alta frecuencia de diversos sitios a lo largo de las costas de la Península de Baja California. Hasta el momento se tienen 47 sitios; sin embargo, esta red de monitoreo pretende expandirse con el objetivo de generar bases de datos de acceso público y gratuito, proporcionando una valiosa herramienta no solo para la investigación, sino también para aplicaciones como la producción acuícola. Sicard-González, M.T., M.A, Tripp-Valdéz, L. Ocampo, A.N. Maeda-Martínez & S.E. Lluch-Cota. Coastal sea surface temperature records along the Baja California peninsula. CICIMAR Oceánides, 27(2): 65-69.

The main physical factor controlling the abundance and distribution of organisms in their habitat is environmental temperature through biological process such as mortality, reproduction, recruitment and growth (PonceDíaz et al., 2003). Therefore, species that live in highly variable environments must be adapted to different thermal conditions (Lluch-Belda et al., 2000). The Baja California peninsula exhibits strong environmental fluctuations varying in timescales from hourly to interdecadal scales (Ponce-Díaz et al., 2003; Lluch-Belda et al., 2003; Lavin et al., 2003; Lluch-Cota et al., 2007). To understand the way in which temperature variations affect the structure and function of marine ecosystems it is essential to analyze each one of the timescales for variation (circadian, fortnightly, monthly, seasonal, interannual, and longer term), and how they behave in different ecosystems (coastal lagoons, estuaries, shelf seas, open ocean, etc). Existing databases of sea surface temperature like HadISST1 (Rayner et al., 2003), OISST.v2 (Reynolds et al., 2002) and ERSST.v3 (Smith et al., 2008) are freely available, however, those databases do not have enough temporal resolution to detect large daily temperature fluctuations (Sicard et al., 2006; Hughes et al., 2009). Temperature monitoring at higher-than-monthly resolution along the coasts of Baja California generates valuable information not only for the understanding of the effects of temperature variations on coastal ecosystems, but also for applications such as the evaluation of potential locations for aquaculture of selected species, or for selection of physiologically suitable species for particular aquaculture sites. Fecha de recepción: 8 de febrero de 2012

Over the last decade several data loggers have been installed along the coasts of the Baja California peninsula and maintained with resources from projects sponsored by governmental and non-governmental sources, generating valuable data, albeit with different timescales. Recently, this data has been integrated into an online database with the purpose of: 1) Making data records available to the scientific community and farmers for scientific studies and to aid in the selection of aquaculture locations, respectively. 2) Encouraging a policy of data sharing for the benefit of the society, by providing a freely available tool for scientists and aquaculture farmers. 3) Increasing and continuing the monitoring effort by inviting scientists and other individuals whose activities are connected with coastal areas, to participate by deploying instruments at these sites. The authors hope that this policy of cooperation will engender a general sharing of data between different research groups, and that the temperature data can be incorporated into the general database. The temperature records are from different locations along the Pacific coast of Baja California Sur and inside the Gulf of California (Fig. 1) using digital temperature loggers (Optic Stow Away Temp, Models: WTA32-5+37 and HOBO® Pendant Temperature/Light Data Logger, Onset Computer Corp.). In most cases the data loggers were deployed at a depth of 2 m with sampling interval of 30 minutes (any difference in these conditions are indicated in the database). The data treatment included a Fecha de aceptación: 18 de abril de 2012

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calculation of basic statistic parameters (mean, maximum, minimum and standard deviation; Table 1). All invalid or outlaying data (such as data recorded during periods when the logger was outside of the water) have been discarded. To date, data from 47 sites along the west coast of Baja California Sur and inside of the Gulf of California have been recorded (Fig. 1). Locations where the greater number of data loggers are located are: Laguna Ojo de Liebre, Bahía Ballenas, Bahía Magdalena, Bahía de La Paz and Bahía de Loreto, which are sites with economical importance given that there is fishery activity and active cultivation of ben-

thic mollusks at these locations (Casas-Valdéz & Ponce-Díaz, 1996). Data coverage of each one of the 47 data loggers is shown in Fig. 2a, and encompasses a time span beginning in January 2000 and ending in December 2011. The site with the largest data coverage for the aforementioned time span is Laguna San Ignacio (SIG) with more than 60%, followed by one series at Laguna Manuela (LMF) with a 56% and Rancho Bueno 2 (RB2) with 38% (Fig. 2c). The time period when more sites where monitored is from 2006 to 2010 (Fig. 2b). Table 1 shows the basic statistic descriptors (minimum, maximum, average and stan-

Table 1. List of 47 sites with sea surface temperature records. Sites marked in bold were used for annual cycle and frequency distribution of temperature; * sites with one record each 60 minutes; **sites with one record each 15 minutes. Region

Laguna Manuelas

Laguna Guerrero Negro Laguna Ojo de Liebre Bahía Tortugas Bahía Asunción La Bocana Punta Abreojos Laguna San Ignacio Santo Domingo Estero San Buto Bahía Magdalena

Bahía de La Paz

Bahía de Loreto

Sonora

Name 1 Laguna Manuela (Boca) Manuela (Camas de 2 Laguna cultivo) 3 Laguna Manuela (Fondo)* 4 Campo Chupa Lodo 5 El Conchalito 6 La ventana 7 El Mariscal 8 El Rincón 9 Queen 10 Arvin 11 Isla Asunción* 12 El Rito 13 La Bocana 14 Punta Abreojos 15 San Ignacio 16 Sol Azul 17 Santo Domingo 18 San Buto 19 Bahía Magdalena 1(9.5m) 20 Bahía Magdalena 2(11m) 21 Bahía Magdalena 3(14.7m) 22 Bahía Magdalena 4(17m) 23 Rancho Bueno 1 24 Rancho Bueno 2 25 Rancho Bueno 3 26 El Remate 27 Punta Arenas 28 Mogote (18m) 29 Mogote (7m) 30 Canal de San Lorenzo 31 Punta Diablo 32 Rancho Rodríguez 33 San Gabriel 34 Isla Gallo(20m) 35 Isla Gallo(7m) 36 Isla Gaviota (22m) 37 Isla Gaviota (7m) 38 El Portugués** 39 Balandra 40 Enfermería 41 Zacatecas 42 Candeleros 43 La Choya 44 Galeras 45 Puerto Escondido 46 Bahía Bacoherehuis 47 Bahía Kino

Code Minimum Maximum Mean SD

LMB

13.19

28.65

18.93 2.62 28.1834 -114.0608

LMC

10.71

30.27

19.78 2.97 28.1371 -114.0719

LMF CCH ECO LVE EMA ERI QUE ARV BAI BAE BOC PTA SIG SAZ SDO SBU BM1 BM2 BM3 BM4 RB1 RB2 RB3 ERE PAR MO1 MO2 SLO PDI RRO SGA IG1 IG2 GA1 GA2 EPO BAL ENF ZAC CAN LCH GAL PES BBA BKI

10.74 10.26 13.85 14.71 17.34 11.82 15.11 13.28 11.96 12.25 12.5 15.28 7.66 14.33 8.98 13.37 13.08 14.23 13.08 13.17 10.39 8.68 12.24 16.31 18.04 19.19 19.95 18.53 15.19 20.04 19.67 19.95 20.33 18.71 18.9 24.86 12.3 16.99 9.57 17.91 16.94 17.62 18.33 18.62 13.88

36.3 33.22 30.86 25.51 22.89 25.22 25.96 23.13 33.77 22.99 29.95 29.35 39.96 36.62 32.09 34.69 28.75 31.88 29.25 28.06 38.14 38.83 33.54 31.58 30.56 22.24 23.29 25.9 32.98 32.19 29.5 21 21.09 22.81 23.97 38.14 39.5 37.05 35.65 30.29 30.67 31.02 33.22 35.12 33.63

21.56 20.75 19.15 18.81 20.5 17.14 19.88 17.15 22.55 16.94 20.74 22.12 21.17 22.19 23.83 24.26 19.18 20.69 19.48 18.98 22.42 22.86 22.45 23.01 25.7 20.88 21.61 21.07 22.82 24.55 24.19 20.43 20.71 21.59 21.69 29.13 25.13 26.19 22.72 22.95 22.79 23.96 24.35 27.74 24.13

4.23 3.44 3.22 2.78 1.73 2.67 1.83 2.02 6.13 2.64 4.03 3.27 4.43 3.89 4.06 3.4 3.74 3.65 3.99 3.89 4.29 4.13 3.76 3.35 2.65 0.45 0.62 1.27 3.18 1.95 1.77 0.2 0.21 0.69 0.65 2.16 3.77 4.28 4.11 3.77 3.51 4.05 3.66 3.91 5.28

28.1311 27.9946 27.7763 27.7358 27.6800 27.6629 27.7779 27.6477 27.1462 27.1339 26.7862 26.8194 26.793 26.7914 25.5655 24.7746 24.658 24.6319 24.5504 24.6452 24.3738 24.3748 24.3500 24.3113 24.0445 24.1839 24.1839 24.3878 24.3125 24.2019 24.4268 24.4631 24.4631 24.2892 24.2892 24.7476 24.3166 24.2293 24.1209 25.7448 26.0449 25.7382 25.8096 26.5261 28.7999

-114.0680 -114.0716 -114.2781 -114.2696 -114.1579 -114.8656 -114.6362 -114.8665 -114.3767 -114.2953 -113.6868 -113.4347 -113.1515 -113.1561 -112.0731 -112.0477 -112.0673 -111.9189 -111.9479 -111.9634 -111.6430 -111.5773 -111.4811 -111.4022 -109.8259 -110.3797 -110.3797 -110.3218 -110.3365 -110.5270 -110.3698 -110.3861 -110.3861 -110.3406 -110.3406 -110.6782 -110.3212 -110.3193 -110.4334 -111.2277 -111.1816 -111.0447 -111.3075 -109.1531 -111.9176

OPEN SEA SURFACE TEMPERATURE DATABASE

Figure 1. Map with location of the 47 registered sites so far along the coast of the Baja California peninsula.

Figure 2. a) Total observation period for each logger with a within the 2000 to 2012 time window; x axis is graduated in month; y axis corresponds to each of the 47 sites. b) Coverage percentage for each month. c) Coverage percentage for each logger.

SICARD et al.

dard deviation) of the time series for each of the sites. Sites from the Pacific side of the peninsula (sites 1 to 26) tended to have colder average values (between 16.9 and 24.3°C) with a larger standard deviation (1.7 to 6.1) compared with sites inside the Gulf of California (sites 27 – 45; averages between 20.4 and 29.1°C and standard deviations between 0.2 and 5.3). Figure 3 shows the annual cycles of monthly averaged temperature and amplitude (daily maximum -minimum) for the ten sites with the largest and most continuous data records (Table 1). The amplitude values indicate the distribution of registered daily temperature fluctuations for each location and month. Figure 4 reports the frequency distributions of temperature of the same ten sites (Table I). This mode of presenting the temperature records of

a location facilitates the rapid identification of temperature ranges and frequent values, and the comparison with physiological thermal preferences of marine populations, including those with aquacultural potential (Sicard et al., 2006) It should be noted that many of the records correspond to coastal water bodies, where local dynamics (exchange rates with open ocean, local heating, depth) play a major role in shaping the temperature changes, and thus should be interpreted as representative of those water bodies and not the surrounding open coastal systems. The online database is currently hosted in the Centro de Investigaciones Biológicas del Noroeste (CIBNOR) by the Laboratorio de Ecofisiología de Organismos Acuáticos (LEOA;

Figure 3. Annual cycle for the ten sites with most continuous records. Monthly mean temperature values are shown with solid lines; dashed lines correspond to monthly maximum and minimum. Mean amplitude values are indicated with squares± SD. Notice mean temperature variations according to site.

OPEN SEA SURFACE TEMPERATURE DATABASE

Figure 4. Frequency distribution of temperature for the ten sites with most continuous records (gray bars). Solid line corresponds to Kernel distribution for each site.

www.leoa.org.mx/RAF), and stored by the recently created Observatorio de los Mares y Costas de México (contact slluch@cibnor.mx). The temperature data is freely available online as a KMZ file, which is a file type supported by the Google Earth®software program. This provides a free and straightforward platform to explore and visualize the information generated from all observation sites. ACKNOWLEDGMENTS This report is a product of the Laboratorio de Ecofisiología de Organismos Acuáticos (LEOA) and the Observatorio de los Mares y Costas de México. Funding was provided by the Project SEMARNAT-CIBNOR: Fortalecimiento de infraestructura del observatorio de los mares y costas de México para el manejo

de información ambiental, zona del Pacífico. REFERENCES Casas-Valdéz, M. & G. Ponce-Díaz (eds). 1996. Estudio del potencial pesquero y acuícola de Baja California Sur. Vol. 1 and 2, B.C.S., México: Secretaría de Medio Ambiente, Recursos Naturales y Pesca, 693p. Hughes, S., N. P. Holliday, E. Colbourne, V. Ozhigin, H. Valdimarsson, S. Østerhus & K. Wiltshire. 2009. Comparison of in situ time-series of temperature with gridded sea surface temperature datasets in the North Atlantic. ICES Journal of Marine Science, 66 (7): 1467 – 1479. Lavin, M.F., E. Palacios-Hernández & C. Ca-

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brera.2003. Sea surface temperature anomalies in the Gulf of California. Geofísi� ca Internacional, 42(3): 363 – 375. Lluch-Belda, D., M.E. Hernández-Rivas, R. Saldierna-Martínez & R. Guerrero-Caballero. 2000. Variabilidad de la temperatura superficial del mar en Bahía Magdalena, B.C.S. Oceánides. 15(1): 1 – 23. Lluch-Belda, D., S.E. Lluch-Cota & D. LluchCota. 2003. Scales of interannual variability in the California Current system: Associated physical mechanisms and likely ecological impacts. CalCOFI Rep., 44: 76 – 85. Lluch-Cota, S.E., E.A. Aragón-Noriega, F. Arreguín-Sanchez, D. Aurioles-Gamboa & J.J. Bautista-Romero. 2007. The Gulf of California: Review of ecosystem status and sustainability challenges. Progress in Oceanography, 73: 1 – 26. Ponce-Díaz, G., S.E. Lluch-Cota, J.J. BautistaRomero & D. Lluch-Belda. 2003. Caracterización multiescala de la temperatura del mar en una zona de bancos de abulón (Haliotis spp.) en Bahía Asunción, Baja California Sur, México. Ciencias Marinas, 29(3): 291 – 303.

Rayner, N.A., D.E. Parker, E.B. Horton, C.K. Folland, L.V. Alexander & D.P. Rowell. 2003. Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. Journal of Geophysical Research, 108: 4407. Reynolds, R.W., N.A. Rayner, T.M. Smith, D.C. Stokes & W. Wang. 2002. An improven in situ and satellite SST analysis of climate. Journal of Climate, 20: 5473 – 5496. Sicard, M.T., A.N. Maeda-Martínez, S.E. LluchCota, C. Lodeiros, L. M. Roldán-Carrillo & R. Mendoza-Alfaro. 2006. Frequent monitoring of temperature: an essential requirement for site selection in bivalve aquaculture in tropical-temperate transition zones. Aquaculture Research, 37: 1040 – 1049. Smith, T.M., R. W. Reynolds & J. Lawrimore. 2008. Improvements to NOAA´s historical merged land-ocean surface temperature analysis (1880 – 2006). Journal of Climate, 21: 2283 – 2296.

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