CICIMAR Oceánides Vol. 27 (2) 2012

Volumen 27(2) Diciembre 2012

ISSN 1870-0713

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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 Te-huantepec, Mexico. LÓPEZ-CHÁVEZ, O., G. ACEVES-MEDINA, R. J. SALDIERNA-MARTÍNEZ, S. P. A. JIMÉNEZ-ROSENBERG, J. P. MURAD-SERRANO, Á. MARÍN-GUTIÉRREZ & O. HERNÁNDEZ-HERNÁNDEZ. 1

Metabolic scaling regularity in aquatic ecosystems. SALCIDO-GUEVARA, L. A., F. ARREGUÍN-SÁNCHEZ, L. PALMERI & A. BARAUSSE. 13

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. AGUÍÑI-GA & E. F. BALART 27

Proliferation of Amphidinium carterae (Gymnodiniales: Gymnodiniaceae) in Bahía de La Paz, Gulf of California. GÁRATE-LIZÁRRAGA, I. 37

Marine and lagoon recruitment of Litopenaeus vannamei (Boone, 1931) (Decapo-da: Penaeidae) in the “cabeza de toro-la joya buenavista” lagoon system, Chiapas, Mexico. CERVANTES-HERNÁNDEZ, P., M. A. GÓMEZ-PONCE & P. TORRES-HERNÁNDEZ 51

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 59Coastal 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. 65

CICIMAR Oceánides 27(2): 1-11 (2012)

Fecha de recepción: 7 de febrero de 2012 Fecha de aceptación: 13 de agosto de 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. Jiménez-Rosenberg¹, J. P. Murad-Serrano², Á. Marín-Gutiérrez² & O. Hernández-Hernández²

1Departamento 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: [email protected]

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, MéxicoRESUMEN. 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.

INTRODUCTIONThe 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 pri-mary 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 (Orte-ga–García et al., 2000), and most of them are limited to a few taxonomic groups such as co-pepods and euphausiids (Farber-Lorda et al., 1994; Fernández-Alamo et al., 2000).

The Gulf of Tehuantepec is also a key bio-geographic area. Bahía Tangolunda (Fig. 1) is a transition area between two main biogeograph-ic regions: the Panamic and Mexican provinces (Briggs, 1974). Although these biogeographic

provinces were based mainly on fishes, the ich-thyofauna of the Gulf of Tehuantepec is still not well known with only few descriptive studies in this area. The pioneer studies described a de-mersal 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,

2 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 composi-tion in the Gulf of Tehuantepec.

Studies on the early life stages of fish pro-vide evidence of the adult presence, as well as their reproduction; both are key elements in the biogeographical sense, and for recognizing re-productive and nursery habitats. At the present, there is no information at the species level con-cerning the fish larvae of this important area. The work by Ahlstrom (1972) during the EAST-ROPAC 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 re-gion of the gulf, but they identified specimens only to family and order taxonomic levels.

During the summer of 2007 (July 3rd-12th) and spring 2008 (May 26th-June 8th) the Secre-taria de Marina made two oceanographic sur-veys 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

summer in this area corresponds with the dry season in which the Tehuano winds (which flow perpendicular to the coast) decrease signifi-cantly (Gallegos–García & Barberán–Falcón, 1998) and is characterized by a higher abun-dance 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 in-creases (Tapia-García et al., 1994).

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 METHODSThe 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 riv-er 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

99 98 97 96 95 94 93

West Longitude

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titud

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May 2008

July 2007

-115 -110 -105 -100 -95 -90

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Pto.Escondido Bahía

Tangolunda

Salina Cruz

México

Pacific Ocean

Gulf ofTehuantepec

Gulf of California

BahíaSebastiánVizcaino

Pto. ÁngelSuchiate

river

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

3FISH LARVAE FROM THE GULF OF TEHUANTEPEC

surface temperature ranges between 25º and 30º C (Gallegos–García & Barberán-Falcón, 1998).

Two oceanographic surveys were conduct-ed, one in summer (July 3rd to 12th, 2007) and one in spring (May 26th –June 8th, 2008). Zoo-plankton 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 shal-low, 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 digi-tal 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 bo-rate, 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 follow-ing Moser (1996). Identified organisms were counted and their abundance was standardized on each sampling station to 10 m² of sea sur-face (Smith & Richardson, 1979). When speci-mens could not be identified to species level in the absence of descriptions, they were iden-tified to family or genus and the meristic and morphometric characteristics of each speci-men 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 add-ing 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 Nel-son (2006) and includes biogeographic affinity (tropical, transitional), habitat of adult distribu-tion (shallow demersal, deep demersal, epipe-lagic, mesopelagic or bathypelagic) based on Eschmeyer (2009). All specimens were pre-served 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 Tehuante-pec 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–Medi-na, 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 re-gions and the Gulf of Tehuantepec.

RESULTSA total of 145 taxa were found, 73 were

identified to species, 43 to genus and 29 to family (Table 1). From the 55 identified fami-lies, 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, represent-ing 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 com-position 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 pe-lagic 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


Taxon % HA Taxon % HAO. Anguiliformes Ophidion sp. 2 <0.1 sd S. O. Congroidei O. Lophiiformes F. Ophichthidae S.O. LophioideiMyrophis vafer Jordan and Gilbert, 1883 <0.1 sd F. LophiidaeOphichthus sp. 1 <0.1 sd Lophiodes sp. 1 <0.1 ddOphichthus triserialis (Kaup, 1856) <0.1 sd F. MelanocetidaeOphichthus zophochir Jordan and Gilbert, 1882 <0.1 sd Melanocetidae sp. 1 <0.1 bpOphichthus sp. 2 <0.1 sd Melanocetidae sp. 2 <0.1 bpF. Congridae O. MugiliformesAriosoma gilberti (Ogilby, 1898) <0.1 sd F. MugilidaeBathycongrus varidens (Garman,1899) <0.1 sd Mugil cephalus Linnaeus, 1758 <0.1 sdCongridae sp. 1 <0.1 sd O. BeloniformesParaconger californiensis Kanazawa, 1961 <0.1 sd F. ExocoetidaeO. Clupeiformes Cheilopogon sp. 1 <0.1 cpS.O. Clupeoidei Cheilopogon sp. 2 <0.1 cpF. Clupeidae Cheilopogon sp. 3 <0.1 cpEtrumeus teres (DeKay, 1842) <0.1 cp Fodiator rostratus (Günther, 1866) <0.1 cpHarengula thrissina (Jordan and Gilbert, 1882) <0.1 cp Prognichthys tringa Breder, 1928 <0.1 cpOpisthonema sp. 1 2.7 cp F. HemiramphidaeOpisthonema sp. 3 4.2 cp Oxyporhamphus micropterus (Valenciennes, 1847) <0.1 cpF. Engraulidae O. StephanoberyciformesCetengraulis mysticetus (Günther, 1867) 1.8 cp F. MelamphaidaeO. Argentiniformes Melamphaes sp. 1 <0.1 mpS.O. Argentinoidei Melamphaidae sp. 1 <0.1 mpF. Microstomatidae Melamphaidae sp. 2 <0.1 mpBathylagoides nigrigenys (Parr, 1931) <0.1 bp Scopelogadus mizolepis (Günther 1878) <0.1 mpBathylagoides wesethi (Bolin, 1938) <0.1 bp O. BeryciformesO. Stomiiformes S.O. HolocentroideiS.O. Phoschthyoidei F. HolocentridaeF. Phosichthyidae Myripristis leiognathos Valenciennes, 1846 <0.1 sdVinciguerria lucetia (Garman, 1899) 14.3 mp O. ScorpaeniformesF. Stomiidae S.O. ScorpaenidaeIdiacanthus antrostomus Gilbert, 1890 <0.1 mp F. ScorpaenidaeO. Aulopiformes Pontinus sp. 1 3.3 sdS.O. Synodontoidei Scorpaenodes xyris (Jordan and Gilbert, 1882) <0.1 sdF. Synodontidae F. TriglidaeSynodus sp. 1 <0.1 sd Prionotus sp. 1 sdSynodus sp. 2 <0.1 sd O. PerciformesS.O. Alepisauroidei S.O. PercoideF. Scopelarchidae F. SerranidaeScopelarchoides nicholsi (Parr, 1929) <0.1 bp Cephalopholis panamensis (Steindachner, 1877) <0.1 sdF. Paralepididae Diplectrum sp. 1 <0.1 sdLestidiops neles (Harry, 1953) <0.1 op Diplectrum sp. 3 <0.1 sdLestidiops sp. 1 <0.1 op Epinephelus sp.1 <0.1 sdParalepididae sp. 1 <0.1 Paralabrax nebulifer (Girard 1854) <0.1 sdO. Myctophiformes Paralabrax maculatofasciatus Steindachner, (1868) <0.1 sdF. Myctophidae Serranus sp. 1 <0.1 sdBenthosema panamense (Tåning, 1932) 2.3 mp Serranus sp. 3 <0.1 sdDiaphus pacificus Parr, 1931 1.8 mp F. ApogonidaeDiogenichthys laternatus (Garman, 1899) <0.1 mp Apogon sp. 1 <0.1 sdHygophum atratum Garman, 1899 <0.1 mp F. CoryphaenidaeLampanyctus parvicauda Parr, 1931 <0.1 mp Coryphaena hippurus Linnaeus, 1758 <0.1 opO. Lampriformes F. CarangidaeF. Trachipteridae Caranx caballus Günther, 1868 <0.1 cpTrachipterus altivelis Kner, 1859 <0.1 cp Caranx sexfasciatus Quoy and Gaimard, 1825 1 cpO. Gadiformes Chloroscombrus orqueta Jordan and Gilbert, 1883 <0.1 cpF. Bregmacerotidae Decapterus sp. 1 <0.1 cpBregmaceros bathymaster Jordan & Bollman 1889 35.9 cp Naucrates ductor (Linnaeus, 1758) <0.1 cpBregmaceros sp. 1 <0.1 cp Oligoplites saurus (Bloch and Schneider, 1801) <0.1 cpO. Ophidiiformes Selar crumenophthalmus (Bloch, 1793) <0.1 cpS.O. Ophidioidei Selene peruviana (Guichenot, 1866) <0.1 cpF. Ophidiidae F. BramidaeCherublemma emmelas (Gilbert, 1890) <0.1 dd Bramidae sp. 1 <0.1 opOphidion sp. 1 <0.1 sd F. Lutjanidae

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).


(Aceves–Medina, 2003) and Bahía Sebastián Vizcaíno on the west coast of Baja California Sur (Jiménez–Rosenberg et al., 2007; Jimé-nez–Rosenberg, 2008).

The mode in the number of species by sam-pling station (18 taxa per sample) also shows a higher alpha diversity compared with other re-

gions of the Eastern Pacific (Table 5).DISCUSSION

This is the first descriptive work on the lar-val fish assemblage of the Gulf of Tehuantepec which includes 145 taxa from the Eastern Tropi-cal Pacific.

Taxon % HA Taxon % HALutjanus peru (Nichols & Murphy, 1922) <0.1 sd F. MicrodesmidaeLutjanus sp.1 <0.1 sd Clarkichthys bilineatus (Clark, 1936) <0.1 sdF. Lobotidae S.O. AcanthuroideiLobotes surinamensis (Bloch, 1790) <0.1 sd F. EphippidaeF. Gerreidae Chaetodipterus zonatus (Girard, 1858) <0.1 sdEucinostomus currani Zahuranec, 1980 <0.1 sd Ephippidae sp. 1 <0.1 sdEucinostomus dowii (Gill, 1863) <0.1 sd F. LuvaridaeEucinostomus gracilis (Gill, 1862) <0.1 sd Luvarus imperialis (Rafinesque, 1810) <0.1 sdF. Haemulidae S.O. ScombroideiHaemulidae sp. 1 <0.1 sd F. SphyraenidaeHaemulidae sp. 2 <0.1 sd Sphyraena ensis Jordan & Gilbert, 1882 <0.1 cpHaemulidae sp. 3 <0.1 sd F. ScombridaeHaemulidae sp. 4 <0.1 sd Auxis sp. 1 1.7 opHaemulidae sp. 5 <0.1 sd Euthynnus lineatus Kishinouye, 1920 <0.1 opF. Haemulidae F. IstiophoridaeHaemulon sp. 1 <0.1 sd Kajikia audax (Philippi, 1887) <0.1 opF. Polynemidae S.O. StromateoideiPolydactylus approximans (Lay & Bennett, 1839) <0.1 sd F. StromateidaeF. Sciaenidae Peprilus sp. 1 <0.1 sdSciaenidae sp. 1 <0.1 sd F. NomeidaeSciaenidae sp. 2 <0.1 sd Cubiceps pauciradiatus Günther, 1872 <0.1 opSciaenidae sp. 3 <0.1 sd Nomeidae sp. 1 <0.1Sciaenidae sp. 4 <0.1 sd Psenes sio Haedrich 1970 <0.1 opSciaenidae sp. 5 <0.1 sd O. PleuronectiformesSciaenidae sp. 6 <0.1 sd S.O. PleuronectoideiSciaenidae sp. 7 <0.1 sd F. ParalichthyidaeSciaenidae sp. 8 <0.1 sd Cyclopsetta panamensis (Steindachner, 1876) <0.1 sdF. Kyphosidae Etropus sp. 1 <0.1 sdKyphosidae sp. 1 <0.1 sd Paralichthyidae sp. 1 <0.1 sdS.O. Labroidei Syacium sp. 1 3.5 sdF. Pomacentridae Syacium sp. 2 2.9 sdAbudefduf troschelii (Gill, 1862) <0.1 sd F. PleuronectidaeStegastes sp. 1 <0.1 sd Pleuronectidae sp. 1 <0.1 sdF. Labridae F. BothidaeThalassoma sp. 1 <0.1 sd Bothus leopardinus (Günther, 1862) 1.8 sdS.O. Zoarcoidei Bothus sp. 1 sdF. Stichaeidae Monolene asaedai Clark, 1936 <0.1 sdStichaeidae sp. 1 <0.1 dd F. CynoglossidaeS.O.Trachinoidei Symphurus atramentatus Jordan & Bollman, 1890 <0.1 ddF. Uranoscopidae Symphurus callopterus Munroe & Mahadeva, 1989 <0.1 ddUranoscopidae sp. 1 <0.1 sd Symphurus chabanaudi Mahadeva & Munroe, 1990 <0.1 sdS.O. Blennioidei Symphurus elongatus (Günther, 1868) <0.1 sdF. Blenniidae Symphurus melanurus Clark, 1936 <0.1 sdHypsoblennius sp. 1 <0.1 sd Symphurus sp. 1 <0.1 sdOphioblennius steindachneri Jordan & Evermann, 1898

<0.1 sd Symphurus sp. 4 <0.1 sd

S.O. Gobioidei Symphurus sp. 5 <0.1 sdF. Eleotridae Symphurus sp. 6 <0.1 sdDormitator latifrons (Richardson, 1844) <0.1 sd Symphurus sp. 7 <0.1 sdEleotridae sp. 1 <0.1 sd Symphurus sp. 8 <0.1 sdErotelis armiger (Jordan & Richardson, 1895) <0.1 sd Symphurus sp. 9 <0.1 sdF. Gobiidae Symphurus williamsi Jordan & Culver, 1895 <0.1 sdCtenogobius manglicola (Jordan & Starks, 1895) <0.1 sd O. TetraodontiformesCtenogobius sagittula (Günther, 1862) <0.1 sd S.O. BalistoideiGobiidae sp. 1 <0.1 sd F. BalistidaeMicrogobius sp. 1 <0.1 sd Balistes polilepis Steindachner, 1876 <0.1 sdMicrogobius sp. 2 <0.1 sd Sufflamen verres (Gilbert & Starks, 1904) <0.1 sd

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).


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 Te-huantepec consists of a group of dominant spe-cies found in both, summer and spring seasons. Contrasting with other areas of the Mexican Pa-

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 ich-thyoplankton all year round (Franco–Gordo et al., 2001; Siordia-Cermeño et al., 2006). The abundance of the tropical–subtropical species

Family % NT Family % NT Family % NTBregmacerotidae 40 2 Eleotridae 0.4 3 Melanocetidae <0.1 2Phosichthyidae 14.3 1 Coryphaenidae 0.3 1 Triglidae <0.1 1Clupeidae 7.2 4 Sphyraenidae 0.3 1 Trachipteridae <0.1 1Paralichthyidae 7 5 Paralepididae 0.3 3 Bramidae <0.1 1Myctophidae 5.4 5 Balistidae 0.3 2 Microdesmidae <0.1 1Scorpaenidae 3.4 2 Melamphaidae 0.2 4 Labridae <0.1 1Sciaenidae 2.1 8 Ophichthidae 0.2 5 Istiophoridae <0.1 1Bothidae 2.1 3 Ophidiidae 0.2 3 Lobotidae <0.1 1Carangidae 2 8 Congridae 0.2 4 Stromateidae <0.1 1Engraulidae 1.8 1 Exocoetidae 0.2 5 Kyphosidae <0.1 1Cynoglossidae 1.8 13 Serranidae 0.1 8 Pleuronectidae <0.1 1Scombridae 1.7 2 Synodontidae 0.1 2 Uranoscopidae <0.1 1Gerreidae 1.4 3 Stomiidae 0.1 1 Apogonidae <0.1 1Lutjanidae 1.2 2 Pomacentridae 0.1 2 Luvaridae <0.1 1Nomeidae 1 3 Polynemidae 0.1 1 Holocentridae <0.1 1Hemiramphidae 0.9 1 Ephippidae 0.1 2 Stichaeidae <0.1 1Microstomatidae 0.6 2 Mugilidae 0.1 1 Lophiidae <0.1 1Haemulidae 0.4 6 Scopelarchidae <0.1 1Gobiidae 0.4 5 Blenniidae <0.1 2

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).

Species jul-07 (%) may-08 (%) G.M. S.D.Bregmaceros bathymaster 4462 31.4 10453 45.2 41 10.1Vinciguerria lucetia 3427 24.1 1926 8.3 22.3 7.8Syacium sp. 1 539 3.8 788 3.4 7.5 4.7Pontinus sp. 1 625 4.4 623 2.7 4.6 5.5Syacium sp. 2 212 1.5 868 3.8 3.7 5.5Diaphus pacificus 488 3.4 185 1 3.1 4.4Auxis sp. 1 517 3.6 135 0.6 3.1 4.4Bothus leopardinus 361 2.5 335 1.5 2.9 4.3Opisthonema sp. 3 170 1.2 1426 6.2 2.2 4.8Benthosema panamense 412 2.9 481 2.1 2.2 4.5Oxyporhamphus micropterus 107 0.8 227 1 2.1 3.3Diogenichthys laternatus 98 0.7 263 1.1 2.1 3.4Lutjanus peru 167 1.2 170 0.7 2 3.3Psenes sio 93 0.7 206 1 1.9 3.2Symphurus elongatus 61 0.4 215 1 1.9 3.2Caranx sexfasciatus 191 1.3 208 0.9 1.7 3.4Opisthonema sp. 1 0 0 1014 4.4 1.5 3.9Cetengraulis mysticetus 29 0.2 663 2.9 1.5 3.3Eucinostomus dowii 0 0 255 1.1 1.4 2.6

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.


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 de-scribing 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 Cali-fornia 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 Ameri-can Pacific Ocean has been determined from adult records in the Gulf of California and Pan-ama (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 (Fran-co–Gordo et al., 2001; Siordia-Cermeño et al., 2006). In our surveys, several juveniles of B.

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 ich-thyoplankton protocol analysis excludes them (Smith & Richardson, 1979), the high abun-dance 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; Si-ordia–Cermeño et al., 2006).

Larval abundancesurvey cp mp sd op bp dd nd Total

July-07 5399(37.9) 4571(32.2) 3205(22.6) 791(5.6) 146(1.0) 58(0.4) 38(0.3) 1420830 ± 8.5 63 ± 6.1 56 ± 3.1 13 ± 3.9 2 ± 3.3 1.2 ± 2.3 1 ± 2 280 ± 3

may-08 14253(61.6) 2972(12.9) 5216(22.6) 504(2.1) 143(0.6) 28(0.1) 9(0.03) 23125187 ± 3.6 29 ± 6.5 91 ± 2.9 5 ± 4.5 2 ± 3.1 1 ± 1.8 1.1 ± 1.4 452 ± 2.4

Number of speciessurvey sd cp mp op bp dd nd TotalJuly-07 57 (58.8) 19 (19.6) 10 (10.1) 5 (5.2) 3 (3.1) 1 (1) 2 (2.1) 97may-08 68 (61.8) 19 (17.3) 9 (8.2) 5 (4.5) 5 (4.5) 3 (2.7) 1 (0.9) 110

Total 91 25 12 6 5 3 3 145CS 34 13 7 4 3 1 62

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.

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).


Other coastal pelagic species also includ-ed 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 ecolog-ical 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 dur-ing 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 repre-sented 22 % of the abundance. This feature,

along with the lower abundance of larvae of mesopelagic species during spring, is relevant since in other regions of the Eastern Pacific, in-cluding 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 spe-cies 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 oceano-graphic processes that transport fish larvae of neritic species off the Gulf of Tehuantepec, and could explain also the lower abundance of lar-vae 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 Tehuante-pec is more than twice than in any other region studied in the Eastern Pacific. These results indicate that the Gulf of Tehuantepec is an im-portant reproduction area, mainly of species of coastal pelagic and demersal environments.

Even to family level, the Gulf of Tehuante-pec 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

NS R M NF. SourceCalifornia Current 31,214 249 6 ND Moser & Smith, 1993

Sebastián Vizcaíno 377 208 8 78 Jiménez-Rosenberg et al., 2007Gulf of California 464 283 4 53 Aceves-Medina 2003Jalisco-Colima 132 102 ND ND Franco-Gordo et al., 1999

Gulf of Tehuantepec 68 145 18 55 This workEastern Tropical Pacific 482 ND ND 56 Ahlstrom, 1971; Ahlstrom, 1972

Costa Rica Dome ND ND ND 37 Aguilar-Ibarra & Vicencio-Aguilar, 1994

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.


of highest diversity in the Mexican Pacific, even when compared with the Gulf of California, con-sidered one of the most diverse ecosystems in the Eastern Pacific (Walker, 1960; Thompson et al., 1979; Castro–Aguirre et al., 1995; Acev-es–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–Gar-cía et al., 2000). This together with the high species richness found, make the Gulf of Tehu-antepec a key area in the understanding of the oceanic ecosystems from low latitudes, which are poorly studied.

ACKNOWLEDGEMENTSWe thank the Instituto Politécnico Nacio nal,

Secretaria de Investigación y Posgrado IPN and Consejo Nacional de Ciencia y Tec nología for the funding through the projects SIP-20090303; SIP-20090421; SIP-20120878 and CONACYT 90331. We also thank to the Secretaría de Ma-rina- Dirección General Adjunta de Oceano-grafía, 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 Ves-sel 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.

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Fecha de recepción: 8 de marzo de 2012 Fecha de aceptación: 30 de julio de 2012

METABOLIC SCALING REGULARITY IN AQUATIC ECOSYSTEMSSalcido-Guevara, L. A.1, F. Arreguín-Sánchez1,*, L. Palmeri2 & A. Barausse2

1Centro Interdisciplinario de Ciencias Marinas del IPN, Apartado Postal 592, La Paz, Baja California Sur, México 2 LASA, Dip. di Processi Chimici dell’Ingegneria, Universita di Padova via Marzolo 9, 35131 Padova, Italy. email: [email protected]

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 efficiencyRegularidad 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.

INTRODUCTIONMass and size of organisms are key at-

tributes associated to metabolism and conse-quently 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 or-ganisms with different life histories (Ernest et al., 2003; West & Brown, 2004; Brown et al., 2002). Such metabolic regularities are repre-sented 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 sca-ling factor between metabolic rate and indi-

vidual mass, where the quarter scaling, instead of 2/3 derived from size dimensions, is associ-ated to network constrains for energy transport and their assimilation within the living systems which are characterized by having a hierarchi-cal 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 pro-ducers 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).

14 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 METHODSThe information used comes from 98 tro-

phic 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 ex-ploited 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 accep-table 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 pro-duction/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 propor-tion 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 ecosys-tem 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 bio-mass 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 lon-gevity (Pauly & Christensen, 1993) reflecting attributes related to metabolism. For a given population, energy is gained through assimila-tion stored as biomass and removed by respi-

ration and biomass mortality (Allen, 1971). In a stable population mortality equals production, meaning sustained biomass through metabo-lism. 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.

In our case, the trophic level is estimated as:

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), be-tween TL’s was also considered since this pro-cess 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 trans-ferred by predation and export.

Correction of the exponentWe 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 βBP 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 ex-ponential rate of change of with TLi, mean-ing 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 (Jen-nings 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 β=0.75, while the ordinate is assumed normalization constant.

15METABOLIC SCALING REGULARITY

Distribution of β values for the 98 ecosys-tems (see Annex) is shown in figure 3A, with a mean of β=0.64 (standard deviation of d=0.19) significantly different to the expected 0.75 value (p<0.05). β<2/3 has been interpreted as that the network is not fully representing a real ecosys-tem (Bendoricchio & Palmeri, 2005); or that dif-ferences 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 (Jen-nings 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 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.

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).

BA


along living systems having the same efficiency (in circulatory system it is expressed as main-tenance 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 obtain-ing a new set of vs. TLi for 95 ecosys-tems (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; specifi-cally for latitudinal changes. Figure 1 shows ecosystems locations, and areas drawn indi-cate 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 (Garlas-chelli et al., 2003) our results confirm the hy-pothesis that ecosystems metabolism follows the 3/4-power law, transfer efficiency being a key process.

Considering the quantitative analysis, or-dinary least squares regression assumes that

Figure 3. Slope distribution of log (B/P) versus TL for ecosystem models showing a normal-type distribution with (A) a modal value β =0.64 and δ=0.19, (B) modal value β0=0.726 and δ =0.25 after TE correction, both solved by a least squares algorithm, (C) a modal value of β0=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).

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 β0=0.75. C.I. is the confidence interval of the β0 and r the coefficient of correlation.

Region β0 βTE+/-95%

C.I. r1 0.6786 -0.0016 0.0052 0.152 0.7763 -0.0043 0.0072 0.273 1.2897 -0.0083 0.0253 0.214 0.9550 -0.0083 0.0154 0.365 0.8250 -0.0082 0.0243 0.186 0.6495 -0.0031 0.0038 0.35


error exists only in the dependent variable, re-sulting 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 alter-natively 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 vari-ables are measured with error. Results indi-cate 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 regular-ity 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 con-cept that complex living systems also follow the 3/4-metabolism scaling rule as a global regular-ity (West & Brown, 2005; Brown et al., 2007; Banavar et al., 2010).

ACKNOWLEDGMENTSAuthors thank Luis Capurro, Steve Mack-

inson and Daniel Pauly for their valuable com-ments and suggestions to an early versions of this manuscript. Authors also thank partial sup-port through projects CONACyT (SEP-CONA-CYT 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.

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C

anad

a-6

348

.5C

ontin

enta

l she

lf32

1 (1

)0.

5911

-0.0

183

0.60

190.

575

(15)

Sea

gras

s in

St.

Mar

ks, U

nite

d S

tate

s-8

4.5

30B

ay49

5 (1

)0.

2889

-0.2

218

0.35

30.

686

(16)

Bah

ia A

scen

cion

, Mex

ico

-87.

519

.75

Bay

192

(1)

0.76

3-0

.087

90.

830.

853

(17)

Cel

estu

n M

angr

ove,

Mex

ico

-90.

2520

.75

Coa

stal

lago

on19

2 (1

)0.

4079

-0.1

576

0.47

220.

663

(18)

Term

inos

Lag

oon,

Mex

ico

-91.

1667

18.3

333

Coa

stal

lago

on16

2 (1

)0.

7912

0.09

490.

8663

1.04

7(1

9)Lo

oe K

ey N

atio

nal M

arin

e S

anct

uary

, Uni

ted

Sta

tes

-81.

424

.533

3C

oral

reef

202

(1)

0.44

67-0

.196

90.

5347

0.72

1(2

0)C

oral

Ree

f Mex

ican

Car

ibbe

an-8

621

Cor

al re

ef18

2 (1

)0.

4518

-0.2

789

0.57

780.

562

(21)

Lake

Ont

ario

, Can

ada

-78.

543

.5La

ke14

1 (1

)0.

6086

-0.0

626

0.64

670.

752

(22)

Upw

ellin

g G

ulf o

f Sal

aman

ca,

Col

ombi

a-7

4.5

11.0

833

Con

tinen

tal s

helf

182

(1)

0.60

060.

0441

0.62

710.

637

(23)

Wea

t Gre

enla

nd-5

564

Con

tinen

tal s

helf

121

(1)

0.50

340.

0797

0.54

350.

657

(24)

Cam

pech

e S

ound

, Mex

ico

-91.

520

Con

tinen

tal s

helf

191

(1)

0.64

69-0

.079

60.

6984

0.73

6(2

5)Te

rmin

os L

agoo

n, M

exic

o-9

1.5

18.5

Con

tinen

tal s

helf

202

(1)

0.86

130.

0245

0.88

241.

047

(26)

Man

ding

a La

goon

, Mex

ico

-96

19C

oast

al la

goon

201

(1)

0.85

23-0

.516

51.

2925

0.48

1(2

7)Ta

mpa

mac

hoco

Lag

oon,

Mex

ico

-97.

521

Coa

stal

lago

on23

2 (1

)0.

4242

-0.1

662

0.49

470.

484

(28)

Cel

estu

n La

goon

, Mex

ico

-90.

521

Coa

stal

lago

on16

2 (1

)0.

6187

0.01

950.

6307

0.80

8(2

9)


Eco

syst

em n

ame

Long

itude

Latit

ude

Type

of e

cosy

stem

Num

ber o

f fu

nctio

nal

grou

ps

Num

ber o

f P

P (in

clui

ding

de

tritu

s)βP

BβT

Eβ0

β0,R

MA

Ref

eren

ce

Reg

ion

IIIIc

elan

d 19

50-1

162

Con

tinen

tal s

helf

242

(1)

0.80

8-0

.087

60.

8788

0.77

7(3

0)S

eine

Est

uary

, Fra

nce

0.16

6749

.441

7C

oast

al la

goon

152

(1)

0.54

73-0

.217

20.

6662

0.82

9(3

1)La

goon

of V

enic

e, It

aly

12.5

45.5

Coa

stal

lago

on16

2 (1

)0.

5443

-0.1

148

0.60

680.

836

(32)

Giro

nde

Est

uary

, Fra

nce

045

Coa

stal

lago

on18

2 (1

)0.

9351

0.02

230.

956

1.50

2(3

3)E

tang

de

Thau

, Fra

nce

3.5

43.5

Coa

stal

lago

on11

2 (1

)0.

4755

0.15

670.

550.

777

(34)

Orb

etel

lo L

agoo

n, It

aly

10.5

43C

oast

al la

goon

122

(1)

0.64

86-0

.147

30.

7442

0.69

3(3

5)G

aron

ne R

iver

, Fra

nce

1.5

44R

iver

102

(1)

0.81

97-0

.851

61.

5178

0.09

3(3

6)La

ke A

ydat

, Fra

nce

645

.5La

ke11

2 (1

)0.

787

0.04

730.

8242

0.66

9(3

7)R

ia F

orm

osa

lago

onal

sys

tem

, P

ortu

gal

-7.8

37.0

333

Res

ervo

ir14

1 (1

)1.

2186

-0.0

686

1.30

220.

894

(38)

Bal

tic S

ea20

60O

cean

ic16

2 (1

)0.

782

-0.1

419

0.89

30.

816

(39)

Reg

ion

IVLa

ke K

inne

ret,

Isra

el35

.533

Lake

142

(1)

0.58

5-0

.266

70.

741

1.00

8(4

0)La

ke T

urka

na 1

973,

Ken

ya36

.54.

5La

ke8

1 (1

)0.

7669

-0.2

898

0.98

920.

643

(41)

Lake

Tur

kana

198

7, K

enya

36.5

4.5

Lake

81

(1)

0.76

75-0

.322

41.

015

0.60

4(4

1)La

ke G

eorg

e, U

gand

a30

.20

Lake

142

(1)

0.67

390.

0406

0.70

120.

958

(42)

Lake

Vic

toria

, Ken

ya34

.5-1

Lake

162

(1)

0.68

89-0

.166

0.80

330.

782

(43)

Lake

Tan

gany

ica,

Afri

ca30

-7La

ke7

1 (1

)0.

8654

-0.0

280.

8896

0.84

6(4

4)La

ke K

arib

a, Z

imba

bwe

29-1

6.5

Lake

103

(1)

0.66

69-0

.218

80.

8128

0.91

7(4

5)La

ke M

alaw

i35

-9.5

Lake

91

(1)

1.16

51-0

.511

91.

7615

0.65

8(4

6)S

ri La

nkan

Res

ervo

ir, S

ri La

nka

35.3

333

10.7

5R

eser

voir

174

(1)

0.65

170.

1129

0.72

531.

267

(47)

Reg

ion

VB

rune

i Dar

ussa

lam

, Phi

lippi

nes

114

5C

ontin

enta

l she

lf13

1 (1

)0.

6865

-0.1

483

0.78

830.

732

(48)

Coa

st o

f Sar

awak

, Mal

aysi

a11

2.5

4.83

33C

ontin

enta

l she

lf29

2 (1

)0.

6245

-0.0

914

0.68

160.

741

(49)

Coa

st o

f Sab

ah, M

alay

sia

112.

54.

8333

Con

tinen

tal s

helf

292

(1)

0.54

32-0

.065

90.

579

0.65

8(4

9)K

uosh

eng

Bay

, Tai

wan

121.

6667

25.2

167

Bay

172

(1)

0.27

96-0

.116

80.

3123

1.13

8(5

0)S

an M

igue

l Bay

, Phi

lippi

nes

123

14B

ay16

1 (1

)0.

6384

0.03

610.

6615

0.75

5(5

1)S

an P

edro

Bay

, Phi

lippi

nes

125

11.0

917

Bay

162

(1)

0.37

980.

1122

0.42

240.

546

(52)

Bol

inao

Cor

al R

eef,

Phi

lippi

nes

119.

9167

16.4

167

Cor

al re

ef26

3 (1

)0.

2825

0.02

420.

2893

0.61

4(5

3)La

guna

de

Bay

182

0, P

hilip

pine

s12

1.5

14.5

Lake

302

(1)

0.86

66-0

.129

70.

979

0.65

2(5

4)La

guna

de

Bay

192

0, P

hilip

pine

s12

1.5

14.5

Lake

262

(1)

0.86

940.

1759

1.02

230.

874

(54)

Lagu

na d

e B

ay 1

950,

Phi

lippi

nes

121.

514

.5La

ke21

2 (1

)0.

8308

0.01

360.

8421

0.71

9(5

4)La

guna

de

Bay

196

8, P

hilip

pine

s12

1.5

14.5

Lake

162

(1)

0.67

890.

1975

0.81

30.

548

(54)

Lagu

na d

e B

ay 1

980,

Phi

lippi

nes

121.

514

.5La

ke17

2 (1

)0.

8196

0.20

240.

9855

0.76

3(5

4)La

guna

de

Bay

199

0, P

hilip

pine

s12

1.5

14.5

Lake

202

(1)

0.75

230.

2787

0.96

20.

801

(54)

Reg

ion

VI

Bru

nei D

arus

sala

m, P

hilip

pine

s11

45

Con

tinen

tal s

helf

131

(1)

0.68

65-0

.148

30.

7883

0.73

2(4

8)C

oast

of S

araw

ak, M

alay

sia

112.

54.

8333

Con

tinen

tal s

helf

292

(1)

0.62

45-0

.091

40.

6816

0.74

1(4

9)C

oast

of S

abah

, Mal

aysi

a11

2.5

4.83

33C

ontin

enta

l she

lf29

2 (1

)0.

5432

-0.0

659

0.57

90.

658

(49)

Pen

insu

la M

alay

sia,

Mal

aysi

a98

1C

ontin

enta

l she

lf15

1 (1

)0.

4885

0.02

570.

5011

0.62

(55)

Nor

th C

oast

of C

entra

l Jav

a,

Indo

nesi

a10

9-6

.5C

ontin

enta

l she

lf27

2 (1

)0.

4502

0.06

630.

4801

0.96

1(5

6)K

uosh

eng

Bay

, Tai

wan

121.

6667

25.2

167

Bay

172

(1)

0.27

96-0

.116

80.

3123

1.13

8(5

0)S

an M

igue

l Bay

, Phi

lippi

nes

123

14B

ay16

1 (1

)0.

6384

0.03

610.

6615

0.75

5(5

1)S

an P

edro

Bay

, Phi

lippi

nes

125

11.0

917

Bay

162

(1)

0.37

980.

1122

0.42

240.

546

(52)

Boh

ai S

ea, C

hina

120

39B

ay13

1 (1

)0.

5968

-0.0

097

0.60

260.

626

(57)

Ann

ex. C

ontin

ued.


Eco

syst

em n

ame

Long

itude

Latit

ude

Type

of e

cosy

stem

Num

ber o

f fu

nctio

nal

grou

ps

Num

ber o

f P

P (in

clui

ding

de

tritu

s)βP

BβT

Eβ0

β0,R

MA

Ref

eren

ce

Bay

of B

enga

l, B

angl

ades

h91

21B

ay15

1 (1

)0.

6806

0.19

660.

8144

0.53

3(5

8)B

olin

ao C

oral

Ree

f, P

hilip

pine

s11

9.91

6716

.416

7C

oral

reef

263

(1)

0.28

250.

0242

0.28

930.

614

(53)

Nor

ther

n G

reat

B

arrie

r R

eef,

Aus

tralia

150

-16

Cor

al re

ef25

2 (1

)0.

6528

-0.1

330.

7397

0.91

3(5

9)

Cen

tral

Gre

at

Bar

rier

Ree

f, A

ustra

lia14

7-1

8C

oral

reef

252

(1)

0.68

69-0

.131

0.77

710.

899

(60)

Uve

a A

toll

Loya

lty I

slan

ds,

New

C

aled

onia

166.

5-2

0.5

Cor

al re

ef25

3 (2

)0.

7128

-0.1

020.

7853

0.74

3(6

1)

Cen

tral P

acifi

c O

cean

170

20O

cean

ic26

1 (1

)0.

6399

-0.0

207

0.65

320.

7(6

2)S

uban

tarc

tic w

ater

Pla

teau

, N

ew

Zela

nd17

0-5

0O

cean

ic19

1 (2

)0.

7164

-0.1

030.

7902

0.70

5(6

3)

Lagu

na d

e B

ay 1

990,

Phi

lippi

nes

121.

514

.5La

ke20

2 (1

)0.

7523

0.27

870.

962

0.80

1(5

4)M

odel

s us

ed fo

r B

P vs

TL

but n

ot

for l

atitu

dina

l ana

lysi

sC

entra

l Chi

le 1

992,

Chi

le-7

3-3

3C

ontin

enta

l she

lf21

1 (1

)0.

6288

-0.1

650.

7326

0.60

7(6

4)C

entra

l Chi

le 1

998,

Chi

le-7

3-3

3C

ontin

enta

l she

lf21

1 (1

)0.

5728

-0.1

830.

6778

0.70

1(6

4)Ic

elan

d’s

fishe

ries,

Icel

and

-25

62.5

Con

tinen

tal s

helf

211

(1)

0.98

18-0

.147

1.12

61.

009

(65)

Sou

th

Ork

neys

/Geo

rgia

, B

ritis

h A

ntar

ctic

Ter

ritor

y-3

4-5

0C

ontin

enta

l she

lf30

1 (1

)0.

7456

-0.1

310.

8436

0.68

2(6

6)

Nor

ther

n B

engu

ela,

Nam

ibia

12-2

2C

ontin

enta

l she

lf24

1 (2

)0.

0269

-0.0

50.

0282

0.70

5(6

7)E

aste

rn B

erin

g S

ea, U

nite

d S

tate

s-1

63.5

52C

ontin

enta

l she

lf38

1 (3

)0.

7134

-0.1

940.

852

0.70

7(6

8)W

este

rn

Ber

ing

Sea

, U

nite

d S

tate

s-1

79.5

65C

ontin

enta

l she

lf36

1 (3

)0.

7002

-0.1

470.

8031

0.81

2(6

8)

Vene

zuel

a sh

elf,

Vene

zuel

a-6

210

Con

tinen

tal s

helf

162

(1)

0.71

41-0

.108

0.79

090.

732

(69)

Sou

ther

n B

razi

l, B

rzil

-51

-32.

5C

ontin

enta

l she

lf13

1 (1

)0.

7557

0.18

550.

8959

0.98

9(7

0)B

aren

ts S

ea 1

990

4080

Con

tinen

tal s

helf

412

(3)

0.66

9-0

.138

0.76

130.

813

(71)

Bar

ents

Sea

199

540

80C

ontin

enta

l she

lf41

2 (3

)0.

672

-0.1

190.

752

0.78

8(7

1)S

outh

wes

t coa

st o

f Ind

ia, I

ndia

7513

Con

tinen

tal s

helf

111

(1)

0.61

010.

2447

0.75

940.

815

(72)

Tong

o B

ay, C

hile

-71.

5-3

0.24

17B

ay17

2 (1

)0.

606

0.00

740.

6105

0.9

(73)

Bay

of S

omm

e, F

ranc

e1.

5550

.233

3B

ay9

2 (1

)0.

7796

--

-(7

4)M

aput

o ba

y, M

ozam

biqu

e33

-26

Bay

102

(1)

0.73

97-0

.275

0.94

310.

719

(75)

San

dy

Bar

rier

Lago

on

Chi

ku,

Taiw

an12

4.06

6723

.133

3C

oast

al la

goon

132

(1)

0.90

720.

1296

1.02

471.

491

(78)

Sak

umo

Lago

on, G

hana

0.03

335.

6167

Coa

stal

lago

on13

1 (1

)0.

8797

--

-(7

6)M

angr

ove

in

Cel

estu

n La

goon

, M

exic

o-9

0.25

20.7

5C

oast

al la

goon

192

(1)

0.40

59-0

.079

0.43

80.

545

(77

Ann

ex. C

ontin

ued.


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(2) Dalsgaard, J. & D. Pauly, 1997. FCRR, 5(2): 33. Available from: http://www.fisheries.ubc.ca/publications/preliminary-mass-bal-ance-model-prince-william-sound-alaska-pre-spill-period-1980-1989 [Accessed 1 February 2012]

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(6) Salcido-Guevara, L.A., 2006. M.Sc. thesis, CICIMAR-IPN., 83 Available from: http://www.biblioteca.cicimar.ipn.mx/oacis/tesis-desplegardetalles.php?id=422 [Accessed 1 February 2012]

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Fecha de recepción: 9 de mayo de 2012 Fecha de aceptación: 5 de julio de 2012

THE POTENTIAL EFFECT OF NITROGEN REMOVAL PROCESSES ON THE d15N FROM DIFFERENT TAXA IN THE MEXICAN SUBTROPI-

CAL NORTH EASTERN PACIFICCamalich, J.1*, A. Sánchez1, S. Aguíñiga1 & E. F. Balart2

1 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.

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 (d15N) increases in relation to trophic levels but little is known about the transfer of this d15N signal from the dissolved fraction to higher trophic levels in oceanic regions with low oxygen. The objectives of this study are: 1) to report d15N 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 d15N 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 d15N enriched in 15N through the trophic web up to top predators. The d15N 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 d15N signal reflects denitrification and this signal is transferred up though the food web.

Keywords: Subtropical north eastern Pacific, nitrogen cycle, d15N, oxygen minimum zone.Efecto potencial del proceso de remoción de nitrógeno sobre el d15N de distintos

taxa en el Pacífico noreste mexicano subtropicalRESUMEN. 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 (d15N) 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 d15N 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 d15N 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 d15N enriquecido en 15N a través de la red trófica hasta depredadores tope. El d15N 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 d15N refleja desnitrificación y esta señal es transferida a lo largo de la cadena trófica.

Palabras clave: Pacifico nororiental subtropical, ciclo del nitrógeno, d15N, 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.

INTRODUCTIONUpwelling areas, where nutrient rich water

is transferred from the deep ocean to the pro-ductive 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. How-ever, in some areas a combination of high pro-ductivity and poor water exchange can create large areas in the water column with very low oxygen concentrations (0.5 ml/l) called oxy-gen minimum zones (OMZ, Levin et al., 2002). Within these OMZ, processes take place which transfer nitrogen, one of the most important nu-trients in the ocean, to a form which cannot be used by phytoplankton and thus result in a loss of biologically available nitrogen. The major ni-

trogen removal processes behind this are deni-trification, in which heterotrophic bacteria con-vert nitrate (NO3

-) to dinitrogen gas (N2), and anaerobic ammonium oxidation (anammox), where microbes use ammonium (NH4

+) and ni-trite (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 es-timated that as much as 20 - 40% (or approxi-mately 200 x106 ton/year) of the oceanic nitro-gen 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 sub-stantial expansion of OMZ is predicted to occur (Stramma et al., 2008). Another emerging pro-

28 CAMALICH et al.

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). Fur-thermore, oxygen minimum zones are inhospi-table 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 addi-tion 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 iso-topic composition of nitrogen (d15N) to trace nitrogen removal processes. Water column denitrification in the OMZ and the incorpora-tion of NO3

-by phytoplankton in the ocean sur-face leads to an increase in nitrate d15N. 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 d15N signal of NO3

-from the deep water to the surface. In addition, a significant difference between the d15N 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 d15N sig-nal 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 d15N 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 d15N 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 d15N. Since this signal is transferred trough the food web, our hypothesis is that higher trophic levels including

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).

200

Norgánico

Upper OMZ

Anammox

Assim.

Remin.

DNRA

Nitrate

reduction

NO2-

NO3- NH4

+ N2

NO2-

Norg

400

Depth

(m)

0

0 2

Nitrification

N 2

fixa tio n Lower OMZ

Upper OMZ – BM

oceanic region

[O ] ml/l2

29EFFECT OF NITROGEN REMOVAL PROCESSES ON d15N

top predators are considerably more enriched in 15N than similar taxa living in regions were the d15N at the base of the food web is lower.

MATERIAL AND METHODSSamples of water, sediments, phytoplank-

ton, zooplankton, bentho-pelagic crustaceans and demersal fishes were collected on board the research vessel BIP XII during four cam-paigns (March and November, 2006 and 2007) at the oceanic region in front of the Bahía Mag-dalena-Almejas lagoon complex (Fig. 2). Phy-toplankton and zooplankton were collected si-multaneously 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 pa- trolling 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 sta-tions.

Stable isotope analysisNitrogen stable isotopes from water sam-

ples were analyzed following the ammonia diffusion method from by Sigman et al. (1997) at the Facultad de Ciencias del Mar y Lim-nologia (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 environ-ment (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

30 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 freeze-dried and packed into tin capsules. The analy-sis reproducibility was 0.1‰ for δ15N (n = 19, UC Davis internal standard). The highest stan-dard deviation from duplicates was 0.3‰.

Literature data comparisonWe used the concept of N* proposed by

Gruber and Sarmiento (1997) to distinguish be-tween 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 be-hind 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 fixa-tion and searched the literature for species of similar taxa to those collected at the northeast-ern subtropical Pacific to use in a comparison of δ15N transfer in N-fixing and N-removing en-vironments.

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 cya-nobacteria blooms constantly occur (e.g. Zehr & Ward, 2002) reveal N fixation (Carpenter & Capone, 2008)

RESULTSOxygen profiles

The oxygen profiles constructed for the studied area show a fast reduction in O2-con-centration 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 isotopesThe analysis of d15N-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 comparisonNitrogen stable isotope data (d15N) 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 Hob-son 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 Atlan-tic Ocean and Caribbean to compare different levels of human impacts. The study of Bode et al. (2007) was conducted on the Iberian Atlan-tic 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 eco-logical descriptions, important values from fish species were found for this comparison. Pe-tursdottir et al. (2008) described trophic routes from benthic and pelagic crustaceans to meso-pelagic 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. Sigman et al. (1997) described the method for d15NO3

- analysis using samples from the Sargasso Sea, a region of the ocean commonly known for in-tense N2 fixation. The mean and standard de-viations of each component are summarized in Table 1.

DISCUSSIONIn the present study our purpose was to

highlight the utility of d15N as a tracer of N re-moval 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 biot-ic components from the studied region and the Atlantic Ocean shows the transfer of dissolved nitrogen, and its progressive enrichment, along the food web. The d15N-NO3

- found in this study were higher compared to those reported as av-


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 tropi-cal north Pacific OMZ (8‰ to 16‰). In addi-tion we found that the d15N 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 d15N sinking particles since the low oxygen enhance the preservation of surface organic matter (Altabet et al., 1999). Although the O2-concentration in the water col-umn in the area is potentially not low enough (~2 ml/l) for denitrification, the record of 15N-enriched particles in the sediments appear to confirm the presence of nitrogen removal pro-cesses 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 d15N in the Bahía Magdalena oceanic region fit into the values measured at the southern end of the Baja California peninsula reported by Lopez-Ibarra (2008) and Olson et al. (2010). In addi-tion, 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 li-ons) 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, prob-ably hunting one of its preferred prey species, Pleuroncodes planipes. .

In the case of higher trophic levels the aver-age d15N values showed a 15N enrichment com-pared 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 biogeochemi-cal 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) re-corded a change in the d15N signal correspond-ing to a change in N dynamics. As they found the highest d15N 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 cascad-ing effect in the d15N-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 Maza-tlán 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

Compartment N* d15N (‰) CitationGruber 2008 Mean ± S.D.NO3

- 3 5 Sigman et al., 1997

POM 3 - 4 5.6 ± 1.7 Bode et al., 2007; Corbisier et al., 2006

Crustaceans* 3 10 ± 0.5 Corbisier et al., 2006; Petursdottir et al., 2008

Cephalopods* 2 - 3 11 ± 1.3 Bode et al., 2007; Corbisier et al., 2006

Demersal species* 1 - 2 12.5 ± 0.1

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

Delphinus delphis 3 13.1 Bode et al., 2007Pusa hispida -1 17.5 Hobson et al., 2002

Table 1. Average values and standard deviations of d15N from different components in areas where nitrogen fixation is the dominating process.

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

32 CAMALICH et al.

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 Loc’h et al., 2008; Stowasser et al., 2009).

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


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 contribu-tion of denitrification and anammox to the en-richment of 15N in low oxygen areas and deter-mining the potential transfer of the δ15N signal from anammox processes throughout the food web is important in future studies.

ACKNOWLEDGEMENTSThis study was supported by the grants

SEP-CONACYT (project C01-46806, 2005-2008), SAGARPA-CONACYT (project 2003-02-019) and project EP2 of CIBNOR. We are grateful to the crew of the R/V BIP XII and Ar-turo Tecuapetla for their assistance during the field work. The first author is grateful to CONA-CyT and COFAA for the scholarships provided during his doctoral work. Thanks to Elisabeth Svensson for her help in improving the final manuscript.

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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: [email protected]

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 CaliforniaProliferación de Amphidinium carterae (Dinophyceae: Gymnodiniales) en Bahía

de La Paz, Golfo de CaliforniaRESUMEN. 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.

INTRODUCTIONMicroalgae blooms are frequent and peri-

odic throughout the year in Bahía de La Paz, at the southwestern part of the Gulf of Califor-nia. Harmful blooms cause negative impacts to marine fauna through poisoning, mechani-cal 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 underestima- ted because they are normally deformed or des- troyed by sampling nets, storage, and by tra-ditional preservation solutions used in routine phytoplankton sampling (Okolodkov & Gárate-Lizárraga, 2006; Gárate-Lizárraga et al., 2011).

Gymnodiniales are unarmored dinofla-gellates that lack cellulose plates, but have a membranous outer covering of small vesicles. Most of the studies of gymnodinioid dinofla-gellates 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 &

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 defi-nition was emended by Flø Jørgensen et al. (2004) as follows: Athecate benthic or endo-symbiotic dinoflagellates with minute irregular triangular- or crescent- shaped epicones. Epi-cone overlays anterior ventral part of hypocone. Epicone deflected to the left. Cells are dorso-ventrally flattened, with or without chloroplasts.

Members of Amphidinium are among the most abundant and diverse benthic dinoflagel-lates worldwide (Fukuyo, 1981; Dodge, 1982; Sampayo, 1985; Ismael et al., 1999; Hoppen-rath, 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 micro-

38 GÁRATE-LIZÁRRAGA

algae community present during this bloom is also described.

MATERIAL AND METHODSBahía 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 in-let (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 collect-ed at sampling station 1 (off PEMEX) in Bahía de La Paz (Fig. 1) December 15, 2011.Samples were fixed with Lugol´s solution. Identifica-tion and cell counts were made in 5 ml settling chambers under an inverted Carl Zeiss phase-contrast 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 mea-sured with a bucket thermometer (Kahlsico In-ternational Corp., El Cajon, CA, USA). Scien-tific names of microalgae species were updated using the algae data base (http://www.algae-base.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 DISCUSSIONA total of 107 microalgae taxa were identi-

fied: 56 were diatoms, 46 dinoflagellates, 2 sili-coflagellates, 1 raphydophyte, 1 cyanobacteria and 1 coccolithophorid. This survey revealed the presence of benthic diatoms and dinofla-gellates, 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; Gárate-Lizárraga et al., 2009a). The species list and abundance are summarized in Table 1. Micro-phytoplankton was numerically more important than nano-phytoplankton, and diatoms were the most important group followed by dinofla-gellates; in this last group Amphidinium cart�

erae was the most abundant. The abundance of A. carterae in three sam-

ples 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 Okolod-kov & Gárate-Lizárraga (2006). Only a few specimens were found in February 12, March 24, April 28 and May 24 of 2011, in the net phy-toplankton 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 chlo-roplast 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 surround-ed 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 ag-gregated (Figs. 7, 8), while in a few cases, 12 cells were aggregated (Fig. 9). Inside another mucilaginous membrane, four cells were joined (Fig. 10).

110.7 110.6 110.5 110.4 110.3

24.2

24.3

24.4

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

39PROLIFERATION 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 mem-brane and that binary fission takes place within a cyst or in freely-swimming forms. Fusion of A. carterae cells have been observed as men-tioned 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).

5 6 7

8 9 10

42 3


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 CDiatoms cells L−1 cells L−1 cells L−1

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


Microalgae species Sample A Sample B Sample CDiatoms cells L−1 cells L−1 cells L−1

Rhizosolenia setigera, Brightwell 1858 0 0 400Thalassionema nitzschioides (Grunow) Mereschkowsky, 1902 0 3000 1200Thalassiosira eccentrica (Ehrenberg) Cleve, 1904 800 1800 200Thalassiosira rotula Meunier, 1910 1200 800 800Thalassiosira subtilis (Ostenfeld) Gran, 1900 1600 1200 1400Stephanopyxis palmeriana (Greville) Grunow, 1884 0 1200 1600Total abundance of diatoms 214600 223000 169400DinoflagellatesActiniscus pentasterias (Ehrenberg) Ehrenberg, 1854 200 0 200Alexandrium tamiyavanichii Balech, 1994 800 200 400Amphidiniopsis hirsuta (Balech) J.D.Dodge, 1982 0 200 0Amphidiniopsis sp. 0 200 0Amphidinium carterae Hulburt, 1957 28200 42000 64800Amphidinium sphenoides WüIff, 1916 0 200 0Amylax buxus (Balech) J.D. Dodge, 1989 800 0 200Cochlodinium pulchelum Lebour, 1917 400 0 200Cochlodinium virescens Kofoid & Swezy, 1921 0 0 200Cochlodinium sp. 0 0 200Coolia monotis Meunier, 1919 400 200 0Dinophysis acuminata Claparède & Lachmann, 1859 0 1200 400Dinophysis caudata Saville-Kent, 1881 200 400 200Dinophysis tripos Gourret, 1883 0 0 200Dinophysis ovum Schütt, F.,1895 0 400 200Dissodinium pseudolunula E.V. Swift ex Elbrächter & Drebes, 1978 200 0 200Durinskia cf. baltica (Levander 1892) Carty et Cox, 1986 * * *Gonyaulax digitale (Pouchet) Kofoid, 1911 0 1200 1400Gymnodinium coeruleum Dogiel, 1906 200 0 0Gymnodinium gracile, Bergh 1881 0 200 400Gymnodinium instriatum Freudenthal & Lee, 1963 0 200 200Gyrodinium sp. 0 0 400Katodinium glaucum (Lebour) Loeblich III, 1965 200 400 1600Neoceratium azoricum (Cleve) F.Gómez, D.Moreira & P.López-Garcia, 2010 200 0 200Neoceratium dens (Ostenfeld & Schmidt) F.Gomez, D.Moreira & P.Lopez-Garcia, 2010 0 400 200Neoceratium fusus (Ehrenberg) F.Gomez, D.Moreira & P.Lopez-Garcia, 2010 0 400 0Neoceratium furca (Ehrenberg) F.Gomez, D.Moreira & P.López-García, 2010 200 0 200Ornithocercus magnificus Stein, 1883 200 0 200Phalacroma favus Kofoid & J.R.Michener, 1911 0 0 400Prorocentrum compressum (J.W.Bailey) Abé ex Dodge, 1975 800 0 1200Prorocentrum emarginatum Fukuyo, 1981 400 400 200Prorocentrum gracile Schütt, 1895 200 400 200Prorocentrum micans Ehrenberg, 1833 200 200 600Prorocentrum minimum var. triangulatum (Martin) Hulburt, 1965 0 400 0Prorocentrum rhathymum Loeblich, Sherley & Schmidt,1979 400 200 0Protoperidinium abei (Paulsen) Balech, 1974 200 200 0Protoperidinium compressum (Abé) Balech, 1974 1600 400 200Protoperidinium excentricum (Paulsen, 1907) Balech, 1974 400 0 200Protoperidinium oblongum (Aurivillius) Parke & Dodge, 1976 200 200 0Protoperidinium pentagonum (Gran) Balech, 1974 0 200 200Protoperidinium subinerme (Paulsen) Loeblich III, 1969 200 0 200Ptychodiscus noctiluca Stein, 1883 200 0 200

Table 1. Continued


At least 48 species of dinoflagellates form thin-walled cysts as part of their life cycle, as-sociated with very different conditions, both in culture and nature (Bravo et al., 2010). Pel-licle 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 spe-cies 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 consid-ered a benthic or epiphytic species, it makes daily upward migrations in the water column from the benthos (Kamykowski & Zentara,

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 prolif-erations of microalgae are common in shrimp ponds (Gárate-Lizárraga et al., 2009b).

Amphidinium carterae has been recog-nized 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 sev-eral invertebrates and is implicated as a caus-ative 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. Phar-macological effects on mice include muscle contraction in lower back area, increased res-piration, 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.

Microalgae speciesDinoflagellates cells L−1 cells L−1 cells L−1

Pyrocystis fusiformis var. fusiformis (Wyville-Thomson ex Haeckel) V. H. Blackmann, 1902

0 200 200

Pyrocystis noctiluca Murray ex Haeckel, 1890 400 200 0Pyrocystis robusta Kofoid, 1907 0 0 200Thecadinium sp. 200 0 0Total abundance of dinoflagellates 37600 50800 76200SilicoflagellatesOctactis octonaria (Ehrenberg) Hovasse, 1946 400 200 200Dictyocha fibula var. robusta Schrader &Murray, 1985 0 0 400RhaphydophytesChattonella marina var. ovata (Y. Hara & Chihara) Demura & Kawachi, 2009 0 0 200CyanobacteriaTrichodesmium erythraeum Ehrenberg ex Gomont, 1892 8200 4200 16800Total abundance of the other groups 8600 4400 17600Micro-phytoplankton 260800 278200 263200Nano-phytoplankton 312400 211200 245800Total phytoplankton abundance 573200 489400 509000

Table 1. Continued


Figures 11–26. 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).

11 12 13 14

15

19 20 21 22

23 2624 25

17 1816


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).

29 30

31 32 33

35 36 37 38

39 40 41

27 28

34

42


Figures 43–58. 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).

43

47 48 50

51 53

55 56

54

57 58

464544

52

49


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).

59 61 62

63 64 65 66

68 69 70

71 72 7473

60

67


Figures 75–90. 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).

75 76 77 78

79 81 82

83 84 86

87 88 9089

80

85


New recordsSeveral 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 speci-mens 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.

ACKNOWLEDGMENTSResearch projects were funded by Insti-

tuto Politécnico Nacional (SIP-20110281, SIP-20110590, 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 CO-FAA and EDI fellow.

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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 1Instituto 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: [email protected]

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 CJB-SL hacia la zona marina de pesca (ZMP) del Golfo de Tehuantepec. El RL, es el movimiento natural de post-larvas 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.

INTRODUCTIONIn 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) (Rey-na-Cabrera & Ramos-Cruz, 1998) (Cervantes-Hernández, 2008) (Fig. 1). The marine fishing zone 90 has a total area of 8085 km2 of conti-nental platform and it is composed of five sub-sectors (Reyna-Cabrera & Ramos-Cruz, 1998). In the marine fishing zone 90, the ships oper-ate from five to 40 fathoms (i.e., 9.1 to 72.8 m)

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

52 CERVANTES-HERNÁNDEZ et al.

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

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 peri-ods of Farfantepenaeus californiensis (Holmes, 1900). In this work the author defined the Ma-rine Recruitment as the natural movement of ju-venile 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 de-fined 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 re-production periods of F. californiensis occur in the marine fishing zone 90, larvae shrimp must

increase, activating then lagoon recruitment period. The author associated massive repro-duction periods with maximum abundance of shrimp spawners close to and at sexual ma-turity 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.

The results obtained by Cervantes-Hernán-dez (2008), were used by Cervantes-Hernán-dez et al. (2008 a) to demonstrate, that the ma-rine 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 exploi-tation 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 Octo-ber to protect both recruitment periods.

The results published by Cervantes-Hernández 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 generat-ed. For this reason, in this work marine and la-goon recruitment periods were analyzed in the

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) “Patos-Solo Dios”; (5) “Carretas-Pereyra”; (6) “Chantuto-Panzacola”; (S.C.) Salina Cruz City.

53RECRUITMENT OF Litopenaeus vannamei

“Cabeza de Toro - La Joya-Buenavista” lagoon system (CJB-LS) from GT.

The results obtained in this work were com-pared with the results reported by Cervantes-Hernández (2008) to determine if both recruit-ment 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. Impor-tant 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 pe-riods. 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). Field-work 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 ana-lyzed at the Universidad del Mar, Puerto Ángel, Oaxaca, Mexico, under project 2IR1104.

Cohort’s analysisBhattacharya’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 dif-ference 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 sepa-rated from other cohorts using a negative lineal model. This negative lineal model is:

∆Ln (Nt) = a - b ∙ LT (1) According to Malcolm (2001), the param-

eters a and b of the function (1) were estimated using the minimum likelihood of log-normal dis-tribution (-Ln (a, b / Nt, LT)), this is:

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

-Ln(a, b/Nt, LT)=sum(Ln(SDƐ)+(Ln(2π)/2)+(Ɛ2/(2∙ SDƐ)) (2)

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


(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 us-

ing the computer software BOBP/MAG/4. The function (2) was resolved using computer soft-ware Analysis Matrix Population (Pop-Tools) and with support “Solver” an Excel tool. Solver was used with a precision at 0.000001 com-bined tangent, progressive and Newton algo-rithms.

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 X-axis and LM as Y-axis. This plot was used to de-velop a modal progression analysis according to Sparre and Venema (1995). In this analysis type, a modal progression line must be diago-nally 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 be-tween 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 indi-cated 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, fol-lowing 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 fort-night by fortnight until reaching the maximum value of LM in each modal progression lines ob-tained. 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 (be-tween 2001-04-24 and 2002-03-28) were sepa-rated into two periods on the aforementioned plot. These periods were the same as those used by Cervantes-Hernández (2008) to de-scribe marine and lagoon recruitment periods in the marine fishing zone 90. According to this author, the first period represented marine re-cruitment and was delimited from April to Oc-tober (during rainy season). The second period represented lagoon recruitment and was delim-ited 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 co-hort reached the maximum LM value in a modal progression line, this line would continue grow-ing within the CJB-LS, but the next shrimp co-hort would not be able to be observed inside the lagoon system, because it migrated toward the marine fishing zone 90, then marine recruit-ment 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 in-terior CJB-LS. The presence of younger shrimp within the CJB-LS suggests that lagoon recruit-ment had begun.

RESULTSCohort’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 co-horts 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-


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 (dur-ing “Tehuanos” season) and 13 modal progres-sion 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 begin-ning to emigrate from the interior the CJB-LS towards the marine fishing zone 90 (Fig. 3), but

a greater number of shrimp cohorts were ob-served 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 through-out 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 sec-ond period, especially in the last days of Octo-ber 2001(Fig. 3).

The age at which L. vannamei began to em-igrate towards the marine fishing zone 90 was recorded between 4.5 and five months old (Fig. 3). We named these ages “recruitment age”.

DISCUSSIONKnowledge of the annual abundance varia-

tion 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 recruit-ment and spawning periods in natural popula-tions (Watson et al., 1996).

The INP (2004) described the massive egg-laying 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-

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.


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 au-thor reported an increase in the spawners num-ber of this shrimp. In the CJB-LS, 25 day old white shrimp cohorts were observed only dur-ing 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 post-larvae 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 re-production 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 ob-served 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) de-scribed some oceanographic conditions of the GT between 1989 and 1998. On average, chlo-rophyll a concentration was lower during ma-rine 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 egg-laying 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 abun-dance of recruits and the lower percentage of egg-laying of mature females in phase IV oc-curred), larval survival was lower because food availability diminished according to the low lev-els 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 au-thor reported an increase in the juvenile num-ber of this species. For L. vannamei from the CJB-LS, a higher number of white shrimp co-horts between 4.5 and five months of age were observed within the CJB-LS, especially during

June and July. This fact was interpreted as evi-dence that those shrimp cohorts began to mi-grate 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 re-corded between June and September 2001 (337-397 mm). During the “Tehuanos” season lower levels of pluvial precipitation were re-corded 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 precipita-tion together with fluvial unloading in lagoon systems stimulate the emigration of juvenile shrimp due to diminishing salinity (chemical stimulus). Another associated factor is an in-crease of the water turbidity which diminishes the natural mortality rate due to depredation when shrimp leave lagoon systems.

Our results indicate that between the CJB-LS and the marine fishing zone 90, marine re-cruitment period for L. vannamei was delimited from April 2001 to mid October 2001 and re-cruitment 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 Cervantes-Hernández 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 sys-tem changes, see Cervantes-Hernández et al. (2008 a).

ACKNOWLEDGMENTSWe 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


Berumen (UMAR), Saul J. Serrano Guzmán (UMAR) and anonymous reviewers for their valuable time and comments regarding this ar-ticle.

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Cervantes-Hernández, P., M. I. Gallardo-Beru-men, S. Ramos-Cruz, M. A. Gómez-Ponce & A. Gracia. 2008 a. Análisis de las tem-poradas 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 cali-forniensis (Holmes, 1900) en el Golfo de Tehuantepec. Hidrobiológica, 18(3): 215-226.

Chávez, E. A. 1979. Diagnosis de la pesquería del camarón del Golfo de Tehuantepec, Pa-cífico Sur Occidental de México. An. Centro de Cienc. Mar y Limnol. Univ. Nal. Autón. México, 6(2): 7-14.

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

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

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].

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Fecha de recepción: 19 de enero de 2012 Fecha de aceptación: 9 de mayo de 2012

ADDITIONAL DATA RELATED TO THE DISTRIBUTION OF VENTRALLY SCLEROTIZED SPECIES OF Lepidophthalmus HOLMES, 1904 (DECAPODA: AXIIDEA, CALLIANASSIDAE,

CHALLICHIRINAE) FROM THE TROPICAL EASTERN PACIFICHendrickx, M. E.1 & J. López 2

1Laboratorio 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: [email protected]

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.

INTRODUCTIONA recent review of the “Thalassinidean”

families and genera from the American conti-nent 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 restruc-tured in order to follow arguments in favor of di-viding this paraphyletic group into two separate infraorders: Gebiidea and Axiidea. All details related to this are available in previously pub-lished literature (see Sakai & de Saint Laurent, 1989; Lemaitre & Ramos, 1992; Felder & Man-ning 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 Cal-lianassidae 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 east-ern 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

withdrew L. eiseni Holmes, 1904 from the syn-onymy of L. bocourti (A. Milne-Edwards, 1870) (originally described as Callianassa bocourti). After reviewing numerous specimens from southern Mexico to Panama, the type mate-rial 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 presence-absence of distolateral spines on the basis of pleopods 3-5, and the shape of the terminal ar-ticle 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 ma-terial belongs to the two “ventrally sclerotized” species of Lepidophthalmus from the eastern Pacific. This material is reported herein.

MATERIAL AND METHODSAll 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 formal-dehyde (5-10%), washed after a few days and preserved with 70% ethanol. Illustrations were made with the help of a camera lucida mounted

60 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.

RESULTSLepidophthalmus 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. Hen-drickx) ) (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, in-tertidal 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.

61Lepidophthalmus FROM THE TROPICAL EASTERN PACIFIC

One male (CL/TL/MCL: 18.0/76.0/46.5 mm), SW part of Caimanero lagoon, south of Mazat-lán, 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, Navo-lato, 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 (EMU-9613).

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 mod-erately 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 in-definite pattern (Fig. 2 E), while in L. eiseni this pattern is much more regular and elaborated (see infra).

According to Felder (2003: 434), the ma-terial 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 unde-scribed species (maybe the same species) lacking these sclerotized structures altogether.

Distribution range.- According to Felder (2003), L. bocourti is known with certainty from

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.

62 HENDRICKX & LÓPEZ.

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-DLepidophtahlmus 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), Bar-ra 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 separat-ed 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 abdomi-nal 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 ante-rior 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 posterolat-eral 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

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.

63Lepidophthalmus 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 posi-tive records in Guatemala, Nicaragua, and El Salvador. The type locality in “San José del Cabo”, Mexico, is uncertain.

ACKNOWLEDGEMENTSThe 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. Va-lenzuela 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 lit-erature.

REFERENCESBott, R. Von. 1955. Dekapoden (Crustacea)

aus El Salvador. 2. Litorale Dekapoden, au-ber 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 mem-bers of Lepidophthalmus (Crustacea: De-capoda: 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 (De-capoda: 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 imperfect-ly known species of west American Crusta-cea. 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 de-scriptions 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 Phy-logeny of the Thalassinidea based on Nu-clear 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 Callia-nassidae, with keys to subfamilies, genera and species, and the description of new taxa (Crustacea: Decapoda: Thalassini-dea). 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 subfam-ily, eleven new genera and two new spe-cies. 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: Callianas-sidae). J. Crust. Biol., 20 (special number): 157-169.


Fecha de recepción: 8 de febrero de 2012 Fecha de aceptación: 18 de abril de 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: [email protected]

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 (Ponce-Díaz et al., 2003). Therefore, species that live in highly variable environments must be adap-ted to different thermal conditions (Lluch-Belda et al., 2000). The Baja California peninsula exhibits strong environmental fluctuations vary-ing 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 tempera-ture variations affect the structure and function of marine ecosystems it is essential to analyze each one of the timescales for variation (cir-cadian, fortnightly, monthly, seasonal, interan-nual, and longer term), and how they behave in different ecosystems (coastal lagoons, es-tuaries, shelf seas, open ocean, etc). Existing databases of sea surface temperature like Had-ISST1 (Rayner et al., 2003), OISST.v2 (Reyn-olds et al., 2002) and ERSST.v3 (Smith et al., 2008) are freely available, however, those da-tabases do not have enough temporal resolu-tion to detect large daily temperature fluctua-tions (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 spe-cies for particular aquaculture sites.

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 govern-mental and non-governmental sources, gener-ating valuable data, albeit with different times-cales. Recently, this data has been integrated into an online database with the purpose of:1) Making data records available to the scien-tific community and farmers for scientific stud-ies 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 avail-able tool for scientists and aquaculture farmers. 3) Increasing and continuing the monitoring ef-fort by inviting scientists and other individuals whose activities are connected with coastal ar-eas, to participate by deploying instruments at these sites.

The authors hope that this policy of coop-eration 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 differ-ent locations along the Pacific coast of Baja California Sur and inside the Gulf of California (Fig. 1) using digital temperature loggers (Op-tic 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

66 SICARD et al.

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 Igna-cio (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 moni-tored is from 2006 to 2010 (Fig. 2b).

Table 1 shows the basic statistic descrip-tors (minimum, maximum, average and stan-

Region Name Code Minimum Maximum Mean SD N WLaguna Manuelas 1 Laguna Manuela (Boca) LMB 13.19 28.65 18.93 2.62 28.1834 -114.0608

2 Laguna Manuela (Camas de cultivo) LMC 10.71 30.27 19.78 2.97 28.1371 -114.0719

3 Laguna Manuela (Fondo)* LMF 10.74 36.3 21.56 4.23 28.1311 -114.0680Laguna Guerrero Negro 4 Campo Chupa Lodo CCH 10.26 33.22 20.75 3.44 27.9946 -114.0716Laguna Ojo de Liebre 5 El Conchalito ECO 13.85 30.86 19.15 3.22 27.7763 -114.2781

6 La ventana LVE 14.71 25.51 18.81 2.78 27.7358 -114.26967 El Mariscal EMA 17.34 22.89 20.5 1.73 27.6800 -114.1579

Bahía Tortugas 8 El Rincón ERI 11.82 25.22 17.14 2.67 27.6629 -114.86569 Queen QUE 15.11 25.96 19.88 1.83 27.7779 -114.6362

10 Arvin ARV 13.28 23.13 17.15 2.02 27.6477 -114.8665Bahía Asunción 11 Isla Asunción* BAI 11.96 33.77 22.55 6.13 27.1462 -114.3767

12 El Rito BAE 12.25 22.99 16.94 2.64 27.1339 -114.2953La Bocana 13 La Bocana BOC 12.5 29.95 20.74 4.03 26.7862 -113.6868Punta Abreojos 14 Punta Abreojos PTA 15.28 29.35 22.12 3.27 26.8194 -113.4347Laguna San Ignacio 15 San Ignacio SIG 7.66 39.96 21.17 4.43 26.793 -113.1515

16 Sol Azul SAZ 14.33 36.62 22.19 3.89 26.7914 -113.1561Santo Domingo 17 Santo Domingo SDO 8.98 32.09 23.83 4.06 25.5655 -112.0731Estero San Buto 18 San Buto SBU 13.37 34.69 24.26 3.4 24.7746 -112.0477Bahía Magdalena 19 Bahía Magdalena 1(9.5m) BM1 13.08 28.75 19.18 3.74 24.658 -112.0673

20 Bahía Magdalena 2(11m) BM2 14.23 31.88 20.69 3.65 24.6319 -111.918921 Bahía Magdalena 3(14.7m) BM3 13.08 29.25 19.48 3.99 24.5504 -111.947922 Bahía Magdalena 4(17m) BM4 13.17 28.06 18.98 3.89 24.6452 -111.963423 Rancho Bueno 1 RB1 10.39 38.14 22.42 4.29 24.3738 -111.643024 Rancho Bueno 2 RB2 8.68 38.83 22.86 4.13 24.3748 -111.577325 Rancho Bueno 3 RB3 12.24 33.54 22.45 3.76 24.3500 -111.481126 El Remate ERE 16.31 31.58 23.01 3.35 24.3113 -111.4022

Bahía de La Paz 27 Punta Arenas PAR 18.04 30.56 25.7 2.65 24.0445 -109.825928 Mogote (18m) MO1 19.19 22.24 20.88 0.45 24.1839 -110.379729 Mogote (7m) MO2 19.95 23.29 21.61 0.62 24.1839 -110.379730 Canal de San Lorenzo SLO 18.53 25.9 21.07 1.27 24.3878 -110.321831 Punta Diablo PDI 15.19 32.98 22.82 3.18 24.3125 -110.336532 Rancho Rodríguez RRO 20.04 32.19 24.55 1.95 24.2019 -110.527033 San Gabriel SGA 19.67 29.5 24.19 1.77 24.4268 -110.369834 Isla Gallo(20m) IG1 19.95 21 20.43 0.2 24.4631 -110.386135 Isla Gallo(7m) IG2 20.33 21.09 20.71 0.21 24.4631 -110.386136 Isla Gaviota (22m) GA1 18.71 22.81 21.59 0.69 24.2892 -110.340637 Isla Gaviota (7m) GA2 18.9 23.97 21.69 0.65 24.2892 -110.340638 El Portugués** EPO 24.86 38.14 29.13 2.16 24.7476 -110.678239 Balandra BAL 12.3 39.5 25.13 3.77 24.3166 -110.321240 Enfermería ENF 16.99 37.05 26.19 4.28 24.2293 -110.319341 Zacatecas ZAC 9.57 35.65 22.72 4.11 24.1209 -110.4334

Bahía de Loreto 42 Candeleros CAN 17.91 30.29 22.95 3.77 25.7448 -111.227743 La Choya LCH 16.94 30.67 22.79 3.51 26.0449 -111.181644 Galeras GAL 17.62 31.02 23.96 4.05 25.7382 -111.044745 Puerto Escondido PES 18.33 33.22 24.35 3.66 25.8096 -111.3075

Sonora 46 Bahía Bacoherehuis BBA 18.62 35.12 27.74 3.91 26.5261 -109.153147 Bahía Kino BKI 13.88 33.63 24.13 5.28 28.7999 -111.9176

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.

67OPEN 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.

68 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 Califor-nia (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 re-cords (Table 1). The amplitude values indicate the distribution of registered daily temperature fluctuations for each location and month. Fig-ure 4 reports the frequency distributions of tem-perature 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 pref-erences 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 lo-cal dynamics (exchange rates with open ocean, local heating, depth) play a major role in shap-ing 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.

69OPEN SEA SURFACE TEMPERATURE DATABASE

www.leoa.org.mx/RAF), and stored by the re-cently created Observatorio de los Mares y Costas de México (contact [email protected]). The temperature data is freely available online as a KMZ file, which is a file type supported by the Google Earth®software program. This pro-vides a free and straightforward platform to ex-plore and visualize the information generated from all observation sites.

ACKNOWLEDGMENTSThis report is a product of the Laborato-

rio de Ecofisiología de Organismos Acuáticos (LEOA) and the Observatorio de los Mares y Costas de México. Funding was provided by the Project SEMARNAT-CIBNOR: Fortaleci-miento 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-

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.

70 SICARD et al.

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-Cabal-lero. 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. Lluch-Cota. 2003. Scales of interannual variability in the California Current system: Associ-ated physical mechanisms and likely eco-logical 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. Bautista-Romero & D. Lluch-Belda. 2003. Carac-terización 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 tem-perature, sea ice, and night marine air tem-perature 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. Lluch-Cota, C. Lodeiros, L. M. Roldán-Carrillo & R. Mendoza-Alfaro. 2006. Frequent moni-toring of temperature: an essential require-ment for site selection in bivalve aquacul-ture 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.

INSTRUCCIONES A LOS AUTORESCICIMAR Oceánides publica trabajos originales de investi-

v. gr., tópicos de: Biología y Ecología Marina, Geología Marina, Oceanografía Física y Química, así como Meteorología, Pesquerías y Acuicultura. Las contribuciones podrán ser: Artículos, informes in ex-tenso de investigaciones acerca de los temas propios de la revista. Notas, contribuciones originales de corta extensión que contengan resultados parciales o hallazgos que merez-can ser dados a conocer en el corto plazo. Todos ellos serán considerados siempre que su contenido tenga carácter teóri-co, técnico, o metodológico y no hayan sido sometidos si-multáneamente en ninguna otra revista. Si el manuscrito ya

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-licarán revisiones y ensayos que hagan aportaciones al de-sarrollo de una rama de la ciencia y artículos por invitación formal del Consejo Editorial. También, se aceptan réplicas a trabajos publicados en CICIMAR Oceánides. En todos se exigirá claridad y congruencia entre el título, el problema y su planteamiento, así como con la(s) hipótesis del estudio. CICIMAR Oceánidesa la trascendencia de una obra determinada. La revista está incluida en el sistema de resúmenes ASFA (Aquatic Sciences and Fisheries Abstracts), Ecological Abs-tracts, Oceanography Literature Review, BIOSIS (Zoological Record), Periódica y Thompson Master Journal list.Los trabajos deberán remitirse al Editor de CICIMAR-Oceánides por vía electrónica en formato Microsoft Word (doc) o Adobe Acrobat (pdf) incluyendo en un solo archivo el

serán arbitrados por pares de su especialidad; el autor po-drá sugerir revisores, proporcionando su correo electrónico,

rentemente internacionales de reconocido prestigio). Asimis-mo, se podrá solicitar el descarte de árbitros inadecuados

-tor devolverá a los autores, sin evaluarlos, los manuscritos que no caigan dentro del ámbito de CICIMAR Oceánides. Aquellos que no se adapten a los requerimientos de las presentes instrucciones serán también devueltos para una corrección previa a su evaluación. Se enviarán pruebas de imprenta (en formato PDF) a los autores, quienes serán re-sponsables de la corrección de errores y de devolverlas en un término de dos semanas desde su recepción. En caso contrario, el Consejo Editorial podrá efectuar la corrección o aplazar la publicación del trabajo.

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leyendas de tablas, notas a pie de página, etc.) en hoja tama-ño carta (letter). Todas las páginas deberán numerarse in-

pero excluyendo éstas. Salvo casos extraordinarios, el núme-ro total de páginas no superará las 40 (incluyendo tablas y

Se recomienda someter sus manuscritos en idioma Inglés, aunque también son aceptados aquellos en Español. Las notas serán publicadas en Inglés. Se recomienda que los artículos se dividan en: Título, Resumen, Introducción, Mate-rial y Métodos, Resultados, Discusión, Agradecimientos y Re- ferencias. Las palabras a imprimir en cursiva deberán sub-rayarsede organismos y símbolos matemáticos en el texto). Las me-

didas se expresaránen unidades SI, usando las abreviatu-ras de la International Standards Organization (ISO) La lo-

como E, W, N, S.El Título deberá presentarse tanto en Inglés como en Espa-

-vos o temáticos; se incluirá un título abreviado que no exceda de 40 caracteres. A continuación se indicarán el nombre, in-stitución y dirección del autor (incluyendo su E-mail) y coau-tores, diferenciando las instituciones de los participantes con números arábigos consecutivos.Se requerirá un Abstract y su versión en Español (máximo 300 palabras), donde incluirán en un sólo párrafo objetivos, resultados y conclusiones, mencionando lo esencial del nue-vo conocimiento aportado; sólo se aceptarán referencias bi-

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-bajo en bases de datos electrónicas. Las Tablas y Figuras, junto con sus leyendas, deberán pre-sentarse consecutivamente con numeración arábiga y en ho-jas aparte. Las leyendas deben ser breves y explicativas. Deberán evitarse repeticiones de información entre tablas y

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-te.En las Referencias rrespondencia entre las citas en el texto (incluidas las ta-

incluir en las Referencias trabajos publicados o “en prensa” (i.e -juntando copia de la carta de aceptación). Expresiones como “com. pers.”, “in litt.“, “datos no publ.”, etc., sólo serán permi-tidas en el texto, en donde se usará el sistema de citas por

indicarse mediante el apellido del autor, o autores si son dos, seguido del año de publicación separado por una coma; todo entre paréntesis. Si el nombre del autor forma parte de la re-dacción del escrito, sólo el año se pondrá entre paréntesis. Cuando sean más de dos autores se escribirá el apellido del

-tará por orden alfabético. Se tendrá en cuenta la cronología sólo cuando exista más de una referencia con idénticos au-tores. Las referencias deberán incluir el título completo y los números de las páginas. Las abreviaturas de revistas serán según la WORLDLIST OF SCIENTIFIC PERIODICALS. De-berán subrayarse (para cursivas) todas las abreviaturas de revistas y títulos de libros. CORRESPONDENCIA: Se dirigirá al Editor: Ave. IPN s/n, Col. Playa Palo de Sta. Rita, 23096, La Paz, B.C.S., al Apartado Postal 592, La Paz, B.C.S., México, o al email: [email protected].

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CICIMAR Oceánides Vol. 27 (2) 2012