CICIMAR Oceánides Vol. 24 (2) 2009 by CICIMAR Oceánides

DIRECTORIO INSTITUTO POLITÉCNICO NACIONAL JOSÉ ENRIQUE VILLA RIVERA Director General YOLOXÓCHITL BUSTAMANTE DÍEZ Secretario Académico LUIS HUMBERTO FABILA CASTILLO Secretario de Investigación y Posgrado

CENTRO INTERDISCIPLINARIO DE CIENCIAS MARINAS

RAFAEL CERVANTES DUARTE Director AGUSTÍN HERNÁNDEZ HERRERA Subdirector Académico y de Investigación PEDRO GONZÁLEZ RAMÍREZ Subdirector de Extensión y Apoyo Académico LETICIA REYES FAMANIA Subdirectora Administrativa

CONSEJO EDITORIAL

DAVID A. SIQUEIROS BELTRONES (Editor ) ALEJANDRO ÁLVAREZ ARELLANO FRANCISCO ARREGUÍN SÁNCHEZ DAVID AURIOLES GAMBOA JOSÉ LUIS CASTRO AGUIRRE ERNESTO A. CHÁVEZ ORTIZ JAIME GÓMEZ GUTIÉRREZ VÍCTOR M. GÓMEZ MUÑOZ SERGIO HERNÁNDEZ TRUJILLO OSCAR E. HOLGUÍN QUIÑÓNES DANIEL LLUCH BELDA GUSTAVO DE LA CRUZ AGÜERO

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CICIMAR Oceánides

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CICIMAR Oceánides, 2009

VOL. 24(2)

ISSN-1870-0713

CONTENIDO

Effect of diatom and dinoflagellate diets on egg production and ingestion rate of Centropages furcatus (Copepoda: Calanoida) from a subtropical bay (Bahía de La Paz, Gulf of California). BAND-SCHMIDT, C. J., R. PACHECO-CHÁVEZ, L. CARREÓN-PALAU, J. A. DEL ÁNGELRODRÍGUEZ & S. HERNÁNDEZ-TRUJILLO.

Estimation of Taylor's power law parameters a and b for tidal marsh macrobenthic species. FLYNN, M. N. & W. R. L. S. PEREIRA.

Variación de los índices morfofisiológicos de la almeja mano de león Nodipecten subnodosus (Sowerby, 1835) en Bahía de Los Ángeles, B. C., Golfo de California. YEE-DUARTE, J. A., B. P. CEBALLOS-VÁZQUEZ & M. ARELLANO-MARTÍNEZ.

a-Diversidad de diatomeas epilíticas del oasis de San Ignacio, Baja California Sur, México. LÓPEZ FUERTE, F. O.

101

ARTÍCULOS DE REVISIÓN Indicadores biológicos en el ambiente pelágico. JIMÉNEZ-ROSENBERG, S. P. A. & G. ACEVES-MEDINA. Codes of conduct and certification issues for shrimp farming: a review. NAEGEL, L. C. A. & I. FOGEL.

113 129

NOTAS Analysis of the vertical distribution of the abundance of small pelagic fish larvae in the Gulf of California using submarine videocameras. ACEVES-MEDINA, G., C.J. ROBINSON, R. PALOMARES-GARCÍA & J. GÓMEZ-GUTIÉRREZ.

153

Sea stars (Echinodermata:Asteroidea) in rocky reefs of Guadalupe Island, Northwest Mexico. REYES BONILLA, H., S. GONZÁLEZ ROMERO & A. MOHEDANO NAVARRETE.

161

First record of Ceratium dens (Dinophyceae) in the Gulf of California. GÁRATE-LIZÁRRAGA, I.

167

CICIMAR Oceánides, 24(2): 71-83 (2009)

EFFECT OF DIATOM AND DINOFLAGELLATE DIETS ON EGG PRODUCTION AND INGESTION RATE OF Centropages furcatus (COPEPODA: CALANOIDA) FROM A SUBTROPICAL BAY (BAHÍA DE LA PAZ, GULF OF CALIFORNIA) Band-Schmidt, C. J.1,a, R. Pacheco-Chávez1, L. Carreón-Palau2, J. A. Del Ángel-Rodríguez2 & S. Hernández-Trujillo1,a 1

Departamento de Plancton y Ecología Marina. Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Apdo. Postal 592, La Paz, B.C.S. 23000, Mexico. Tel.: +52-612-122-5344 / +52-612-123-0350, ext 82434 Fax: +52-612-122-5322. 2 Laboratorio de Biotecnología de Microalgas, Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Apdo. Postal 128, La Paz, B.C.S. 23000, Mexico. a EDI and COFAA recipients. email: cbands@ipn.mx. ABSTRACT. This study experimentally determined the role of local diatom and dinoflagellate diets and their fatty acid composition on the survival, ingestion, and egg production rates of the copepod Centropages furcatus from Bahía de La Paz. The fatty acid profiles of the diatoms Odontella longicruris and Chaetoceros sp., and of the dinoflagellates Scrippsiella sp., Gyrodinium sp., and Prorocentrum micans were determined. After incubating at 24 °C in darkness during 24 h, survival within all phytoplankton diets was > 90%. Dinoflagellate diets provided higher egg production (>25 eggs female-1 day-1) than diatom diets (<10 eggs female-1 day-1). No significant differences were observed in the ingestion rates when fed dinoflagellates or diatoms, which varied between 400 and 900 ng C copepod-1 h-1. Higher egg production with dinoflagellate diets suggests better food quality, which may be attributed to higher proportions of the fatty acids 18:4 (n-3) and 22:6 (n-3). These results suggest that when C. furcatus predominantly graze on dinoflagellates egg production will increase. Higher abundances of dinoflagellates in the La Paz bay could be coupled with higher egg production of the copepod C. furcatus.

Keywords: Centropages furcatus, egg production, fatty acids, Bahía de La Paz, phytoplankton. Efecto de dietas con diatomeas y dinoflagelados en la producción de huevos y tasas de ingestión de Centropages furcatus (Copepoda:Clanoidea) de una bahía subtropical (Bahía de La Paz, Golfo de California) RESUMEN. El objetivo del presente trabajo fue estimar bajo condiciones de laboratorio el efecto de dietas de diatomeas y dinoflagelados en las tasas de sobrevivencia, ingestión y producción de huevos del copépodo Centropages furcatus recolectado en la Bahía de La Paz. Se determinó el perfil de ácidos grasos de las diatomeas Odontella longicruris y Chaetoceros sp. y de los dinoflagelados Scrippsiella sp., Gyrodinium sp. y Prorocentrum micans, suministrados como alimento a C. furcatus. Después de incubar a 24 °C en oscuridad durante 24 h, la sobrevivencia de las hembras en todas las dietas fue > 90%. Las dietas de dinoflagelados favorecieron una mayor producción de huevos (>25 huevos hembra-1 día-1) con respecto a las diatomeas (<10 huevos hembra-1 día-1). No se observaron diferencias significativas en las tasas de ingesta al alimentarse con dinoflagelados o diatomeas, que variaron entre 400 y 900 ng C copépodos-1 h-1. Se obtuvo una mayor producción de huevos al utilizar dinoflagelados como alimento, sugiriendo una mayor calidad nutricional que se pudiera atribuir en parte a la mayor proporción de los ácidos grasos 18:4 (n-3) y 22:6 (n-3). Es posible que una mayor abundancia de dinoflagelados en la Bahía de La Paz pudieran relacionarse con una mayor producción de huevos de C. furcatus.

Palabras clave: Centropages furcatus, producción de huevos, ácidos grasos, Bahía de La Paz, fitoplancton. Band-Schmidt, C. J., R. Pacheco-Chávez, L. Carreón-Palau, J. A. Del Ángel-Rodríguez & S. Hernández-Trujillo. 2009. Effect of diatom and dinoflagellate diets on egg production and ingestion rate of Centropages furcatus (Copepoda: Calanoida) from a subtropical bay (Bahía de La Paz, Gulf of California).CICIMAR Oceánides, 24(2): 71-83. Fecha de recepción: 13 de agosto, 2009

Fecha de aceptación: 27 de noviembre, 2009

BAND-SHIMIDT et al.

INTRODUCTION There is often a clear functional relationship between annual cycles of zooplankton and phytoplankton productivity. In general, in polar and temperate ecosystems, the former lags the second by two months, approximately but there are different cycles in different latitudes (Fernández-Álamo & Färber-Lorda, 2006). There is only one annual peak of phytoplankton and zooplankton stocks in polar oceans, due to the brief period of light, while in the North Atlantic and other temperate waters there are typically two peaks in the annual cycle, one during spring and a smaller one during autumn (Fernández-Álamo & Färber-Lorda, 2006). In tropical and subtropical latitudes, there are not always such obvious seasonal changes, but a succession of small pulses of increases and decreases in phytoplankton and zooplankton stocks, largely modulated by local weather conditions and the movement of water masses (Sournia, 1969). Most of the studies on egg production and ingestion rates in copepods are restricted to temperate ecosystems. Several studies have demonstrated correlations between copepod production and food quality and quantity (Roman, 1984; Kleppel, 1993), which ultimately affect production at higher trophic levels (Smith & Eppley, 1982, in Kleppel 1993). Recently the nutritional value of diatoms for copepods has been challenged since high ingestion rates are frequently followed by low egg production and hatching success rates, including abnormal eggs and nauplii (Poulet et al., 1994; Laabir et al., 1995; Hyung-Ku & Poulet, 2000). Other studies demonstrated that some diatom species produce toxic, unsaturated aldehydes that affect normal embryogenesis (Pohnert et al., 2002; Ceballos & Ianora, 2003) or deform nauplii (Ianora et al., 2004). In several ecosystems dinoflagellates species are a major component of copepod diets (Kleppel et al., 1991; Cottonec et al., 2001), but their role has been rarely quantified and seems to depend upon the copepod species under study (Morey-Gaines, 1982) and the nutritive value of dinoflagellates (Cottonec et al., 2001). Particular relationships have been found between polyunsaturated fatty acids (PUFA) and zooplankton growth and egg production, particularly 20:5 (n-3) (eicosapentaenoic acid, EPA) and 22:6 (n-3) (docosahexaneoic acid, DHA) (Jónasdóttir, 1994; Müller-Navarra et al.,

2000; Anderson & Pond, 2000). Specific fatty acid requirements for egg production occur in different Acartia species (Jónasdóttir, 1994). Diatoms are typically rich in EPA, but deficient in DHA, whereas dinoflagellates contain high DHA and low EPA (Anderson & Pond, 2000). Several studies have demonstrated that egg production rates in copepods in polar and temperate ecosystems can be a biological index to estimate feeding conditions of females (Dagg, 1977; Saiz et al., 1993), but few studies have been done in subtropical zones to support this hypothesis. Copepod secondary production has been extensively studied (Runge & Roff, 2000). Planktonic copepods play a key role in the transfer of material and energy between primary producers and higher trophic levels (Cotonnec et al., 2001; Hirst & Bunker, 2003). To assess secondary production of copepods in natural habitats, where several environmental factors have influence, the effect of each environmental factor should be studied independently maintaining the rest of the variables constant (Shin et al., 2003). Several studies have already considered these aspects in different copepod species of Calanus, Temora, and Acartia (Mauchline, 1998). Although Centropages furcatus Dana 1894 is numerically abundant in coastal waters of subtropical regions, such has Bahía de La Paz (Palomares-García, 1996; Lavaniegos & González-Navarro, 1999). Gómez-Gutiérrez et al. (1999) where the first in estimate the egg production of C. furcatus but few studies have dealt with this species. The determination of grazing rates and egg production of copepods fed with different local phytoplankton species can allow a better understanding of the environmental factors that define the ecological niches of the copepods, leading the way to a description of environmental controls on community composition and on food web structure. This cannot be attained easily from field studies and requires experimental laboratory designed studies to test such trophic effects. The goal of this study was to determine the role of dinoflagellate and diatom diets isolated from Bahía de La Paz and their fatty acid composition, on survival, ingestion rate, and egg production of the tropical copepod C. furcatus collected in Bahía de La Paz, under laboratory conditions.

EFFECT OF DIATOM AND DINOFLAGELLATE DIETS

MATERIALS AND METHODS Cultures of Odontella longicruris (Greville) Hoban 1983, Chaetoceros sp., and Prorocentrum micans Ehrenberg 1833 collected from Bahía de La Paz, located on the western side of the Gulf of California and Scrippsiella sp. and Gyrodinium sp. collected from Bahía de Topolobampo on the eastern side of the Gulf of California were cloned under laboratory conditions (Table 1, Fig. 1). Vegetative cells of these species were collected by vertical tows with a 20-µm phytoplankton net. The phytoplankton was sieved through a 60-µm mesh screen to eliminate larger organisms. It was then placed in a 250-mL culture container filled with filtered seawater. In the laboratory, phytoplankton vegetative cells were isolated with micro-pipettes under an inverted microscope. Single cells and chains were transferred to 96-well plates with modified f/2 medium (Anderson et al., 1984) and maintained at 24 ± 1°C with 150 µE m-2 s overhead illumination supplied with cool-white fluorescent lights. Culture media were prepared with seawater obtained from the Ensenada de La Paz, a lagoon located at the southern part of Bahía de La Paz. Seawater was filtered through GF/F filters and sterilized in an autoclave at 121 °C and 1.1 kg cm-2 for 20 min. Cultures from wells were transferred to 50-mL culture tubes for maintaining the strains. Dinoflagellate strains where grown in modified f/2 medium (Anderson et al., 1984) and silica was added for diatom strains. Batch cultures where cultivated in 1-L polycarbonate

Figure 1. Location of Bahía de La Paz (B.P) and Bahía Topolobampo (B.T.) on opposite sides of the Gulf of California.

vials and maintained under temperature and light conditions described previously. Phytoplankton carbon content was estimated from cell volume, based on length and width measurements of 30 cells from each strain (Strathmann, 1967) (Table 1). Copepods were collected from Bahía de La Paz near the surface with a 333-µm plankton mesh net (Fig. 1). Plankton samples were transferred to the laboratory in iceboxes filled with in situ surface seawater. In the laboratory, adult females of C. furcatus where separated manually using a stereoscopic microscope and acclimated for two hours in filtered seawater at 24 °C and salinity of ~35 psu. Additionally 80 adult females of C. furcatus were separated, stored at -20 ºC for analysis of fatty acids. For each phytoplankton diet tested, 30 adult females were transferred to 1 L plastic flasks with 500-mL filtered seawater passed through GF/F filters and incubated in darkness at a temperature of 24 °C, salinity of 35 psu during 24 h. There were three replicates of each treatment within each trial. To determine the phytoplankton growth rate, two flasks without copepods where incubated under previously described conditions. At the beginning and the end of each trial, two mL subsamples of phytoplankton where fixed in Lugol´s iodine solution (Throndsen, 1978). At least 400 cells where counted on 1 mL Sedgwick-Rafter counting slides. Cell density was used to calculate exponential growth rates according to Guillard (1973) and female ingestion rates according to the equation of Frost (1972): I = ([V×g]/N) × C, g = (ln(Ci) – ln(Cf))/(t + k), where, V = volume of cell suspension in each flask (mL), g = grazing coefficient, N = number of copepods in each flask, C = cell concentration (cells mL-1), Ci = initial cell concentration (cells mL-1), Cf = final cell concentration (cells mL-1), t = time (h), and k = phytoplankton growth rate h-1. Copepods incubated in filtered seawater without phytoplankton represented the initial reproductive condition of females. After incubation for 24 h, 30 adult females in each bottle were gently separated through a 200-µm mesh screen and eggs and nauplii were collected in a 50-µm mesh screen. Surviving females, eggs, and nauplii where counted. Surviving females were pooled to complete at least 1mg of dry biomass for fatty acid analysis.

BAND-SCHIMIDT et al.

Table 1. Isolation date, geographical origin, cell volume, carbon content, and initial carbon concentration of different phytoplankton, and survival outcome of the copepod Centropages furcatus fed a diet composed of each phytoplankton species Cell Carbon Initial Isolation Survival Phytoplankton diets Source volume content-1 concentration 3 -1 date (%) (µm ) (pg cell ) (µg C L )

Odontella longicruris

February, 2004

Bahía de La Paz

Chaetoceros sp. Scrippsiella sp.

de November, 2004 Bahía Topolobampo

Gyrodinium sp. Prorocentrum micans

18,536

650

1000

91.8 ± 2.1

650

1000

90.1 ± 10

2,478

352

1000

96.9 ± 4.4

400

100 ± 0

873

800

100 ± 0

486 May, 2004

Bahía de La Paz

6,898

No food (control)

Dry biomass of microalgae and copepods were obtained by centrifugation and washed with 0.5 M ammonium formate before lyophilization (Virtis, SL, Gardiner, NY). Extraction and methanolysis of fatty acids where carried out by direct trans-esterification (Lepage & Roy, 1984, 1986; Barnung & Grahl-Nielsen, 1987). Samples were placed in thick-walled glass tubes adding 500 mL dry methanolic HCl, 2 N (Supelco, Bellefonte, PA) tightly closed with teflon-lined caps, sonicated for 20 min and heated at 90 ºC for 2 h in a water bath (Terlab, Guadalajara, Mexico). Excess of hydrochloric acid was removed under a nitrogen stream. The remaining solution was mixed with 4 mL hexane and 0.5 mL distilled water, mixed for 1 min with a vortex and centrifuged for 5 min at 10°C at 2000 g. The upper phase of hexane with fatty acids was separated and 10 mL of buthylated hydroxytoluene (BHT 1%) was added to prevent oxidation. Methyl esters were analyzed by gas chromatography with a 30 m × 0.25 mm fused silica capillary column (Omegawax, Supelco, Bellefonte, PA), with polyethylene glycol as the stationary phase with a thickness of 0.25 mm and helium as the carrier gas. The column was mounted in a gas chromatograph coupled to a mass spectrometer detector (GCD 1800B, Hewlett-Packard, Palo Alto, CA). The chromatographic conditions were: helium flow of 0.9 mL min-1 and injector temperature 250 °C. After injection, the temperature of the column was subjected to the following sequence: 110°C for three min, increased to 165 °C at a rate of 30 °C min-1, maintained at 165 °C for two min, increased to 209 °C at a rate of 2.2 °C min-1, and maintained at 220 °C for 35 min. The detector temperature was set at 260 °C and the ion source was set at 70 eV.

97.2 ± 3.0

Fatty acid identification was based on the interpretation of their mass spectra and compared with the mass spectra generated from commercial standards of 30 fatty acid methyl esters (FAMEs) commonly reported in marine organisms (Sigma, St. Louis, USA). When fatty acid isomers where found, retention time of at least one of the isomers in commercial standards allowed double bond positioning of the other isomers because the isomers with double bonds closer to the ester group elute earlier than isomers with more remote double bonds. Differences among fatty acid detector responses were calculated by plotting five different concentrations of FAMEs, ranging from 20 to 100 µg mL-1 on the x-axis against their peak areas on the y-axis. Simple linear regression models of each plot estimated the response factor for each fatty acid, and its concentration (ng/µg DW-dry weight) was calculated with the formula: Fi=[(Ai/Ri) × V]/DW where, Fi = concentration of each fatty acid (ng µg DW-1); Ai = peak area of each fatty acid (area units); Ri = response factor of each fatty acid (area units × µL µg-1); V = hexane volume of sample (µL); and DW = sample’s dry weight (µg). Fatty acid percentages were further calculated as Fi × 100 /S Fi for each sample. Carbon ingestion rates (ng C copepod-1 h ) were transformed to daily dry mass ingestion rates (µg DW copepod-1 day-1) as follow: DW = [100 × Ic × 24] / [{(P*CP)+ (L*CL)+ (C*CC)}/100], where, Ic = carbon ingestion rate, P = protein, L = lipid, C = carbohydrate percentages of diatoms (Rivero-Rodríguez et al., 2007) and dinoflagellates (Cabell & Alatalo, 1992), and CP, CL, and CC = the relative carbon content in proteins (53.06 %), lipids ( 77.63 %), and carbohydrates (44.44 %) respectively (Postel et al., 2000). -1

EFFECT OF DIATOM AND DINOFLAGELLATE DIETS

Daily fatty-acid ingestion rate of C. furcatus fed with diatom or dinoflagellate diets (ng copepod-1 day-1) was calculated by multiplying the amount of each fatty acid on each phytoplankton diet (ng µg DW-1) with the daily dry mass ingestion rates. The percentage of the fatty acid concentration data were arcsine-transformed, and the ingestion and egg production rates were log-transformed prior to statistical analyses. A one-way ANOVA test was applied (p < 0.05), followed by Tukey's post hoc analyses. The relative contribution of each fatty acid to the overall fatty acid composition between diatoms and dinoflagellates diets and composition of copepods where analyzed using a cluster analysis technique estimated with single linkage and Euclidean distance. Statistical analyses were performed with Statistica v.6 software (StatSoft). RESULTS Characteristics of phytoplankton diets: Isolation date, source, cell volume, and carbon content of phytoplankton diets are presented in Table 1. Species volume varied from 31 to 18536 µm3. Initial carbon concentration ranged from 400 to 1000 µg C L-1.

Fatty acid composition of C. furcatus females and their different phytoplankton diets are shown in Table 2 and Figure 3. Common fatty acids in all samples were 14:0, 16:0, 18:0, 18:1 (n-9), 18:1 (n-7), 18:2 (n-6), 18:4 (n-3), 20:5 (n-3) (except in Gyrodinium sp.), and 22:6 (n-3). Some saturated and monounsaturated fatty acids observed in C. furcatus were not present in each phytoplankton diet, such as iso 18:0, 19:0, 17:0, 17:1, ante iso 17:0, ante iso 16:0, 20:1 (n-9), 22:1 (n-9), and 23:0. Higher 16:1 (n-7)/C18 PUFA and 20:5 (n-3)/22:6 (n-3) ratios, and C16 PUFAs were common in diatom diets, whereas high proportions of C18 PUFA and 22:6 (n-3) were common in dinoflagellate diets. The biomass and fatty acid consumption per day indicate that when females of C. furcatus are fed with diatoms, the ingestion rate is higher (Fig. 4a). The ingestion of polyunsaturated fatty acids (PUFA), monounsaturated fatty acids (MUFA), and saturated fatty acids (SFA) varies between each diet offered. However, the proportion of DHA is higher with dinoflagellate diets (Fig. 4b). 1200

1000

800

600

400

200

-1

eggs f emale-1 day-1

Egg production rates in C. furcatus was different with each unialgal diet (Fig. 2). Significantly higher egg production rates were found in dinoflagellate diets (>30 eggs female-1 day-1) with the exception of the Scrippsiella sp. based diet. When C. furcatus were fed diatoms, egg production rates were below 10 eggs female-1 day-1. No significant differences were observed in the ingestion rates in C. furcatus when fed dinoflagellates or diatoms (Fig. 2). Ingestion rates varied between 400 and 900 ng C copepod-1 h-1.

ng C c opepod hr

egg production increase

After 24 h incubation, no significant differences were detected in the survival of adult females of C. furcatus. Survival rates with the different phytoplankton diets was >90.1% (Table 1). When C. furcatus was fed Gyrodinium sp. and P. micans no mortality was observed. Without food (control) survival of C. furcatus was also high (97.2%).

0 G y ro d i n iu m s p . S c r i p p s ie ll a s p .

P . m ica n s

O . lo n gicr u r is

C h a et oc e r o s s p .

Control

Figure. 2. Average egg production (bars, eggs/female day) and ingestion rates (circles, ng C/copepod hr) of Centropages furcatus fed different phytoplankton diets. Vertical whisker lines = SD.

BAND-SCHIMIDT et al.

Chaetoceros sp.

30 20 10 0 40 O. longicruris 30 20 10

Total fatty ac id percent

0 40

P. micans

30 20 10 0 40 Scrippsiella sp. 30 20 10 0 40

Gyrodinium sp.

30 20

iso 14:0 anteiso 14:0 15:0 16:0 iso 16:0 iso 17:0 18:0 20:0 22:0 24:0 16:1 n9 16:1 n7 16:1 n5 18:1 n9 18:1 n7 24:1 16:2 n6 16:2 n4 16:3 16:4 18:2 n6 18:3 n6 18:3 n3 18:4 n3 18:5 20:4 n6 20:5 n3 22:6 n3

12:0 14:0

Figure. 3. Fatty acid profile (%) of diatom and dinoflagellate diets.

Greater similarities between the fatty acid profiles of C. furcatus collected from the field and dinoflagellate diets were confirmed by cluster analysis (Fig. 5). C. furcatus, Gyrodinium sp., and Scrippsiella sp. were grouped at a Euclidean distance of 23, whereas P. micans was grouped at a Euclidean distance of 24.

The diatoms Chaetoceros sp. and O. longicruris formed a separated group at a Euclidean distance of 37 from C. furcatus. DISCUSSION Under our incubation conditions different phytoplankton diets (diatoms vs. dinoflagella-

EFFECT OF DIATOM AND DINOFLAGELLATE DIETS

Table 2. Comparison of percentages (%) of fatty acids in C. furcatus, diatoms, and dinoflagellates DIATOMS FAME 12:0 14:0 iso 14:0 ante iso 14:0 15:0 16:0 iso 16:0 ante iso 16:0 17:0 iso 17:0 ante iso 17:0 18:0 iso 18:0 19:0 20:0 22:0 23:0 24:0 S SFAS

DINOFLAGELLATES

C. furcatus Chaetoceros sp. O. longicruris P. micans Scrippsiella sp. Gyrodinium sp.

0.2 5.6 0.3 0.2 1.0 22.3 0.2 0.2 1.8 0.3 12.4 0.1 0.2 0.4 1.1 0.5 1.5 48.2

0.2 17.5 1.9 0.1 0.4 8.0 0.3 1.2 0.1 0.8 1.1 31.6

21.2 0.6 0.4 9.5 0.2 0.5 32.4

1.9 24.9 1.8 11.2 0.3 40.1

3.2 17.4 0.8 1.2 0.5 23.1

3.9 0.4 0.1 28.6 3.2 0.6 36.8

16:1 (n-9) 16:1 (n-7) 16:1 (n-5) 17:1 ha18:1 (n-9) 18:1 (n-7) 20:1 (n-9) 22:1 (n-9) 24:1 (n-9) S MUFAS

0.2 3.3 0.1 0.8 2.2 2.2 0.1 0.4 2.2 11.5

17.0 3.0 2.3 5.1 3.7 31.1

11.8 0.3 0.3 1.3 13.7

0.2 0.3 0.1 2.5 1.9 5.0

2.1 0.1 4.9 0.1 7.2

2.2 0.4 2.6

16:2 (n-6) 16:2 (n-4) 16:3 (n3) 16:4 18:2 (n-6) 18:3 (n-6) 18:3 (n-3) 18:4 (n-3) 18:5 (n3) 20:4 (n-6) 20:5 (n-3) 22:5 (n-3) 22:6 (n-3) S PUFAS

1.0 0.5 0.2 2.3 6.9 0.7 28.7 40.3

3.7 5.7 8.5 1.4 0.3 0.7 1.0 14.5 1.5 37.3

0.8 4.2 10.2 1.9 0.9 0.2 1.7 27.6 6.4 53.9

1.2 12.9 0.7 40.1 54.9

0.3 0.2 10.3 19.0 5.0 34.9 69.7

4.5 6.3 0.4 6.7 14.0 28.7 60.6

0.0 1.8 1.9 1.0 0.2

19.3 1.1 15.8 0.5 9.7

17.0 1.1 10.6 4.0 4.3

0 14.1 0 0.8 0

0 29.8 0 0 0.1

0 31.8 0 0.2 0

C16 PUFA C18 PUFA 16:1(n-7)/C18 PUFA 18:1 (n-9)/18:1 (n-7) 20:5 (n-3)/22:6 (n-3)

tes) did not affect survival nor ingestion rates of the copepod C. furcatus. However, dinoflagellate diets favored higher egg production rates (>25 eggs female-1 day-1) than diatom diets (<10 eggs female-1 day-1), this could be explained in part by the higher ingestion of DHA with dinoflagellate diets.

The survival of C. furcatus was not affected when fed with Gyrodinium sp.; in contrast, Acartia lilljeborgii Giesbrecht 1889 and A. clausi Giesbrecht 1892 from BahĂa de La Paz, had lower survival rates, 89.6 and 44.5%, when fed with Gyrodinium sp. (Band-Schmidt

BAND-SCHIMIDT et al.

Figure 4. Daily ingestion of fatty acids of C. furcatus fed different phytoplankton diets.

et al. 2008). Although the possible toxicity of our Gyrodinium strain requires further research, results suggest that Acartia copepod species are probably more sensitive than C. furcatus to Gyrodinium sp. toxic metabolites. Based on egg production rates, single-diatom diets were inadequate for C. furcatus. When A. clausi and A. lilljeborgii were fed with diatom diets Dytilum brightwelli (West) Grun 1860, Cylindrotheca closterium (Ehrenberg) Reimann & Lewin 1964, and Odontella longicruris (Greville) Hobban 1983) low egg production were observed; only Chaetoceros sp. supported high egg production rates (Band-Schmidt et al., 2008). Several studies have shown that ingestion of diatoms at high concentrations (=103 cells mL-1) are deleterious for copepod reproduction (Laabir et al., 1995; Ban et al., 1997), as was also demonstrated by low egg production and low hatching success rates, including abnormal egg and nauplii development (Poulet et al., 1994; Hyung-Ku & Poulet, 2000). Other studies demonstrated that some diatom species produce toxic, unsaturated al-

dehydes that block embryogenesis (Ceballos & Ianora, 2003) or deform nauplii (Ianora et al., 2004). Daily ingestion rates of fatty acids indicate that when fed diatom diets DHA ingestion is relatively low compared to dinoflagellates. Low egg production rates occurred with diatom diets containing low proportions of 22:6 (n-3), despite the high proportions of 20:5 (n-3) (EPA) in C. furcatus. Diets composed of dinoflagellates yield higher egg production rates, perhaps caused by a higher content of 18:4 (n-3) and 22:6 (n-3) (DHA); similar high and low egg productions occurred in Acartia omorii Bradford 1976 with the same combinations of fatty acids (Kyoungsoon et al., 2003). Polyunsaturated fatty acids (PUFAs) particularly 20:4 (n-6), 20:5 (n-3), and 22:6 (n-3) play an important role in reproduction, 20:4 (n-6) and 20:5 (n-3) are precursors of prostaglandins, hormones regulating ion fluxes, oocyte maturation, egg production, and hatching in marine invertebrates (Stanley-Samuelson, 1987, 1994). The fatty acid 22:6 (n-3) was strongly linked

EFFECT OF DIATOM AND DINOFLAGELLATE DIETS

Figure 5. Euclidean distance between the fatty acid profile of the copepod C. furcatus and its various phytoplankton diets.

with development of neural and visual functions in fish larvae (Bell et al., 1995). Several authors report that copepods require 20:5 (n-3) and 22:6 (n-3) in their diets for egg production rates. Theoretically, in omnivorous copepods, 20:5 (n-3) limits egg production when the diatom fraction is low, and 22:6 (n-3) when the dinoflagellate fraction is less abundant or as a lower contribution. However, Anderson & Pond (2000) suggest that the lack of PUFA synthesis in calanoid copepods occurs by stoichiometric limitation in carbon and nitrogen, rather than by lack of the required enzymes, and 22:6 (n-3) when the dinoflagellate fraction is low. In our study, dinoflagellates contributed with a low proportion of 20:5 (n-3), but a higher proportion of their precursor 18:4 (n-3). Limitations of zooplankton production by essential PUFAs is low if they actively synthesize them (Anderson & Pond, 2000), or if copepods can do retro-conversion of 22:6 (n-3) to shorter chains, such as 20:5 (n-3), as has been demonstrated in brine shrimp (Navarro et al., 1999). In this sense, dinoflagellates not only would provide essential PUFA to C. furcatus, but higher concentrations of carbon and nitrogen than other particles of similar size because they provide between 2 to 6 times more protein, 2.5 to 3.5 times more carbohydrate, and 1.1 to 3.0 times more lipid than diatoms of equivalent volume (Kleppel, 1993). This result is consistent with a higher response of egg

production to dinoflagellate diets in C. furcatus. Calbet & Alcaraz (1996) suggested that a close association exists between food availability and egg production in copepods. Higher egg production using dinoflagellate diets suggests that these diets could have a higher food quality for copepods, as these values were even higher than the mean egg production of C. furcatus in Bahía de La Paz under satiated food conditions in laboratory studies (23 eggs female-1 day-1) (Palomares-García et al., 2003). However these egg production values are much lower than those reported in other regions for C. furcatus, such has Bahía Magdalena with maximum values of 54 eggs female-1 day-1 (Gómez-Gutiérrez et al., 1999) and the Gulf of Mexico with 120 eggs female-1 day-1 (Checkley et al., 1992). Different responses in egg production rates have been observed among copepod species when fed dinoflagellate diets. For instance, adult female Centropages hamatus Lilljeborg 1853 fed with P. micans and Scrippsiella trochoidea (Stein) Loeblich 1976 did not produce eggs, whereas Lingulodinium polyedrum (Stein) Dodge1989 and G. sanguineum Hirasaka 1922 provided the nutrients necessary for egg production (Murray & Marcus, 2002). P. minimum proved to be a good diet for Temora stylifera Dana 1849, promoting moderate egg production and excellent egg viability

BAND-SCHIMIDT et al.

(Ceballos & Ianora, 2003). Hatching success and nauplii production of A. clausi decreased after ingestion of a progressively high number of toxic Alexandrium minutum Halim cells (Frangópulos et al., 2000), but the ingestion of the toxic dinoflagellate Gymnodinium catenatum Graham apparently had no adverse effects. The high ingestion and egg production rates of C. furcatus suggest that these dinoflagellates have higher nutritional value than natural phytoplankton assemblages (Palomares-García et al., 2003). The lack of significant differences in ingestion rates between diets of dinoflagellates or diatoms might indicate that C. furcatus is a less selective feeder than other copepod species, such as Acartia lilljeborgii and A. clausi, that exhibit significant differences in ingestion rates between single-celled algae diets (Band-Schmidt et al., 2008). A more diverse diet might increase the probability that C. furcatus will obtain a nutritionally-complete ration under different environmental food conditions. C. furcatus also feeds heavily on micro-zooplankton (Kleppel, 1993), reflecting its dual herbivorous and carnivorous foraging. The ratio between 18:1 (n-9) and 18:1 (n-7) fatty acid isomers has been proposed as a relative measure of carnivorous habits in several groups of marine invertebrates (Graeve et al., 1997; Falk-Petersen et al., 2000). Although C. furcatus can feed heavily on microzooplankton (Kleppel, 1993), a ratio of 1.0 suggests a higher phytoplankton contribution to its diet than for euphausiids from Bahía de La Paz, with a ratio of 3.1 (Del Angel-Rodríguez et al., 2008), or for carnivorous amphipods, with ratios ranging from 3.2 to 4.9 (Auel et al., 2002). The quotients between 16:1 (n-7) versus C18 PUFAs and 20:5 (n-3) versus 22:6 (n-3) have been proposed as indicators of diatom consumption (Graeve et al., 1997). Fatty acid composition of C. furcatus collected from the sea showed a low ratio (1.9%) of 16:1 (n-7)/C18 PUFA and a low ratio (0.2%) of 20:5 (n-3)/22:6 (n-3), suggesting low diatom consumption. Also, C. furcatus collected from Bahía de La Paz showed a higher proportion (29.4%) of 22:6 (n-3), suggesting higher dinoflagellate consumption at the time of collection. Our study suggests that, under natural conditions, C. furcatus predominantly graze on dinoflagellate species. However, a more diverse diet may increase the probability of suc-

cess in C. furcatus to attain the adequate fatty acid composition to fuel its reproduction under different environmental conditions. Grazing on diatoms may provide enough food for survival, but egg production will probably decrease. It is quite possible that higher concentrations of dinoflagellates provide higher biomass production of C. furcatus in Bahía de La Paz . ACKNOWLEDGEMENTS The authors thank J. Cruz for technical assistance and A. L. Ulloa Pérez for collecting samples form Sinaloa. This project was supported by Instituto Politécnico Nacional (SIP grants 20090299 and 20050133), and CONACYT grant 52724. REFERENCES Anderson, D.M., D.M. Kulis & B.J. Binder. 1984. Sexuality and cyst formation in the dinoflagellate Gonyaulax tamarensis: cyst yield in batch cultures. J. Phycol., 20: 418-425. Anderson, T.R. & D.W. Pond. 2000. Stoichiometric theory extended to micronutrients: comparison of the roles of essential fatty acids, carbon and nitrogen in the nutrition of marine copepods. Limnol. Oceanogr., 45: 1162-1167. Auel, H., M. Harjes, R. de Rocha, D. Stubing & W. Hagen. 2002. Lipid biomarkers indicate different ecological niches and trophic relationships of the artic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biology, 25: 374-383. Barnung, T.N. & O. Grahl-Nielsen. 1987. The fatty acids profile in Cod (Gadus morhua L.) eggs and larvae. Developmental variations and responses to oil pollution. Sarsia, 72: 412-417. Ban, S., C. Burns, J. Castel, Y. Chaudron, E. Christou, R. Escribano, S. Fonda, Umani, S. Gasparini, F. Guerrero-Ruiz, M. Hoffmeyer, A. Iaonora, H.K. Kang, M. Laabir, A. Lacste, A. Miralto, X. Ning, S. Poulet, V. Rodríguez, J. Runge, J. Shi, M. Starr, S. Uye & Y. Wang. 1997. The paradox of diatom-copepod interactions. Mar. Ecol. Prog. Ser., 157: 287-293.

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Lavaniegos, B.E. & E. González-Navarro. 1999. Copépodos del Canal de San Lorenzo en el ENSO 1992-93. Ciencias Marinas, 25(2): 240-257.

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Lepage, G. & C.C. Roy. 1986. Direct transesterification of all classes of lipids in a one-step reaction. J. Lipid. Res., 27: 115-120. Mauchline, J. 1998. Advances in Marine Biology. The Biology of Calanoid Copepods. Academic Press, London: 710 p. Morey-Gaines, G. 1982. Gymnodinium catenatum Graham (Dinophyceae): morphology and affinities with armoured forms. Phycologia, 21: 154-163. Müller-Navarra, D.C., M.T. Brett, A.M. Liston & C.R. Goldman. 2000. A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature, 403: 74-77. Murray, M.M. & N.H. Marcus. 2002. Survival and diapause egg production of the copepod Centropages hamatus raised on dinoflagellate diets. J. Exp. Mar. Biol. Ecol., 270: 39-56. Navarro, J.C., R.J. Henderson, L.A. McEvoy, M.V. Bell & F. Amat. 1999. Lipid conversion during enrichment of Artemia. Aquaculture, 174: 155-166. Palomares-García, J.R. 1996. Estructura especial y variación estacional de los copépodos en la Ensenada de La Paz. Oceánides, 11: 29-43. Palomares-García, J.R., A. Martínez-López & R. de Silva-Dávila. 2003. Winter egg production rates of four calanoid copepod species in Bahía de La Paz, Mexico. Contributions to the study of East Pacific Crustaceans, 2: 139-152.

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Pohnert, G., O. Lumineau, A. Cueff, S. Adolph, C. Cordevant, M. Lange & S. Poulet. 2002. Are volatile unsaturated aldehydes from diatoms the main line of chemical defense against copepods? Mar. Ecol. Progr. Ser., 245: 33-45. Postel, L. H. Fock & W. Hagen. 2000. Biomass and abundance. 83-192, In: Harris, R.P., P.H. Wiebe, J. Lenz, H.R. Skjoldal & M. Huntley (Eds.). ICES Zooplankton Methodology Manual. Academic Press, Londres. Poulet, S.A., A. Ianora, A. Miralto & A. Meijer. 1994. Do diatoms arrest embryonic development in copepods? Mar. Ecol. Progr. Ser., 111: 79-86. Rivero-Rodríguez, S., A.R. Beaumont & M.C. Lora-Vilchis. 2007. The effect of microalgal diets on growth, biochemical composition, and fatty acid profile of Crassostrea corteziensis (Hertlein) juveniles. Aquac., 263: 199-210. Roman, M.R. 1984. Utilization of detritus by the copepod, Acartia tonsa. Limnol. Oceanogr., 29: 949-959. Runge, J.A. & J.C. Roff. 2000. The measurement of growth and reproductive rates. 401-444. In: R.P. Harris, P.H. Wiebe, J. Lenz, H.R. Skjoldal & M. Huntley (Eds.). ICES zooplankton methodology manual. Academic Press.

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CICIMAR Oceánides, 24(2): 85-90(2009)

ESTIMATION OF TAYLOR'S POWER LAW PARAMETERS a AND b FOR TIDAL MARSH MACROBENTHIC SPECIES FLYNN, M. N. & W. R. L. S. PEREIRA. Universidade Presbiteriana Mackenzie. Sao Paulo, Brasil. email: flynn@uol.com.br ABSTRACT. In the Cananeia region of southeastern Brazil, Spartina alterniflora marshes colonize tidal flats fringing mangrove woodlands and displaying a zonation typical of monocultures. The pattern observed can be explained by the combined effects of organism resistance to emersion and physical dependence on the plants as habitat. In this context, it is interesting to quantify the aggregation index for the dominant species associated with the salt marsh. A tool which enables us to do it is Taylor´s power law, which combines the mean and the variance distributions of species in a known area. From August 1988 to January 1989, ten random samples were taken monthly from the lower and upper marshes using a 20 cm diameter corer (0.03 m2) at a depth of 10 cm. The five most representative species of the system were selected for further analysis, and for each of these, Taylor´s power law parameters were calculated. Epifaunal species present aggregation indexes approaching randomness. The aggregation indexes for the infaunal species were observed to have consistently high values even in clearly different conditions of population density and availability of organic matter. The smaller number of infauna forms in the lower marsh as compared to the upper marsh does not point to a competitive disadvantage since there is no alteration in b values. For the infauna species only, the value of a shows a sharp decrease from the lower to the upper marsh.

Keywords: Salt marsh macrobenthic fauna, spatial distribution, Taylor´s power law. Cálculo de los parámetros a y b de la Ley de Poder de Taylor para especies macrobentónicas de marisma RESUMEN. En la región de Cananeia al SE de Brasil, el pasto Spartina alterniflora coloniza los bajos de marea de las marismas que rodean los manglares, mostrando una zonación típica de monocultivos. El patrón observado se puede explicar por el efecto combinado de la resistencia de los organismos a la exposición al aire y a la dependencia física de las plantas como hábitat. En este contexto, es interesante cuantificar el índice de agregación para las especies dominantes asociadas a la marisma. Una herramienta que nos permite hacerlo es la Ley de Poder de Taylor, la cual combina las distribuciones promedio y de la varianza de las especies en un área conocida. De agosto de 1988 a enero de 1989, diez muestras mensuales fueron tomadas aleatoriamente de la marisma superior e inferior mediante un nucleador de 20 cm de diámetro (0.03 m2) a una profundidad de 10 cm. Las cinco especies más representativas del sistema fueron elegidas para un análisis posterior y se calcularon los parámetros de la Ley de Poder de Taylor a cada una de ellas. Las especies de epifauna presentaron un índice de agregación cercano a la aleatoriedad. Los índices de agregación de las especies de la endofauna mostraron consistentemente altos valores, incluso en diferentes condiciones de densidad de población y de disponibilidad de materia orgánica. El reducido número de formas de endofauna en la marisma inferior, comparada con la superior, no apunta a una desventaja competitiva, ya que no hay alteraciones en los valores de b. Solo para las especies de endofauna, el valor de a mostró un agudo decremento desde la marisma inferior hacia la superior.

Palabras clave: Marisma, macrofauna bentónica, distribución espacial, Ley de Poder de Taylor. Flynn, M. N. & W. R. L. S. Pereira. 2009. Estimation of Taylor's power law parameters a and b for tidal marsh macrobenthic species. CICIMAR Oceánides, 24(2): 85-90.

INTRODUCTION In southeastern Brazil, Spartina alterniflora Loisel, 1807 marshes colonize tidal flats fringing mangrove woodlands and display a Fecha de recepción: 06 de agosto, 2009

zonation typical of monocultures, with different growth forms and shoot densities characterizing the lower and upper marshes, each presenting different community organizations as to mean densities and faunal dominance. This Fecha de aceptación: 24 de noviembre, 2009

FLYNN & PEREIRA

herbaceous plant community has different structure above and below the mean high water (MHW). Below MHW the assembly is dominated by epifaunal species such as Sphaeromopsis mourei Loyola & Silva, 1960, Parhyale hawaiensis Dana, 1853 and Littorina angulifera Lamarck, 1822, while above MHW it is dominated by the infauna species Isolda pulchella Fritz Muller, 1858 and Nereis oligohalina Fritz Muller, 1858. The pattern observed can be explained by the combined effects of organism resistance to exposure and physical dependence on the plant as substratum (Flynn et al., 1998). The epifaunal crustaceans are associated with the S. alterniflora blades and are dominant in the lower marshes because of the adequate period of immersion. Infauna organisms were dominant in the upper marshes because they can better resist the prolonged exposure to air and benefit from the high plant biomass there (Flynn et al., 1996; Flynn et al., 1998). TaylorÂ´s Power Law (TPL) is a well documented relation between the average and the variance of ecological populations. Its use has been amply discussed and it provides useful information regarding the dispersal patterns of organisms (Gaston et al., 2006). Taylor (1961) first used the formula derived from the negative binomial distribution to measure the level of aggregation. In this equation, m and S2 represent the first and the second moments respectively, which are statistical terms denoting the mean and the variance of the binomial negative probability function (Ascombe, 1949). Taylor expected k to be a characteristic of each species but found that k is not always independent of the mean. Taylor originally suggested that a and b were fixed for each species. Examining sets of samples of various species, Taylor found that the mean was related to the variance according to the power law S2 = a mb suggesting that both, a and b are population characteristics. With log-transformed data, the power law in this case is represented by a straight line of slope b and y-intercept a. The maximum value of the log of the variance is obtained when b equals 2, log S2max = log a + 2 log m. Biologically we can interpret S2max as the maximum variance expected for a given number of population sets of a chosen two dimensional area (b = 2) sampled at a specific location. However, it was found that for different methods of sampling a changes while b remains constant for a

given species (Taylor, 1970). The slope b is considered an aggregation index. The slope equals unity for a random distribution; it is lower than unity in the case of a regular distribution and greater than unity in the case of an aggregated distribution. In a study of aphid distributions with fixed sample methodology (Taylor, 1977; Taylor et al., 1979), a was affected by the host plant distribution, leading to the conclusion that a can be used as an environmental stress index. In spite of the evidence, the behavior of a and b are not completely understood. A full explanation and review of TPL with detailed derivations can be found in Tokeshi (1995) and Eisler et al. (2008). Our objective was to obtain TPLÂ´s parameters (a and b) for five macrofaunal species from empirical data collected in a tidal flat colonized by Spartina alterniflora at Cananeia lagoon estuarine system (Flynn et al., 1998), and estimating their values for the lower and upper marshes. MATERIAL AND METHODS Cananeia lagoon estuarine system is located in the State of SĂŁo Paulo, southeastern Brazil. A complete description and characterization of the system is given in Schaeffer-Novelli et al. (1990). Pure stands of Spartina alterniflora form the bulk of the vegetation. Samples were taken randomly from the lower and upper marshes at Ponta do Arrozal, which contains the largest marsh in the region, covering an area of 25 km2. Faunal samples were taken monthly from August 1988 to January 1989 consisting of 10 randomly chosen replicates taken with a 20 cm diameter corer (0.03 m2) at a depth of 10 cm. Standing dead and live shoots of S. alterniflora were clipped at ground level and visually searched for epifaunal organisms. Samples were sieved through 1.0 and 0.5 mm meshes. The organisms were then fixed in 10% formalin and preserved in 70% ethanol. All specimens were identified at the lowest possible taxonomic level and counted under a dissecting microscope. Five of the total 60 species were used, the epifaunal crustaceans Sphaeromopsis mourei and Parahyalle hawaensis, dominant in the lower marsh, Nereis oligohalina and Isolda pulchella, dominant in the upper marsh, and Littorina angulifera common in both. A total of 14,803 specimens were obtained for these 5 species (S. mourei, lower marsh = 1,417; P. hawaiensis, lower marsh = 965, upper marsh

ESTIMATION OF TAYLOR´S PARAMETERS

= 202; I. pulchella, lower marsh = 334, upper marsh = 5,950; N. oligohalina, lower marsh = 584, upper marsh = 3,650; L. angulifera, lower marsh = 441, upper marsh = 1,260). A two-way analysis of variance with replication was used in order to test for differences in abundance in each of the top five species by site and month. The power of the test was estimated to be around 0.78 based on the method described by Zar (1999) (Flynn et al., 1998). To estimate the parameters a and b of TPL a logarithmic transformation of the data was performed for each species set. The coefficient of determination (Pearson r-squared, R2) was used as an indicator of quality of the linear regression. The angular coefficient (b) and the y-intercept (log a) of each species was tested with the 2-tailed Student’s t-test (a = 0.05) with n-2 degrees of freedom. RESULTS The Taylor´s constants calculated for each macrofaunal species were the slope b (aggregation index) and the y-intercept a (environmental stress index) (Table 1). For the infaunal species I. pulchella and N oligohalina the aggregation index values were around 2. For epifaunal species and for S. mourei, present only at the lower marsh, the aggregation index was lower than 2. The environmental stress indexes for the infaunal species were significantly different for the two sites. For I. pulchella the a value in the lower marsh was higher than in upper marsh. The same behavior was observed in N. oligohalina. Thus, for infaunal species, there is a clear decrease in a with increasing distance to water. Epifaunal species did not show the same trend. L. angulifera in the lower marsh show a higher value than in the upper marsh. P. havaiensis showed similar values between sites and S. mourei presented an environmental stress index value relatively high. The log transformed TPL for the macrofaunal species of the lower and upper marshes is presented in Figure 1. The linear slope represents the aggregation index, and the y-intercept value the environmental stress index. The infaunal species I. pulchella and N. oligohalina presented higher and more stable mean density values at the upper marsh throughout the sampling period, while epifaunal species P. hawaensis and L. angulifera presented clear variations in mean densities,

Table 1. Taylor's parameters resulting in the linear equation log S2 = b log m + log a for the five macrofaunal species, with the determination coefficient (R2) and confidence interval (CI). Lower Marsh a ± CI I. pulchella

b ± CI

2,388 ± 0,186

2,139 ± 0,355 0.899

N. oligohalina 1,770 ± 0,440

2,094 ± 0,566 0.843

L. angulifera

1,982 ± 0,047

1,719 ± 0,068 0.968

P. hawaiensis 4,207 ± 0,037

1,583 ± 0,029 0.983

S. mourei

1,134 ± 0,084 0.937

3,606 ± 0,128

Upper Marsh a ± CI I. pulchella

b ± CI

0.942 ± 2,470

2,010 ± 0,658 0.810

N. oligohalina 0.456 ± 1,586

2,123 ± 0,514 0.859

L. angulifera

1,122 ± 0,109

1,780 ± 0,075 0.967

P. hawaiensis 4,305 ± 0,189

1,214 ± 0,425 0.585

both between sites and throughout the period. Epifaunal species are dominant in the lower marsh, mainly because of the smaller infaunal abundance. S. mourei occurs exclusively in the lower marsh (Table 2). DISCUSSION The positive correlation of the mean densities of N. oligohalina and I. pulchella with the plant biomass (Lana & Guiss, 1992) and their preference for habitats with high plant biomass in areas where tide levels allows a denser colonization by S. alterniflora (Flynn et al., 1996) does not translate into different values of species aggregation index. I. pulchella and N. oligohalina present high values of the aggregation index b, both for high population densities in the upper marsh and for low population densities in the lower marsh. The aggregation indexes for the infaunal species show consistently high values even in clearly different conditions of population density and availability of organic matter. The aggregation of these infaunal species to single stems or groups of stems of salt marsh vegetation seems to protect them against predatory action. Their sedentary habit as detritus feeders with low selectivity, which does not call for great displacements, promotes their continuous permanence in the habitat and, consequently, their aggregated pattern (Rader, 1984). L. angulifera, P. hawaiensis and S. mourei present aggregation indexes below 2. The first two species show a more highly aggregated distribution than the third, which is almost random. In natu-

FLYNN & PEREIRA

Figure 1. Relationship between the log transformed variance and log transformed mean abundance of the macrofaunal species, with the adjusted linear equation for lower and upper marshes.

re, the aggregation index b for true randomness (b = 1) is one possible value within a continuous range from b = 0 (for regular distribution) to b = 2 (highly aggregated distribution). TPL method was applied to more than 400 sets of species data with b varying from 0.9 to 2.6, with a higher concentration of values between 1.0 and 1.8 (Taylor & Woiwod, 1982). Values of b higher than 2 are due to errors caused by the great number of zeros in the ecological data (Tokeshi, 1995). The values we obtained varied from 1.134 to 2.139. With the exception of S. mourei, exclusively of the lower marsh, the aggregation indexes for the species considered were very similar in the upper and lower marshes. Therefore, b seems to describe an intrinsic biological property of the macrofaunal species considered here, consis-

tent with the concept of He and Gaston (2003) of a model considering the abundance-variance occupancy as a explanation for the occurrence of diverse species assemblages at different scales. There is obvious variation about the interspecific abundanceâ&#x20AC;&#x201C;variance relationship (Gaston et al., 2006). The initial impression of homogeneity created by a monospecific bed of S. alterniflora masks the reality of a truly patchy ecosystem. The infaunal species are clearly the numerical dominant forms in the upper marsh, while in the lower marsh the epifaunal forms are dominant (Flynn et al., 1998). N. oligohalina and I. puchella are in numerical disadvantage in the lower marsh. However, this is not reflected in the aggregation index values. As pointed out by Taylor (1961) in his support of

ESTIMATION OF TAYLOR´S PARAMETERS

Table 2. Variation range and results of 2-way ANOVA evaluating effect of site and time on each of the five macrofaunal species considered (lower marsh vs. upper marsh). NS: non significant difference, p>0.05; *0.05>p>0.01; **p<0.01; ***p<0.001.

Species

Variation range (0.03m2)

Total average

Between F-value Interaction Site Time

Lower marsh

Upper marsh

Lower marsh

Upper marsh

(df = 1)

(df = 5)

Sphaeromopsis mourei

0-376

148.2

41.07***

8.99***

Parahyale hawaensis

0-184

0-38

73.6

10.8

20.48***

10.11***

5.67***

Littorina angulifera

11-92

14-174

47.6

104.6

6.49**

4.16***

1.82NS

Isolda pulchella

4-51 102-445

23.2

352.6

35.66***

1.85NS

1.73NS

Nereis oligohalina

7-60 141-348

37.2

305.0

39.24***

1.18NS

0.70NS

the TPL parameter b as an aggregation index, it is plainly desirable that an index of population structure should be the same for different population densities, unless some actual change in behavior is involved. When we compare infaunal polichaets densities for the lower and the upper marshes, we find that the latter is 11.8 times higher (Flynn, 1998). We saw no significant difference in b values. Would the numerical decrease of infaunal forms point to a competitive disadvantage in the lower marsh as compared to the upper marsh? It seems that the answer to this question is no, since there is no significant variation in b values. Based on results obtained from computer simulations Kilpatrick and Ives (2003) associated a strong competition force or a smaller carrying capacity K to a TPL slope decrease. In their simulation, as the average slope decreases from 2 to 1, the competition coefficient increases from 0 to 0.16, so that competitive interactions are also sensitive to population fluctuations and TPL parameters. Nevertheless, the infaunal decline in abundance in the lower marsh could be caused by a decrease in carrying capacity K, since, the more common species are supposedly associated with higher carrying capacities. The lower S. alterniflora densities and the consequently lower availability of organic matter in the lower marsh, coupled with the presence of a higher number of species, seem to interfere with the infaunal species abundance, so that the lower spatial occupation can be related to a greater environmental stress. Supporting this view is

the value of a for infaunal species which is clearly smaller in the upper marsh than in the lower marsh. REFERENCES Ascombe, F. J. 1949. The Statistical Analysis of Insect Counts Based on the Negative Binomial Distributions. Biometrics, 5: 165-173. Eisler, Z., I. Bartos & J. Kertész. 2008. Fluctuation scaling in complex systems: Taylor’s law and beyond. Adv. Phys., 57: 89-142 Flynn, M. N., A. S. Tararam & Y. Wakabara. 1996. Effects of habitat complexity on the structure of macrobenthic association in a Spartina alterniflora marsh. Braz. J. Oceanogr.,44 (1): 9-21. Flynn, M. N., Y. Wakabara & A. S. Tararam. 1998. Macrobenthic associations of the lower and upper marshes of a tidal flat colonized by Spartina alterniflora in Cananeia lagoon estuarine region (southeastern Brazil). Bull. Mar. Sci., 63(2): 427-442. Gaston, K. J., P. A. Borges, F. He, C. Gaspar. 2006. Abundance, spatial variance and occupancy: arthropod species distribution in the Azores. J. Anim. Ecol., 75: 646–656.

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He, F. & K.J. Gaston. 2003. Occupancy, spatial variance, and the abundance of species. Amer. Nat., 162, 366–375.

Taylor, L. R. 1970. Agregation and the transformation of counts of Aphis fabae Scop. on beans. Ann. Appl. Biol., 65: 181-189.

Kilpatrick, A. M. & A. R. Ives. 2003. Species interactions can explain Taylor´s power law for ecological time series. Nature, 422: 65-68.

Taylor, L. R. 1977. Migration and the spatial dynamics of an aphid. J. Anim. Ecol., 46: 411-423.

Lana, P. C. & C. Guiss. 1992. Macrofauna-plant-biomass interactions in euhaline salt marsh in Paranagua Bay (SE Brazil). Mar. Ecol. Prog. Ser., 80: 57-64. Rader, R. D. 1984. Salt-marsh benthic invertebrates: small scale patterns of distribution and abundance. Estuaries, 7: 413-420. Schaeffer-Novelli, Y., H. S. L. Mesquita & B. Cintron-Molero. 1990. The Cananeia lagoon estuarine system, São Paulo, Brazil. Estuaries, 13: 193–203. Taylor, L. R. 1961. Aggregation, variance and the mean. Nature, 189: 732-735.

Taylor, L. R., I. P. Woiwod & J. N. Perry. 1979. The negative binomial as a dynamic ecological model for aggregation, and the density dependence of k. J. Anim. Ecol., 48: 289-304. Taylor, L. R. & I. P. Woiwod. 1982. Comparative synoptic dynamics: 1. Relationships between interspecific and intraspecific spatial and temporal variance-mean population parameters. J. Anim. Ecol., 51: 879-906. Tokeshi, M. 1995. On the mathematical basis of the variance-mean power relationship. Res. Popul. Ecol., 37(1): 43-48. Zar, J.H. 1999. Biostatistical Analysis. 4 ed. Prentice-Hall, Upper Saddle River.

CICIMAR Oceánides, 24(2): 91-99(2009)

VARIACIÓN DE LOS ÍNDICES MORFOFISIOLÓGICOS DE LA ALMEJA MANO DE LEÓN Nodipecten subnodosus (SOWERBY, 1835) EN BAHÍA DE LOS ÁNGELES, B.C., GOLFO DE CALIFORNIA Yee-Duarte, J. A., B. P. Ceballos-Vázquez & M. Arellano-Martínez Centro Interdisciplinario de Ciencias Marinas-IPN, Av. Instituto Politécnico Nacional, S/N, Col. Playa Palo de Santa Rita. Apartado postal 592, La Paz, Baja California Sur, México. CP 23096. Tel: (612)1225366, Fax: (612)1225322, email: bceballo@ipn.mx RESUMEN. De enero a diciembre de 2006 se analizó la variación en los valores de los índices gonadosomático (IGS), de músculo (IM), de glándula digestiva (IGD) y del manto (IMA) de Nodipecten subnodosus en Bahía de los Ángeles, B.C., México. Se analizaron un total de 334 organismos dentro de un intervalo de tallas de 48 a 172 mm de altura de concha. El IGS mostró un patrón estacional, indicando que la madurez gonádica se presentó de abril a junio. Tanto el IGD como el IMA presentaron correlación significativa con el IGS (P< 0.05). El IM no presentó correlación significativa con el IGS (P > 0.05). El análisis de la variación de los índices morfofisiológicos indica que es posible que en Bahía de los Ángeles, B.C., N. subnodosus presente un ciclo de almacenamiento y transferencia de energía desde tejidos somáticos hacia la gónada, para soportar la gametogénesis. N. subnodosus se reproduce en un rango de temperatura bien definido (inicia su gametogénesis entre los 17 °C y 18 °C de temperatura superficial del mar y alcanza su máxima madurez entre los 23.5 °C y 26.8 °C).

Palabras clave: Índices morfofisiológicos, reproducción, pectínidos. Variation in the morphophysiological indices of the lion paw scallop Nodipecten subnodosus (Sowerby, 1835) in Bahía de los Ángeles, B.C., Gulf of California ABSTRACT.From January to December, 2006 the variation of the gonadosomatic (IGS), muscle (IM), digestive gland (IGD) and mantle indices (IMA) of Nodipecten subnodosus in Bahía de Los Angeles, B.C., Mexico were analyzed. A total of 334 organisms were examined, all within an interval of 48 to 172 mm of shell height. The IGS showed a seasonal pattern indicating that the gonadic ripeness appeared from April to June. Both, the IGD and the IMA had a significant correlation with the IGS (P < 0.05). The IM did not show a significant correlation with the IGS (P > 0.05). The analysis of the variation of the morphophysiological indices indicates that it is possible that in the Bahía de Los Angeles, B.C., N. subnodosus presents a cycle of storage and transference of energy from somatic tissues to the gonad to support gametogenesis. N. subnodosus reproduces in a defined rank of temperature, it begins its gametogenesis between 17 °C and 18 °C of temperature of the water and reaches its maximum ripeness between 23.5 °C and 26.8 °C.

Keywords : Morphophysiological indices, reproduction, pectinids. Yee-Duarte, J. A., B. P. Ceballos-Vázquez & M. Arellano-Martínez. 2009. Variación de los índices morfofisiológicos de la almeja mano de león Nodipecten subnodosus (Sowerby, 1835) en Bahía de los Ángeles, B.C., Golfo de California. CICIMAR Oceánides, 24(2): 91-99.

INTRODUCCIÓN La almeja mano de león, Nodipecten subnodosus es un pectínido hermafrodita funcional que se distribuye desde la Laguna Ojo de Liebre en Baja California Sur, México, incluyendo el Golfo de California, hasta las costas del noroeste de Perú (Keen, 1971). Representa un recurso pesquero importante debido a que su gran músculo aductor o “callo” es apreciado en el mercado internacional. En México, su pesquería se limita exclusivamente a la zoFecha de recepción: 11 de junio, 2009

na de la Laguna Ojo de Liebre; en diversos cuerpos de agua de la Península de Baja California se considera una especie sobreexplotada (Taylor et al., 2006). Por lo anterior y aunado a su alta tasa de crecimiento (Villalejo-Fuerte et al., 2004), se considera que N. subnodosus tiene un alto potencial para la acuicultura (Arellano-Martínez et al., 2004a; Koch et al., 2005). Debido a su importancia pesquera y acuícola se han realizado diversos estudios sobre Fecha de aceptación: 24 de septiembre, 2009

YEE DUARTE et al.

la biología de esta almeja, enfocados en evaluar el crecimiento y acondicionamiento en sistemas de cultivo (García-Domínguez et al., 1992; Morales-Hernández & Cáceres-Martínez, 1996; Félix-Pico et al., 1999; Barrios-Ruíz et al., 2003; Quintero-Ojeda, 2003; Villalejo-Fuerte et al., 2004; Koch et al., 2005; Osuna-García, 2006; Pérez-De León, 2006; Taylor et al., 2006), así como para evaluar aspectos sobre su estado fisiológico y su reproducción (Reinecke-Reyes, 1996; Racotta et al., 2003; Arellano-Martínez et al., 2004a; Arellano-Martínez et al., 2004b). Sin embargo, ninguno de estos estudios se ha realizado en Bahía de los Ángeles, B.C., lugar en el que existe el interés por iniciar la pesquería comercial de la especie. La variación del peso de la gónada, manto, músculo o glándula digestiva ha sido asociada al estado fisiológico de los organismos (Sastry, 1968; Villalejo-Fuerte & Ceballos-Vázquez, 1996; Barrios-Ruíz et al., 2003; Marín et al., 2003; Arellano-Martínez et al., 2004b; Barber & Blake, 2006; Didri et al., 2007; Kang et al., 2007), debido a que dichos órganos funcionan como reservorios de nutrientes, que posteriormente son utilizados para diversos procesos metabólicos, tales como la reproducción, que se caracteriza por tener un alto gasto energético (Barber & Blake, 1981; Arellano-Martínez et al., 2004b; Darriba et al., 2005; Matus de La Parra et al., 2005; Villalejo Fuerte et al., 2005; Mercado-Silva, 2005; Sahin et al., 2006). Esta variación puede ocurrir en relación directa con el desarrollo de la gónada (Aldrich & Crowley, 1986; Sahin et al., 2006) o de forma inversa entre el tejido gonádico y los tejidos somáticos, sugiriendo que existe una transferencia de reservas de energía desde los tejidos somáticos a la gónada (Gabbott, 1975; Bayne, 1976; Epp et al., 1988; Park et al., 2001; Arellano-Martínez et al., 2004b; Barber & Blake, 2006). Esta transferencia depende de la especie y las condiciones ambientales que presente la zona en que habita (Bricelj et al. 1987; Epp et al. 1988). Con la finalidad de detectar la posible existencia de un ciclo de transferencia de energía desde los tejidos somáticos hacia la gónada, en este trabajo se analizó la variación temporal de los índices morfofisiológicos de N. subnodosus en Bahía de los Ángeles, B.C., México. Adicionalmente, se probó la posible influencia de la temperatura superficial del mar sobre la reproducción de la especie.

MATERIAL Y MÉTODOS Se recolectaron al azar entre 20 y 30 ejemplares de N. subnodosus mensualmente durante 2006 por medio de buceo semiautónomo en Bahía de los Ángeles, B.C. (Golfo de California) (29º 00’ N y 113º 30’ W) (Fig. 1). De cada organismo se registró el peso total y sin concha, así como la altura de la concha (AC). Las almejas se disectaron en fresco para obtener los pesos de la gónada, del músculo aductor, de la glándula digestiva y del manto. La temperatura superficial del mar se obtuvo de información obtenida mediante sensores remotos (Pacheco-Ayub & Bautista-Romero, 2009). Con los pesos obtenidos se calcularon los siguientes índices morfofisiológicos: gonadosomático (IGS), del músculo (IM), de la glándula digestiva (IGD) y del manto (IMA) como la razón del peso del órgano y el peso sin concha; los resultados se expresaron en porcentaje (Sastry, 1970). Los valores del IGS se consideraron valores cuantitativos que representan la actividad reproductiva (Arellano-Martínez et al., 2004b). De acuerdo a los criterios establecidos por Barber & Blake (2006), un aumento en el IGS se consideró como indicador de maduración gonádica, mien-

Figura 1. Localización del sitio de estudio (O) y de las localidades en donde se ha estudiado Nodipecten subnodosus en la Península de Baja California. Figure 2. Location of study site (O) and localities where Nodipecten subnodosus has been studied along the Baja California Peninsula.

ÍNDICES MORFOFISIOLÓGICOS EN N. subnodosus

tras una disminución se consideró como ocurrencia de desove. Asimismo, un incremento en el IM, IGD e IMA se consideró como un almacenamiento de reservas energéticas y un decremento se consideró como utilización o transferencia de energía. Para verificar si existía variación significativa de todos los índices a lo largo del periodo de estudio, se aplicaron análisis de varianza de una vía (ANDEVA), usando como factor el tiempo (12 niveles: meses); cuando se encontraron diferencias significativas se realizo una prueba a posteriori para comparación de medias (Tukey). Debido a que los valores del IGS, IM, IGD e IMA son porcentajes, se les aplicó la transformación arcoseno (arcoseno Ö p) (Zar, 1996) con la finalidad de normalizar la distribución de los datos. Además, se hicieron correlaciones de Pearson para establecer la posible relación del IGS (indicador del proceso reproductivo) con los otros tres índices; para determinar si el IGS tiene alguna relación con la temperatura se hizo una correlación de rangos de Spearman (Zar, 1996). El nivel de significancia fue establecido en a = 0.05. RESULTADOS Se recolectaron 334 organismos, cuyo intervalo de tallas fue de 48 a 172 mm de AC (media = 117 mm, d. s. = 27.5 mm). En la figura 2 se presentan las variaciones anuales de los cuatro índices. En todos los casos se encontraron diferencias significativas entre los meses analizados (ANDEVA, P < 0.05). De febrero a julio, el IGS presentó valores significativamente más altos, encontrando los mayores en abril, mayo y junio (15%, 15% y 14%, respectivamente). Sin embargo, a partir de julio se observó un decremento hasta alcanzar los valores significativamente más bajos en noviembre y diciembre (5% y 5.7%, respectivamente) (Fig. 2a). Tanto el IGD como el IMA mostraron variaciones similares (Fig. 2b y c). Sus valores significativamente más altos se presentaron en febrero, comenzaron a disminuir concomitantemente en los siguientes meses hasta alcanzar un mínimo en abril y mayo en el caso del IMA, y en junio y julio en el caso del IGD. Los valores de ambos índices aumentaron en agosto; se presentó una segunda disminución significativa en septiembre para volver a aumentar en los siguientes meses.

Por su parte, el IM mostró mayor variación durante el periodo de estudio (Fig. 2d). En febrero-marzo y septiembre se presentaron los valores más altos (56.7%, 55.9% y 54.2%, respectivamente). Mientras que en abril y octubre se observaron disminuciones significativas en sus valores. Se encontró una correlación negativa baja pero significativa del IGS con el IGD (r = -0.12, P < 0.05) y con el IMA (r = -0.27, P < 0.05), pero el IGS no se correlacionó significativamente con el IM (r = 0.01, P > 0.05). Por su parte, no se presentó una correlación entre el IGS y la temperatura superficial del mar (P > 0.05), la cual varió de manera estacional (Fig. 3). Los valores más bajos se presentaron de enero a marzo (16 °C), de abril a septiembre la temperatura aumentó de 19 °C a 30 °C, posteriormente se observó una disminución a partir de octubre y hasta alcanzar una temperatura de 19 °C en diciembre. DISCUSIÓN A partir de un estudio realizado en la Laguna Ojo de Liebre, en el que se contrastó la variación estacional de los valores del IGS con las fases de desarrollo gonádico establecidas histológicamente, se encontró que el IGS es un buen indicador de la estacionalidad de la reproducción de N. subnodosus (Arellano-Martínez et al. 2004a). Considerando lo anterior, en Bahía de los Ángeles, B.C., Golfo de California, la variación del IGS indica que N. subnodosus se reproduce estacionalmente, iniciando el desarrollo de la gónada durante el invierno y madurando durante la primavera. Sin embargo, en localidades de la Península de Baja California ubicadas en la costa del Pacífico (Bahía Magdalena y Laguna Ojo de Liebre, B.C.S., México) esta especie inicia su desarrollo gonádico durante primavera y madura durante verano-otoño (Reineke-Reyes, 1996; Racotta et al., 2003; Arellano-Martínez et al., 2004a). Está bien documentado que la temperatura del agua es uno de los factores ambientales más importantes que modulan la reproducción de muchos moluscos bivalvos (Sastry, 1979; Mackie, 1984; Román et al., 2001; Gosling, 2004; Barber & Blake, 2006), ya sea como iniciador de la gametogénesis o como disparador del desove (Sastry, 1970; Sastry, 1979; Giguere et al., 1994; Barber & Blake, 2006). En este estudio, la variación del IGS indica que la gametogénesis de N. subnodosus en Bahía de Los Ángeles, B.C., comenzó entre enero y febrero (evidenciada por el in-

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Figura 2. Variación estacional de (a) índice gonadosomático, (b) índice de la glándula digestiva, (c) índice del manto, (d) índice del músculo de Nodipecten subnodosus en Bahía de los Ángeles, B.C., México. Las medias que no tienen la misma letra son significativamente diferentes. Las barras corresponden al error estándar. Figure 2. Seasonal variation of (a) gondasomatic, (b) digestive gland, (c) mantle and (d) muscle indices of Nodipecten subnodosus in Bahía de los Ángeles, B.C., México. Distinct literals represent a significant difference. Bars represent the standard error.

cremento en sus valores), cuando la temperatura superficial del mar era la más baja (17.2 °C). Por su parte, la máxima madurez (IGS entre 14% y 15%) se presentó de abril a junio con temperaturas de entre 23 °C y 26.8 °C, mientras que el desove (indicado por la disminución en los valores del IGS) se presentó de junio a agosto. En contraste, en un estudio realizado en la Laguna Ojo de Liebre, B.C.S. (costa W de la península), la gametogénesis de N. subnodosus inició en abril cuando la temperatura superficial del mar comenzó a incremen-

tarse (18 °C) y la máxima madurez se dio en agosto, justo cuando la temperatura fue la más alta (23.5 °C) y los desoves se presentaron de septiembre a noviembre (Arellano-Martínez et al., 2004a). Este patrón general fue también observado por Reinecke-Reyes (1996) en la misma zona y por Racotta et al. (2003) en Bahía Magdalena, B.C.S. (450 km al sur de la Laguna Ojo de Liebre). Este aparente contraste en el patrón reproductivo de N. subnodosus entre localidades del Océano Pacífico y el Golfo de California se explica porque

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(a tejido gonádico) lípidos y proteínas, posiblemente para utilizarse con propósitos estructurales durante la diferenciación y el desarrollo de los ovocitos y para la formación de vitelo (Epp et al., 1988; Racotta et al., 2003). Esto mismo se ha reportado en otros pectínidos, tales como Chlamys septemradiata (Ansell, 1974), Pecten maximus (Comely, 1974), Argopecten irradians concentricus (Barber & Blake, 1981) y A. irradians irradians (Epp et al., 1988). Figura 3. Variación estacional de la temperatura superficial del mar en Bahía de los Ángeles, B.C., durante el periodo de estudio. Figure 3. Seasonal variation of sea surface temperature in Bahía de los Ángeles, B.C., during the study period.

éste último presenta regímenes de temperaturas más altos (de 16.6 °C a 30.8 °C), mientras que en Laguna Ojo de Liebre y Bahía Magdalena (costa W) las temperaturas máximas no sobrepasan los 23.5 °C y 27 °C, respectivamente (Lluch-Belda et al., 2000; Arellano-Martínez et al., 2004a). Lo anterior permite suponer que N. subnodosus se reproduce en un rango de temperatura bien definido (inicia su gametogénesis entre los 17 °C y 18 °C de temperatura superficial del mar y alcanza su máxima madurez entre los 23.5 °C y 26.8 °C), independientemente del mes en que éstas se presenten en cada localidad. Por otro lado, la relación entre los índices de los tejidos somáticos y el IGS (actividad reproductiva) se ha reportado en distintos trabajos como un indicador de almacenamiento y utilización de reservas energéticas relacionado con la reproducción (Barber & Blake 1981; Villalejo-Fuerte & Ceballos-Vázquez, 1996; Barrios-Ruíz et al., 2003; Arellano-Martínez et al., 2004b). En este sentido, la correlación negativa del IGD y del IMA con el IGS, muestra una probable transferencia/utilización de reservas energéticas relacionada con la actividad reproductiva, indicada por valores bajos de los índices (IGD e IMA), principalmente durante el inicio de la gametogénesis (valores ascendentes del IGS) y durante la fase de madurez (valores máximos del IGS) de N. subnodosus en Bahía de los Ángeles B.C. En un contexto general, estos resultados concuerdan con los obtenidos por Arellano-Martínez et al. (2004b) para la misma especie en la Laguna Ojo de Liebre, B.C.S., quienes encontraron que los individuos de esta especie almacenan (en tejidos somáticos) y transfieren

Por otro lado, aunque en este estudio no se encontró una correlación significativa entre el IGS y el IM, se aprecia que hay una disminución significativa del IM durante el inicio de la fase de máxima madurez (abril-junio), lo cual sugiere una transferencia de sustratos metabólicos desde este tejido hacia la gónada en esta fase. Se ha reportado el almacenaje y movilización de sustratos metabólicos desde el músculo aductor a la gónada durante la gametogénesis, en varias especies de pectínidos tales como A. irradians (Barber & Blake, 1981; Epp et al., 1988), C. opercularis (Taylor & Venn, 1979), P. maximus (Comely, 1974), A. ventricosus (Racotta et al., 1998), A. purpuratus (Martínez, 1991), y N. subnodosus (Racotta et al., 2003; Arellano-Martínez et al., 2004b), sugiriendo que éstos son usados para la maduración final y el desove. Bayne (1976) dividió a los bivalvos en dos grupos basado sobre su estrategia o patrón gametogénico: 1) “conservativa” especies donde su gametogénesis ocurre a expensas de la energía almacenada en sus tejidos; 2) “oportunista” especies en las que la gametogénesis ocurre a expensas del alimento ingerido recientemente y cuando el fitoplancton es abundante. En este sentido, el análisis de la variación de los índices morfofisiológicos indica que es posible que en Bahía de Los Ángeles, N. subnodosus presente un ciclo de almacenamiento y transferencia de energía desde tejidos somáticos (estrategia conservativa, Bayne, 1976) hacia la gónada para soportar la gametogénesis, tal como fue reportado para la misma especie en la Laguna Ojo de Liebre, (Arellano-Martínez et al., 2004b). En contraste, los resultados obtenidos por Racotta et al. (2003) para la misma especie, pero de Bahía Magdalena, B.C.S., indican que la energía para la actividad reproductiva depende mínimamente de las reservas energéticas previamente almacenadas y el gasto energético recae sobre el alimento ingerido por el organismo

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(estrategia oportunista; Bayne, 1976). Se sabe que ambas estrategias pueden ser adoptadas por la misma especie para soportar la gametogénesis y depende de la disponibilidad de alimento en una localidad específica (Barber & Blake, 2006). No obstante, para comprobar estos resultados es necesario realizar un análisis bioquímico de los tejidos (Racotta et al., 2003; Arellano-Martínez et al., 2004b). AGRADECIMIENTOS La presente investigación se deriva de los proyectos SIP 20070215 y CONACyT52818-Q. Yee-Duarte, J. A. es becario del PIFI (IPN) y CONACyT. Los resultados que se presentan aquí son parte de su tesis de maestría. B.P. Ceballos–Vázquez y M. Arellano–Martínez reciben apoyo de SIBE (COFAA), EDI (IPN) y SNI-CONACyT. REFERENCIAS Aldrich, J. & M. Crowley. 1986. Condition and variability in Mytilus edulis (L.) from different habitats in Ireland. Aquaculture, 52: 273-286. Ansell, A. 1974. Seasonal changes in biochemical composition of the bivalve Chlamys septemradiata from the Clyde Sea area. Mar. Biol., 25: 85-99. Arellano-Martínez, M., B. P. Ceballos-Vázquez, M. Villalejo-Fuerte, F. García-Domínguez, J. F. Elorduy-Garay, A. Esliman-Salgado & I. S. Racotta. 2004a. Reproduction of the lion´s paw scallop Nodipecten subnodosus Sowerby, 1835 (Bivalvia:Pectinidae) from Laguna Ojo de Liebre, B.C.S. México. J. Shellfish Res., 23(3): 723-729. Arellano-Martínez, M., I. S. Racotta, B. P. Ceballos-Vázquez & J. F. Elorduy-Garay. 2004b. Biochemical composition, reproductive activity and food availability of the lion´s paw scallop Nodipecten subnodosus in the Laguna Ojo de Liebre, Baja California Sur, México. J. Shellfish Res., 23(1): 15-23. Barber, B. J. & N. J. Blake. 1981. Energy storage and utilization in relation to gametogenesis in Argopecten irradians

concentricus (Say). J. Exp. Mar. Biol. Ecol., 5: 121-134. Barber, B. J. & N. J. Blake. 2006. Reproductive physiology, 357-416. En: Shumway, S. E. & G. Jay Parsons (Eds.) Scallops: Biology, Ecology and Aquaculture. Elsevier, Amsterdam, 1460 p. Barrios-Ruíz, D., J. Chávez-Villalba & C. Cáceres-Martínez. 2003. Growth of Nodipecten subnodosus (Bivalvia: Pectinidae) in La Paz, Bay. Aquacult. Res., 34: 633-639. Bayne, B. L. 1976. Aspect of reproduction in bivalve mollusks, 432-448. En: Wiley, M. L. (Ed.). Estuarine Processes. Academic Press, New York, 451 p. Bricelj, V. M., J. Epp & R. E. Malouf. 1987. Intraspecific variation in reproductive and somatic growth cycles of bay scallops Argopecten irradians. Mar. Ecol Prog. Ser., 36: 123-137. Comely, C. A. 1974. Seasonal variations in the flash weights and biochemical content of the scallop Pecten maximus (L.) in the Clyde Sea Area. J. Cons. Int. Explor. Mer., 35: 281-295. Darriba, S., F. San Juan & A. Guerra. 2005. Energy storage and utilization in relation to the reproductive cycle in the razor clam Ensis arcuatus (Jeffreys, 1865). J. Mar. Sci., 62: 886-896. Dridi, S., M. S. Romdhane & M. Elcafsi. 2007. Seasonal variation in weight and biochemical composition of the Pacific oyster, Crassostrea gigas in relation to the gametogenic cycle and environmental conditions of the Bizert lagoon, Tunisia. Aquaculture, 263: 238-248. Epp, J., V. M. Bricelj & R. E. Malouf. 1988. Seasonal partitioning and utilization of energy reserves in two age classes of the Bay scallop Argopecten irradians irradians (L.) J. Exp. Mar. Biol. Ecol., 121: 113-136. Félix-Pico, E. F., M. Villalejo-Fuerte, A. Tripp-Quezada & O. Holguín-Quiñones.

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CICIMAR Oceánides, 24(2): 101-110(2009)

a-DIVERSIDAD DE DIATOMEAS EPILÍTICAS DEL OASIS DE SAN IGNACIO BAJA CALIFORNIA SUR, MÉXICO López Fuerte, F. O. Universidad Autónoma de Baja California Sur, Laboratorio de Sistemas Arrecífales. Dpto. de Economía. La Paz, B. C. S., México. 23080. email: folopez@uabcs.mx. Resumen. Se proporciona el primer registro de diatomeas bentónicas epilíticas para el oasis de San Ignacio, B. C. S., México. Se realizaron dos muestreos (enero de 2007 y en julio de 2008) tratando de representar las épocas de invierno y verano. No obstante que los datos de temperatura fueron puntuales, se observaron diferencias estadísticas (p< 0.05) entre meses, lo que permitió discriminar verano e invierno. Los valores de pH y conductividad no mostraron diferencias estadísticas (p>0.05) entre épocas. Se reconocieron un total de 73 taxa de diatomeas epilíticas a niveles de especie, variedad y forma. De éstos, 66 se registraron en julio y 37 en enero; 29 taxa estuvieron presentes en ambos muestreos, 37 sólo en julio y 7 en enero. La mayor riqueza de especies se registró en julio (S=47) y la mínima en enero (S=14). En verano se registraron los valores más elevados de diversidad (H'=4.06, S=39); mientras que en enero se obtuvo el valor mínimo (H'=2.42, S=13). Las diferencias entre los valores de diversidad según la época de muestreo fueron significativas (p>0.05). La mayoría de las diatomeas identificadas fueron pennadas: 69 taxa (en 32 géneros); sólo 5 especies de los géneros Cyclotella y Stephanodiscus fueron centrales. La especie más frecuente y abundante fue Denticula kuetzingii que estuvo presente en todos los sitios de muestreo en ambas temporadas, con una abundancia relativa superior al 50%. Los análisis de similitud (cualitativos/cuantitativos) permitieron reconocer una asociación representativa del verano y otra del invierno.

Palabras clave: diatomeas epilíticas, oasis, Península de B. C., San Ignacio, diversidad.

a-diversity of epilithic diatoms in the San Ignacio oasis Baja California Sur, México Abstract. The first record of benthic epilithic diatoms for the oasis of San Ignacio, B.C.S., México is presented. Two samplings were conducted in January 2007 and July 2008 in order to represent winter and summer conditions, respectively. Although temperature data were punctual, statistical differences were noted between months (p<0.05), which allow discrimination of summer and winter. Conductivity and pH values did not show statistical differences (p> 0.05). A total of 73 taxa of epilithic diatoms were identified including species, variety and form levels. From these, 66 were recorded in July and 37 in January. Twenty nine taxa occurred in both sampling periods, 37 only in July and 7 in January only. Highest species richness was observed in July (S=47) and the lowest in January (S=14). Highest species diversity values occurred in summer (H´= 4.06, S=39), whilst January showed the lowest diversity (H´= 2.42, S= 13). Species diversity values were statistically different (p>0.05) between sampling periods. Most of the identified diatoms were pennate forms: 69 taxa (32 genera), while only five species of Cyclotella and Stephanodiscus were centric forms. The most frequent and abundant taxon was Denticula kuetzingii which occurred in all sampling sites and both periods with a relative abundance higher than 50%. Qualitative and quantitative similarity analyses allow the definition of two associations, one for summer and another for winter conditions.

Keywords: epilithic diatoms, oasis, Baja California Peninsula, San Ignacio, diversity. López Fuerte, F. O. 2009. a-diversidad de diatomeas epilíticas del oasis de San Ignacio Baja California Sur, México. CICIMAR Oceánides, 24(2): 101-110.

INTRODUCCIÓN La evolución geomorfológica e hidroclimática de la Península de Baja California ha producido una transformación ecológica radical Fecha de recepción: 21 de agosto, 2009

pasando de un hábitat con vegetación propia de condiciones húmedas (mésica) hacia un matorral xerófito (Axelrod, 1979). Esta evolución trajo como consecuencia la formación de Fecha de aceptación: 30 de septiembre, 2009

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una serie de relictos mésicos que actualmente se encuentran en las porciones altas de los macizos montañosos, o bien como oasis (Arriaga, 1997). Estos cuerpos de agua dulce son escasos y se caracterizan por una discontinuidad en su distribución; han sido evaluados y diferenciados ecológicamente sobre la base de distintos grupos biológicos que albergan (Arriaga & Rodríguez-Estrella, 1997). Aunque el número de investigaciones realizadas en los oasis de la península es considerable, solamente Siqueiros-Beltrones (2001) ha abordado el estudio de las algas, particularmente el de las diatomeas. No obstante, que éstas constituyen uno de los grupos taxonómicos autotróficos dominantes en los ambientes dulceacuícolas y es de los más utilizados en los países desarrollados para caracterizar ambientalmente la calidad de las aguas (bioindicadores). Asimismo, la casi nula investigación sobre la composición, diversidad, distribución y variación estacional de las diatomeas bentónicas en estos ambientes, dificulta la comparación entre los oasis y retrasa su posible utilización en la caracterización y monitoreo de la calidad del agua, como se hace en otras regiones. La falta de conocimiento sobre las diatomeas de los oasis de Baja California Sur obliga a su estudio, por lo que el presente trabajo tiene como objetivo describir la composición florística, diversidad y la estructura de la comunidad de diatomeas epilíticas del oasis (manantial) de San Ignacio, Baja California Sur, México. MATERIALES Y MÉTODOS El oasis de San Ignacio (27° 17' 49" N y 112° 52" 57 W) (Fig. 1) es un cuerpo de agua dulce permanente con una extensión aproximada de 2.69 km2. Presenta condiciones microclimáticas diferentes al de su entorno, dadas por la presencia de vegetación que en conjunto determinan que las variables ambientales (temperatura, humedad, viento, entre otras) se comporten de manera casi constante (Coria, 1997). El tipo de clima es BWhs(x')(e), muy árido, semicálido con lluvias de verano y con una oscilación térmica extremosa. El manantial que da origen al cuerpo del oasis brota en el basamento del arroyo San Ignacio y fluye siguiendo la topografía del cañón para filtrarse en el sustrato arenoso, antes de llegar al borde del desierto del Vizcaíno (Diaz & Troyo, 1997). La velocidad de la corriente del agua que brota del manantial es ba-

Figura 1. Localización del oasis de San Ignacio. * Punto de muestreo. Figure 2. Location of San Ignacio Oasis. *Sampling point.

ja, dado que esta se trasfiere de una poza a otra y las condiciones hidrológicas son particulares y diferentes al resto del cuerpo del oasis, el cual se mantiene debido a una represa. Se realizaron dos muestreos tratando de representar condiciones de verano, en julio de 2007 y de invierno, en enero del 2008, estableciendo siete y cuatro sitios de muestreo respectivamente. Los sitios se eligieron con base en la presencia de rocas (>20 cm de largo). Se raspó con un cepillo una superficie de aproximadamente 5 cm2 de roca, obteniéndose alrededor de 50 ml de muestra que se colocó en viales previamente etiquetados. Las muestras fueron guardadas en hielo y obscuridad para ser transportadas al laboratorio. Después de una observación in vivo bajo el microscopio para asegurar la presencia de diatomeas, éstas se preservaron en alcohol y se refrigeraron. La limpieza de las frústulas y su montaje permanente se realizaron siguiendo el método sugerido por Siqueiros-Beltrones (2002), en el cual las muestras son sometidas a digestión de la materia orgánica en el interior (y exterior) de las valvas mediante oxidación, usando un mezcla de; muestra- ácido nítrico-etanol comercial, en proporción de 1: 3: 1. Una vez lavadas (pH >6), las valvas limpias pasaron al proceso de montado permanente para el cual se utilizó Pleurax (IR = 1.7) como medio de montaje. Las valvas de las diatomeas fueron contadas en campos visuales verticales (lineales) a una magnificación de 1000X usando un microscopio óptico Zeiss con contraste de fases y un micrómetro adaptado; se contaron

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no menos de 1000 valvas por sitio. Para la identificación se utilizó literatura especializada: Hustedt (1930, 1961-1966); Krammer & Lange-Bertalot (1986; 1988; 1991), Simonsen (1987) y Round et al. (1990). Los datos físicos y químicos se obtuvieron in situ para cada sitio. El pH y la temperatura del agua se midieron con un potenciómetro pHTestr10 (intervalo de pH de 1.0 a 15.0, resolución de 0.1), con termómetro integrado. Para medir la conductividad se utilizó un conductímetro ECTestr11 (intervalo 2000 mS/cm a 20.00 mS/cm, resolución de 0.10 a 10). Para cada especie se calculó la proporción de sitios en los cuales una especie estuvo presente (frecuencia porcentual) y el porcentaje de abundancia relativa (suma total de las valvas por especie entre el total de valvas contabilizadas) (Apéndice). La diversidad de especies se midió con los índices de Shannon (H´) y Simpson (1-l), mientras que para la uniformidad de su distribución se aplicó el índice de equidad de Pielou (J´). Para medir la semejanza entre las asociaciones de diatomeas las muestras fueron comparadas con base en datos de presencia/ausencia de especies (índice de Jaccard) y de abundancias relativas (Bray Curtis) (Magurran, 1988). Los cálculos se realizaron con los programas BioDiversity Professional © (McAleece, 1997) y Primer V. 5 (Clarke & Warwick, 1994). De acuerdo con Stephenson y Cook (1980) y De la Cruz-Agüero (1994), se recomienda poner especial atención sobre los descriptores con baja frecuencia, representados en este caso por los taxa que aparecieron una vez en un sólo sitio y/o valores extremos como Denticula kuetzingii, cuya frecuencia de ocurrencia fue de 100% en ambos muestreos, su abundancia de 3427 valvas en verano y 2571 en invierno, lo cual representó el 53% del total de las valvas contabilizadas. De acuerdo con lo anterior, esta especie se consideró como valor extremo y no se tomó en cuenta para los análisis numéricos. Los datos de temperatura, pH y de conductividad se compararon estadísticamente mediante una prueba no paramétrica de Mann-Whitney (Snedecor & Cochran, 1981). Los valores de diversidad (H´ y 1-l) se compararon mediante la prueba de Kruskal-Wallis, donde Ho = no existen diferencias significativas entre dichos valores por fecha de mues-

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treo; para ello se usó el programa Statistica v. 8 (StatSoft, 2007). RESULTADOS Los valores de las variables físicas y químicas (Tabla 1) muestran una temperatura superficial mínima del agua en enero (21 °C) y máxima en julio (29.6 °C); el promedio de temperatura para enero fue de 25.6 °C, mientras que en julio fue de 28.9 °C. No obstante que los datos de temperatura fueron puntuales, se observaron diferencias estadísticas entre meses (p<0.05), lo cual permite discriminar verano e invierno. En cuanto al pH, los valores para ambos meses indican una condición neutral, obteniéndose un valor máximo de 7.4 en enero y uno mínimo de 6.9 en julio. Los valores de conductividad muestran que el agua es dura (>1000 mS), indicando que presenta altos niveles de minerales. En cuanto a los valores Tabla 1. Temperatura (ºC), pH y conductividad (µS) de cada sitio por época de muestreo del oasis de San Ignacio. Table 2. Temperature (°C), pH and conductivity (µS) for each site and sampling season in the San Ignacio oasis. SITIO 1 2 3 4 5 6 7

VERANO °C pH mS 29.1 7.1 1010 29.6 6.9 1080 29.2 6.9 1070 29.2 6.9 1070 27.4 7.0 1050 28.7 6.9 1070 28.9 6.9 1050

INVIERNO °C pH mS 26.6 7.3 1010 27.3 7.2 1010 21.4 7.4 1060 27 7.2 1000

de pH y conductividad no mostraron diferencias en términos estadísticos (p>0.05) entre épocas. Flora diatomológica Un total de 73 especies de diatomeas epilíticas fueron identificadas en el oasis de San Ignacio (Apéndice), de las cuales 66 se encontraron en julio y 37 en enero. Sólo 29 de los 73 taxa estuvieron presentes en ambos muestreos, mientras que 37 se presentaron exclusivamente en julio y siete en enero. La riqueza de especies entre épocas fue distinta; en verano varió entre 25 y 47 especies, mientras que en invierno entre 14 y 29. La mayoría de las diatomeas identificadas fueron pennadas, representadas por 69 especies incluidas en 32 géneros; mientras que las

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diatomeas centrales estuvieron representadas por cinco especies de los géneros Cyclotella y Stephanodiscus. Entre éstas, Cyclotella pseudostelligera sobresalió con un porcentaje de abundancia relativa de 3.9 % y un 86 % de frecuencia de ocurrencia, lo cual resulta elevado si se compara con otras formas pennadas como Amphora copulata, Planothidium frequentissimum y Sellaphora pupula con amplia frecuencia de ocurrencia (100%). Los géneros mejor representados en cuanto al número de especies fueron, Nitzschia (16), Navicula (6), Diploneis (4) y Cyclotella (4). Tanto a nivel de género como de especie las mayores variaciones se registraron en verano (Apéndice). La especie más frecuente y abundante fue Denticula kuetzingii que estuvo presente en todos los sitios de muestreo en ambas temporadas, con una abundancia relativa superior al 50%. Otros taxa frecuentes fueron Achnanthidium minutissimum, A. exiguum, Navicula namibica y Amphora acutiuscula. Estructura de la comunidad Las relaciones entre frecuencia y abundancia relativa de las principales especies de diatomeas muestran que en la mayoría de los casos las especies con los valores más elevados de frecuencia de aparición fueron las más abundantes (Apéndice). En el verano, sólo 30 especies (39%) estuvieron presentes en el 50% o más de los sitios de muestreo, 24 (36%) se hallaron exclusivamente en un sitio de muestreo. En esta época, se observaron muchas especies poco abundantes pero frecuentes, por ejemplo; Pseudostaurosira brevistriata var. inflata, Gomphonema parvulum, Nitzschia frustulum y Planothidium frequentissimum. En invierno sólo tres taxa presentaron baja abundancia con una elevada frecuencia: Amphora acutiuscula, Nitzschia amphibia f. frauenfeldii y Sellaphora pupula; no obstante, en el verano estos taxa obtuvieron abundancias elevadas. En verano, en términos de abundancia y frecuencia de ocurrencia, Achnanthidium exiguum, A. minutissimum, Amphora acutiuscula, Sellaphora pupula, Nitzschia palea, N. amphibia f. frauenfeldii, N. amphibioides y Pseudostaurosira brevistriata var. inflata, codominaron la comunidad de diatomeas. Por otra parte, en invierno las especies dominantes y codominantes fueron, Achnanthidium minutissimum, A. exiguum y N. amphibioides; en términos

cualitativos fueron más comunes en invierno que en verano. Mientras que Denticula kuetzingii dominó en ambas épocas. Los valores de diversidad H´ y 1-l pueden considerarse elevados, tanto espacial, como temporalmente (Tabla 2). En verano se registraron los valores más elevados de diversidad y riqueza (H'=4.06, S=39); mientras que en enero se obtuvo el valor mínimo de riqueza (H'=2.42, S=13). En lo que respecta a los valores de diversidad, estadísticamente las diferencias entre épocas de muestreo resultan significativas (p>0.05). Estructuralmente, la elevada diversidad de especies en verano responde a una combinación del número de especies (S), elevada equidad y baja dominancia; aunque la baja riqueza parece ser el factor que más afecta la baja diversidad en invierno. Estacionalmente, la estructura comunitaria presentó variaciones, como lo muestran los análisis de similitud. Las diferencias más claras entre épocas están representadas por la presencia/ausencia de las 38 especies exclusivas del verano. Así, el uso del índice de Jaccard muestra que las comunidades de diatomeas de verano difieren en más del 50% con respecto a las del invierno (Fig. 2a). Por otro lado, el índice de Bray Curtis, muestra un patrón similar al de Jaccard, es decir, permite hacer una diferenciación entre épocas, aunque a un valor menor al 50% de similitud (Fig. 2b). Tabla 2. Valores calculados de los parámetros utilizados para determinar la estructura de la comunidad en las taxocenosis de diatomeas por época y sitio de muestreo del oasis de San Ignacio. S: Riqueza de especies; H': Diversidad de especies (Shannon); J': Equitatibilidad; 1-l : Diversidad de especies (Simpson); l: Dominancia. Table 2. Calculated values of the parameters used for the determination of the community structure in the diatom taxocoenosis by season and sampling site in San Ignacio oasis. S: Species richness; H': Species diversity (Shannon); J': Equitability; 1-l : Species diversity (Simpson); l: Dominance. SITIO

VERANO S

1-l

INVIERNO 1-l

39 3.93 0.74 0.87 0.13 20 2.94 0.68 0.8

0.2

32 3.75 0.75 0.87 0.13 26 2.63 0.56 0.69 0.31

27 2.82 0.59 0.73 0.27 20 2.56 0.59 0.68 0.32

29 3.76 0.77 0.89 0.11 13 2.42 0.66 0.69 0.31

24 3.43 0.75 0.88 0.12

29 2.81 0.58 0.76 0.24

36 4.06 0.78 0.92 0.08

H’

J’

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Figura 2. Agrupamiento de diatomeas epilíticas basado en el índice de similitud de Jaccard (a) y Bray Curtis (b) por sitio y época de muestreo del oasis de San Ignacio. Figure 2. Epilithic diatom clusters based on the similarity indeces of Jaccard (a) and Bray Curtis (b) by sampling season and site in the San Ignacio oasis.

Dicha información permite reconocer asociaciones representativas de verano e invierno, tanto en términos cualitativos como cuantitativos, así como hipotetizar sobre la presencia de una diatomoflora representativa de la época fría y cálida. DISCUSIÓN El conocimiento en general de la flora diatomológica en México es muy pobre y más aún el de aguas continentales, por lo que es muy frecuente que cuando se emprende un estudio florístico se aporte un número importante de novedades, no sólo para el lugar en que se realicen, sino para el país en si. En el único trabajo previo sobre diatomeas de agua dulce de Baja California Sur se registraron 87 taxa para cuatro oasis (Siqueiros-Beltrones, 2001), por lo que las 73 especies determina-

das solo en el oasis de San Ignacio resulta ser elevado. Llama la atención que de las 87 especies previamente reportadas en el trabajo de Siqueiros-Beltrones (2001), sólo 11 se hayan registrado en el oasis de San Ignacio. Según dicho autor Denticula kuetzingii también fue muy abundante en el oasis de San Luis Gonzága, en donde se observó formando agregados de una coloración rojiza en los sedimentos. Asimismo, el bajo número de taxa en común entre el oasis de San Ignacio con los otros oasis estudiados por Siqueiros-Beltrones (2001), permite entrever una diferenciación taxonómica que podría estar marcando un gradiente latitudinal, ya que el oasis de San Ignacio es uno de los más norteños de Baja California Sur. No obstante, es necesario completar el inventario florístico de la parte sur y centro de B. C. S., para tener más elementos

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y poder hacer una diferenciación biogeográfica sustentada, recurriendo a otros parámetros, v. gr., beta diversidad. En lo que respecta a la distribución taxonómica y la estructura de las asociaciones de las diatomeas del oasis de San Ignacio, coincide con lo esperado teóricamente, es decir, una o dos especies dominan la comunidad en términos de abundancia y frecuencia de ocurrencia, pocas especies son codominantes y una gran cantidad de especies presentarían abundancias relativas menores al 1% con frecuencia de ocurrencia muy baja (se registran por lo general una vez) (Kelly, 2000; Bernadette et al., 2008). Este patrón se ha determinado igualmente para comunidades de diatomeas marinas en diferentes sustratos estudiados en Baja California Sur (Siqueiros-Beltrones, 2000; Siqueiros-Beltrones et al., 2005; López-Fuerte & Siqueiros-Beltrones, 2006). Atribuir a la temperatura la diferenciación de una asociación representativa de invierno y otra de verano en términos cualitativos y cuantitativos sería aventurado, no obstante que se ha determinado un gradiente estacional relacionado con la temperatura y cambios bruscos en la conductividad y en el oxígeno disuelto (Israde et al., 2008). Sin embargo, se puede llegar a una mejor aproximación complementando los análisis con la inclusión de otras variables i. e., irradiancia, nutrientes, sólidos disueltos, etc. Además de los factores físicos y químicos, existen factores biológicos que se deben considerar, como lo es el efecto de la interacción biológica con los herbívoros, debido a la potencial eficiencia diferencial de la herbivoría en el consumo afectando la composición y modulación de la estructura comunitaria (Cuker, 1983). Los efectos de las interacciones biológicas se han demostrado en ambientes con bajo flujo de corrientes (Menge & Sutherland, 1987; Rosemond et al., 2000), condición que se presenta en la cabecera del oasis de San Ignacio, por lo que habría de considerarse esta condición para la explicación de las variaciones en composición y abundancia. El registro abundante y presencia constante de taxa pequeños (Denticula kuetzingii, Achnanthidium minutissimum, A. exiguum y Navicula namibica) que son fisiológicamente más activas que las células grandes, permite inferir la posible ventaja de éstos sobre taxa grandes vs. consumidores; lo anterior bajo la premisa de que, cuando la interacción biótica

principal es la herbivoría, las especies pequeñas aunque pueden ser dominantes en términos de abundancia y frecuencia, serán por su tamaño competitivamente inferiores en términos de productividad, pero menos vulnerables a ser consumidas (Rosemond et al., 2000; Ulrich, 2000). El que la composición y el dominio de la comunidad de diatomeas epilíticas sea de formas principalmente pequeñas puede responder a que éstas poseen mecanismos débiles para sujetarse al substrato y pueden ser desprendidas con relativa facilidad con el aumento en la velocidad de la corriente o incremento del caudal (Lamb & Lowe, 1987). El manantial, al poseer una corriente constante y con baja velocidad debido a la existencia de pozas, les confiere estabilidad hidrológica, resultando en un ambiente adecuado para el desarrollo y permanencia de comunidades de este tipo de taxa que utilizan mecanismos de fijación no muy desarrollados; aunque se ha comprobado que taxa pequeños pueden desarrollar mecanismos de adherencia lo suficientemente eficientes para soportar aumentos en el caudal o la velocidad de la corriente, i. e., Achnanthidium minutissimum (Ghosh & Gaur, 1998). No obstante, se ha determinado que especies grandes como Fragilaria capucina prefieren también desarrollarse bajo condiciones de baja velocidad de corriente (Passy, 2001). Algunas especies de diatomeas que dominan la estructura de la comunidad han sido utilizadas como indicadores biológicos, i. e., Achnanthidium minutissimum, A. exiguum, Nitzschia amphibia (Wehr et al., 2003). Basándonos en la presencia, abundancia, complicación taxonómica e incertidumbre en la información taxonómica de dichos taxa, es difícil hacer inferencias sobre la calidad del agua del oasis de San Ignacio. Por otra parte, las medidas de la estructura comunitaria y la información autoecológica, dejan entrever que, por lo menos, la cabecera del oasis de San Ignacio es un cuerpo de agua limpio. Es recomendable el monitoreo constante de la diatomoflora del oasis de San Ignacio, con el fin de poder detectar cambios en la estructura de las asociaciones que puedan representar condiciones de alteración. AGRADECIMIENTOS Se agradece al CONACYT por la beca otorgada. Así como al Instituto Politécnico Na-

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cional el apoyo brindado a través del proyecto IPN-SIP: 20070424. Diatomeas bentónicas de los oasis de Baja California Sur; florística y grupos ecológicos. También se reconoce a la CONABIO (Proyecto HJ032) los recursos para realizar los muestreos. Especial agradecimiento a David A. Siqueiros Beltrones por la revisión y comentarios del manuscrito y a dos revisores anónimos. REFERENCIAS Arriaga, L. 1997. Introducción. 1-4 pp. En: Arriaga, L. & Rodríguez-Estrella, R. (Ed.). Los oasis de la Península de Baja California. Publ. 13, CIBNOR, S. C., La Paz, México, 292 p. Arriaga, L. & R. Rodríguez-Estrella, (Ed.). 1997. Los oasis de la Península de Baja California. Publ. 13, CIBNOR, S. C., La Paz, México, 292 p. Axelrod, D. I. 1979. Age and origin of the Sonoran Desert vegetation. Occasional Pappers of the California Academy of Sciences, 132: 1-74. Coria, B. R. 1997. Climatología. 27-34, En: Arriaga, L. & Rodríguez-Estrella, R. (Ed.). Los oasis de la Península de Baja California. Publ. 13, CIBNOR, S. C., La Paz, México, 292 p. Bernadette, N., Chatham, T. & J. Harrington. 2008. Benthic diatoms of the river Deel: diversity and community structure. Biology and environment, 108(1): 29-42. Clarke, K. R. & R. M. Warwick.1994. Changes in marine communities: an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, Plymouth. 144 p. Cuker, B. 1983. Grazing and nutrient interactions in controlling the activity and composition of the epilithic algal community of an arctic lake. Limnol. Oceanogr., 28(1): 133-141. De la Cruz-Agüero, G. 1994. Sistema de análisis de comunidades. Versión 3.0. Departamento de Pesquerías y Biología Marina. CICMAR-IPN. México. 99 pp.

Diaz, S. & Troyo, E. 1997. Balance Hidrologico y Análisis de la Aridez. 35-49, En:Arria ga, L. & Ro drí guez-Estre lla, R. (Ed.). Los oasis de la Península de Baja California. Publ. 13, CIBNOR, S. C., La Paz, México, 292 p. Ghosh, M. & J. Gaur. 1998. Current velocity and the establishment of stream algal periphyton communities. Aquat. Bot., 60(1): 1-10. Hustedt, F. 1930. Bacillariophyta (Diatomeae). En: Pascher, A. Die Susswasserflora Mitteleuropas. Otto Koeltz Science Pub. Jena. 466 p. Hustedt, F. 1961-66. Die Kieselalgen Deutschland, Österreichs und der Schweiz. en: Rabenhorst, L. (Ed.). Kryptogamen-Flora von Deutschland, Österreich und der Schweiz, VII Band, III Teil. Koeltz Scientific Books (Rep. 1991). Leipzig. 816 p. Israde A. I., G. V., Segura & N. Abarca. 2008. Freshwater diatoms in Lerma River, Central México and their use for Water Quality Assessment. En: NALMS. (Ed.): Lake Management in a Changing Environment. 28th International Symposium of the North American Lake Management Society. Lake Louise, Alberta, Canada. 100 p. Kelly, M. G. 2000 Identification of Common Benthic Diatoms in Rivers. Field Studies, 9: 583-700. Kramer, K. & H. Lange-Bertalot. 1986. Bacillariophyceae, 1 Teil: Naviculaceae. Band 2/1. SüBwasserflora von Mitteleuropa (H. Ettl, J. Gerloff und D. Mollenhauer, eds), Gustav Fischer. Sttutgart, 876 p. Kramer, K. & H. Lange-Bertalot. 1988. Bacillariophyceae, 2 Teil: Epithemiaceae, Surirellaceae. Band 2/2. von SuBwasserflora von Mitteleuropa (H. Ettl, J. Gerloff y D. Mollenhauer, eds), Fischer-Stuttgart, Alemania, 536 p. Kramer, K. & H. Lange-Bertalot. 1991. Bacillariophyceae, 3 Teil: Centrales, Fragilariaceae, Eunotiaceae. Band 2/3 von

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Lamb M. A. & R. Lowe 1987. Effects of current velocity on. the physical structuring of diatom (Bacillariophyceae) communities. Ohio J. Sci., 87(3): 72-78.

Siqueiros-Beltrones, D. A. 2000. Benthic diatoms associated to abalone (Haliotis spp.) on a rocky substratum from Isla Magdalena, B. C. S., México. Oceánides, 15(1): 35-46

López-Fuerte, F. O. & D. A. Siqueiros-Beltrones. 2006. Distribución y estructura de asociaciones de diatomeas en sedimentos de un sistema de manglar. Hidrobiológica, 16(1): 23-33 Magurran, A. E. 1988. Ecological diversity and its measurement. Princenton. University Press. Princeton. 179 p. McAleece, N. 1997. Biodiversity professional beta 1. Version 2. The Natural History Museum & The Scottish Association for Marine Science. http: //www. nhm. ac. uk/zoology/bdpro. Menge B. A. & P. J. Sutherland. 1987. Community Regulation: Variation in Disturbance, Competition, and Predation in Relation to Environmental Stress and Recruitment. Am. Nat., 130(5): 730-757. Passy, S. 2001. Spatial paradigms of lotic diatom distribution: A landscape ecology perspective. J. Phycol., 37: 370-378. Rosemond A. D., P. J. Mulholland & S. H. Brawley. 2000. Seasonally shifting limitation of stream periphyton: Response of algal populations and assemblage biomass and productivity to variation in light, nutrients, and herbivores. Can. J. Fish Aquat. Sci., 57(1): 66-75. Round, F. E., R. M. Crawford & D. G. Mann. 1990. The diatoms. Biology and morphology of the genera. Cambridge University Press. Cambridge. 747 p.

Siqueiros-Beltrones, D. A. 2001. Benthic diatoms from oases in the southern Baja Peninsula. Abstracts of the 16th North American Diatom Symposium. 42 p. Siqueiros-Beltrones, D. A. 2002. Diatomeas bentónicas de la península de Baja California; diversidad y potencial ecológico. CICIMAR-IPN-UABCS. La Paz. 102 p. Siqueiros-Beltrones, D.A., F.O. López-Fuerte & I. Gárate-Lizárraga. 2005. Structure of diatom assemblages living on prop roots of the red mangrove Rhizophora mangle L. from the West coast of Baja California Sur, México. Pacific Science, 59(1): 79-96. Snedecor, G. W. & W. G. Cochran. 1989. Statistical Methods, Eighth Edition. Iowa State University Press. Ames., 503 p. StatSoft, Inc. 2007. STATISTICA (data analysis software system), version 8.0. www.statsoft.com. Stephenson, W. & S. D. Cook. 1980. Elimination of species before cluster analysis. Aust. J. Ecol., 5: 263-273. Stirling, G. & B. Wilsey. 2001. Empirical relationships between species richness, evenness, and proportional diversity. Am. Nat., 158(3): 286-299. Ulrich S. 2000. Benthic microalgal diversity enhanced by spatial heterogeneity of grazing. Oecologia, 122(2): 284-287. Wehr, J. D., Thorp, J. & R. G. Sheath. 2003. Freshwater algae of North America. Ecology and Classification. Academic Press, USA. 917 p.

ALFA DIVERSIDAD EN UN OASIS

109

Apéndice. Diatomeas epilíticas encontradas en el oasis de San Ignacio, BCS. %AR = Porcentaje de Abundancia Relativa ; %FO = Porcentaje de Frecuencia de Ocurrencia por época. VERANO TAXA

%AR

INVIERNO

%FO

%AR

%FO

1. Achnanthes inflatagrandis Metzeltin, Lange-Bertalot & García-Rodriguez 0.132

0.064

2. Achnanthidium exiguum (Grunow) Czarnecki.

20.101

100

10.039

100

3. Achnanthidium minutissimum (Kützing) Czarnecki

9.733

100

50.064

100

4. Amphora acutiuscula Kützing

7.458

100

2.831

100

5. Amphora copulata (Kützing) Schoeman & Archibald

1.693

100

0.064

6. Amphora pseudoholsatica Nagumo & Kobayasi

0.106

7. Aulacoseira granulata var. angustissima (O. Müller) Simonsen

0.026

8. Bacillaria paradoxa Gmelin

0.899

100

0.257

9. Brachysira steinitziae Metzeltin & Lange-Bertalot

0.026

10. Caloneis bacillum (Grunow) Cleve

0.846

0.515

11. Cocconeis placentula Ehrenberg

0.026

12. Craticula ambigua (Ehrenberg) D. G. Mann

0.053

13. Cyclotella atomus Hustedt

1.111

100

0.129

14. Cyclotella meneghiniana Kützing

0.608

15. Cyclotella pseudostelligera Hustedt

3.861

0.064

0.322

0.064

16. Cyclotella stelligera (Cleve & Grunow) van Heurck 17. Cymbella cymbiformis C. Agardh

0.053

18. Cymbella hustedtii Krasske

2.618

19. Cymbella mexicana (Ehrenberg) Cleve

0.053

20. Cymbella sp.

0.476

21. Denticula valida (Pedicino) Grunow

0.503

22. Diadesmis confervacea Kützing

0.132

24. Diploneis oblongella (Nägeli) Cleve

0.079

25. Diploneis suborbicularis (Gregory) Cleve

0.026

26. Diploneis subovalis Cleve

0.106

27. Encyonopsis microcephala (Grunow) Krammer

0.079

28. Eunotia praerupta Ehrenberg

0.053

29. Fallacia pygmaea (Kützing) Stickle & Mann

0.026

30. Fragilaria fasciculata (C. Agardh) Lange-Bertalot

0.053

29 1.351

32. Gomphonema affine Kützing

1.613

100

7.079

100

33. Gomphonema parvulum (Kützing) Kützing

1.746

100

2.381

34. Gomphosphenia oahuensis (Hustedt) Lange-Bertalot

0.820

35. Mastogloia elliptica (Agardh) Cleve

0.026

36. Navicula aquaedurue Lange-Bertalot

2.222

100

0.644

37. Navicula cryptotenelloides Lange-Bertalot

0.053

38. Navicula gregaria Donkin

0.291

39. Navicula longicephala var. longicephala Hustedt

0.026

40. Navicula namibica Lange-Bertalot

11.029

71 0.129

42. Navicymbula pusilla (Grunow) Krammer

0.079

0.257

43. Nitzschia amphibia f. frauenfeldii (Grunow) Lange-Bertalot

4.708

100

3.153

100

7.593

100

6.821

100

23. Diploneis decipens var. parallela Cleve

31. Fragilaria ulna var. acus (Kützing) Lange-Bertalot

41. Navicula rostellata Kützing

44. Nitzschia amphibia Grunow 45. Nitzschia amphibioides Hustedt

3.042

100

110

LÓPEZ-FUERTE

Apéndice. Cont. %AR = Porcentaje de Abundancia Relativa y %FO = Porcentaje de Frecuencia de Ocurrencia por época. VERANO TAXA

%AR

%FO

46. Nitzschia calida Grunow

0.026

47. Nitzschia clausii Hantzsch

0.026

48. Nitzschia compressa (Bailey) Boyer var. compressa

0.264

49. Nitzschia constricta (Kützing) Ralfs

0.132

50. Nitzschia dissipata (Kützing) Grunow

0.212

51. Nitzschia frustulum (Kützing) Grunow

0.820

INVIERNO %AR

%FO

0.064

100

0.708

0.064

52. Nitzschia fusiformis Grunow 53. Nitzschia levidensis (W. Smith) Grunow

0.026

54. Nitzschia linearis (Agardh ex W. Smith) W. Smith

0.026

55. Nitzschia microcephala Grunow

0.106

0.129

56. Nitzschia palea (Kützing) W. Smith

5.871

100

0.129

57. Nitzschia sinuata var. delognei (Grunow) Lange-Bertalot

0.132

58. Opephora krumbeinii Witkowski, Witak & Stachura

2.989

0.901

59. Opephora pacifica Grunow

0.026

60. Paralia sulcata (Ehrenberg) Cleve

0.026

61. Pinnularia gibba Ehrenberg

0.026

62. Pinnularia neomajor Krammer

0.053

63. Pinnularia viridifomis Krammer

0.026

14 0.386

1.416

64. Planothidium frequentissimum (Lange-Bertalot) Round & L. Bukhtiyarova 1.455

100

65. Psammothidium lauenburgianum (Hustedt) Bukhtiyarova & Round 66. Pseudostaurosira brevistriata var. inflata (Pantocsek) Hartley et al.

2.380

100

0.965

67. Rhopalodia gibberula (Ehrenberg) O. Müller

0.132

0.064

68. Sellaphora pupula (Kützing) Mereschkovsky

6.268

100

0.515

100

69. Stephanodiscus minutulus (Kützing) Cleve & Möller

0.238

57 0.515

71. Synedra ulna var. danica (Kützing) Grunow

0.053

72. Terpsinoe musica Ehrenberg

0.053

0.064

73. Ulnaria ulna (Nitzsch) Compère

2.036

100

0.129

70. Synedra acus var. angustissima Grunow

ARTÍCULOS DE REVISIÓN

CICIMAR Oceánides, 24(2): 113-127(2009)

INDICADORES BIOLÓGICOS EN EL AMBIENTE PELÁGICO Jiménez-Rosenberg, S. P. A. & G. Aceves-Medina Departamento de Plancton y Ecología Marina Centro Interdisciplinario de Ciencias Marinas del Instituto Politécnico Nacional. Av. IPN s/n, Col. Playa Palo de Sta. Rita, La Paz, Baja California Sur, CP 23090. email: srosenbe@ipn.mx, gaceves@ipn.mx. RESUMEN. La evaluación de los ecosistemas con respecto a su nivel estabilidad y las causas de su cambio son elementos indispensables para el manejo y regulación de sus recursos. Para tal efecto, los indicadores biológicos se han convertido en un componente vital, ya que están diseñados para proveer señales sobre eventos a gran escala que ocurren en el ambiente y para hacer perceptibles tendencias o fenómenos no detectables fácilmente. Sin embargo, se deben hacer ciertas consideraciones en la selección y el uso de los indicadores biológicos adecuados y entender que estos no deben de ser empleados como sustitutos de otros procedimientos de evaluación ambiental e investigación. Comunidades y organismos de diferentes niveles tróficos en el ambiente marino pelágico han mostrado su utilidad como indicadores biológicos, empero el valor de la información que aportan está en función de la posibilidad de ser extrapolada a diferentes escalas de espacio y/o tiempo, así como de la experiencia y objetividad del investigador. Las series de tiempo largas provenientes de las pesquerías y programas de investigación diversos (muchos de ellos enfocados a las comunidades planctónicas), han mostrado su utilidad para ser utilizadas como indicadores biológicos. En consecuencia, la mayor parte de la investigación encaminada a conocer la variabilidad ambiental se enfoca sobre estos organismos.

Palabras clave: Ambiente pelágico, variabilidad, indicador biológico. Biological indicators in the pelagic enviroment ABSTRACT. Ecosystem evaluation regarding stability and causes of change are indispensable elements for the management and regulation of its resources. For this reason, biological indicators are a vital component since they are designed to provide signals about large scale events that occur in the environment, making trends or events perceptible that otherwise can not be detected easily. Nevertheless, considerations have to be made in the selection and use of adequate biological indicators, and to understand that they should not be used as a substitute of other procedures of environmental evaluation and investigation. In the marine pelagic environment, communities and organisms from different trophic levels have shown their usefulness as biological indicators, although the value of the information that they provide is a function of the possibility to extrapolate this information to different scales of space and time, as well as the experience and objectivity of the researcher. The long time series of information coming from fisheries and long time research programs (many of then focused on the plankton communities) have shown their benefits when used as biological indicators. As a consequence, most of the research effort to understand the environmental variability is focused on these communities.

Keywords: Pelagic environment, variability, biological indicator. Jiménez-Rosenberg, S. P. A. & G. Aceves-Medina. 2009. Indicadores biológicos en el ambiente pelágico. CICIMAR Oceánides, 24(2): 113-127.

INTRODUCCIÓN Recientemente se ha dado mucha importancia a la medición de cambios naturales en la biodiversidad con enfoque en el manejo de los recursos (Lamb et al., 2009). Conforme se incrementa el número de regulaciones ambientales es necesario integrar aspectos ecológicos (bióticos y abióticos), sociales y culturales para definir indicadores que puedan ser Fecha de recepción: 25 de mayo, 2009

empleados como estimadores primordiales de presión en el medio y de su estabilidad y/o cambio (Niemeijer & de Groot, 2008). Los indicadores ambientales están diseñados para proveer señales sobre eventos de amplio significado y hacer perceptibles tendencias o fenómenos no detectables inmediatamente (Hammond et al., 1995). Fecha de aceptación: 07 de septiembre, 2009

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Los indicadores ecológicos son herramientas cualitativas y cuantitativas empleadas para identificar cambios en el ambiente y/o las causas de éstos; ayudan a la descripción y comprensión de la complejidad de los ecosistemas, y la de los fenómenos que en él ocurren (Hyatt, 2001). Se conforman a su vez de índices e indicadores más específicos que aportan información independiente. Una distinción debe hacerse entre lo que es un índice y un indicador. Los índices son valores numéricos que representan convencionalmente el grado o intensidad de una determinada cualidad o fenómeno y son considerados como una posible medida del estatus de un sistema (Lamb et al., 2009; Pinto et al., 2009), como los índices de Shannon (H') y de Simpson (l) , para medir la biodiversidad. Un indicador es un dato cuantitativo o cualitativo (puede ser numérico, de presencia o ausencia de organismos, de estados o respuestas fisiológicas) que pretende reflejar el estado de una situación, o de algún aspecto particular, en un momento y un espacio determinados. Habitualmente se trata de un dato estadístico (porcentaje, tasa, razón…) que pretende sintetizar la información que proporcionan los diversos parámetros o variables que afectan a la situación que se quiere analizar. Un indicador se toma o se mide dentro de un período de tiempo determinado para poder comparar los distintos períodos. La comparación de mediciones permite ver la evolución en el tiempo y estudiar tendencias acerca de la situación que analicen, adquiriendo así un gran valor como herramienta en los procesos de evaluación y de toma de decisiones (Dauvin, 2007). Entre los indicadores ecológicos que por sí solos pueden ser una herramienta útil de evaluación se encuentran los indicadores bióticos o biológicos que se refieren a la interacción de los organismos vivos con su ambiente. La elección de uno o más indicadores biológicos para interpretar las variaciones en un ecosistema no es una tarea fácil, ya que la mayoría son específicos para cierto tipo de estrés o aplicables a un solo tipo de ecosistema o comunidad (Pinto et al., 2009). La selección de un indicador biológico para describir, por ejemplo, el cambio natural en la biodiversidad es arbitraria, lo que lleva a la posibilidad de obtener diferentes escenarios en una misma área geográfica con diferentes índices. Es por ello que se hace necesaria la integración no sólo de indicadores individuales sino de sus

interacciones con otros indicadores biológicos o ecológicos (Niemeijer & de Groot, 2008). Dos tipos de indicadores biológicos son los más comúnmente usados. El primero es de tipo “discreto” y especifica un estado binario (presencia, ausencia; fondo, superficie; delante, detrás). El segundo tipo es “continuo” y permite una mayor precisión del estado o condición (cambios graduales de distribución; variaciones en abundancia; intervalos de tolerancia) y es el más usado en el contexto científico (Bratkovich, 1988). Los indicadores biológicos, a su vez, pueden ser de diferentes niveles de complejidad, desde la respuesta fisiológica de un organismo ante cierto estímulo hasta cambios de distribución o desaparición de una comunidad de organismos (Soule, 1988). Independientemente de la complejidad de la respuesta y del tipo de estímulo, varios organismos marinos han sido evaluados por su potencial como indicadores biológicos. Algunas de las características deseables en estos indicadores son:

• que vivan en el mar durante toda su vida o que aspectos importantes de ella se encuentren estrechamente relacionados con el medio marino (reproducción, alimentación).

• que presenten límites de tolerancia

estrechos a variaciones ambientales relacionadas con el suelo marino y/o las masas de agua.

• que

su captura e identificación taxonómica sean relativamente fáciles de realizar.

• que la abundancia poblacional sea alta, aunque en el caso particular de las especies raras, su escasa abundancia y su distribución geográfica particular son indicativos de condiciones particulares, frecuentemente temporales, en el ambiente.

Aun cuando diversos indicadores biológicos han mostrado su utilidad en la caracterización de ambientes y sus variaciones, se deben tomar ciertas consideraciones con respecto a su uso, como:

• que existe una diferencia entre identificar

variaciones en el ambiente y comprender los factores que las causan.

INDICADORES BIOLÓGICOS

• que un indicador biológico no sea sustituto

de un programa de investigación de amplio espectro o de un programa de monitoreo.

• que el conocimiento a fondo de una

especie indicadora no implique que especies pertenecientes al mismo género, familia, clase o phylum, o que especies con las que comparten un mismo nicho ecológico, tengan respuestas similares a las variaciones ambientales.

Por lo anterior, el uso práctico de un indicador biológico estará en función de la cantidad de información que se posea sobre las características de dicho indicador y las del ambiente estudiado. Desarrollo histórico del concepto de indicador biológico Se han usado diferentes métodos para definir a una especie o a un grupo de especies como indicadores biológicos y todos ellos tienen algo en común, i. e., inician con una lista taxonómica de los organismos identificados en una localidad geográfica. Esto habla de la estrecha relación que tiene el concepto de indicador biológico con la historia de la taxonomía y de la biogeografía. Carolus Linnaeus ya tenía noción de este concepto al asignar características ambientales especiales como condicionantes a la presencia de ciertos insectos y plantas. Linnaeus comprendió que el reto no era simplemente contar el número de especies, sino explicar sus patrones de diversidad y distribución (Brown & Lomolino, 1998). Irónicamente, los indicadores fósiles marinos (usados desde el comienzo de los estudios geológicos para caracterizar ambientes terrestre) fueron los primeros en ser empleados de manera efectiva para estimar la edad relativa de las capas de suelo y las variaciones físicas que han ocurrido a lo largo de la historia en la superficie del planeta. Se reconoce ahora que cada capa en una columna estratigráfica contiene una composición única de fósiles característicos de un periodo de tiempo único. Entre estos indicadores encontramos a fósiles de especies que eran libremente dispersadas por corrientes entre diferentes hábitats marinos, v. gr., varios grupos de protozoarios (foraminíferos calcáreos) de la era Cenozoica, hemicordados de los períodos Ordovícico y Silúrico y cefalópodos de la Era Mesozoica (Brown & Lomolino, 1998).

Darwin y Wallace, con sus trabajos sobre el origen y distribución de las especies, inicialmente lograron establecer las bases de la oceanografía biológica para que en las últimas décadas se hayan determinado los patrones de distribución de una modesta fracción de las comunidades marinas. Como se esperaba, estos patrones sugieren hipótesis ecológicas de la historia y evolución del océano con base en indicadores biológicos (Miller, 2005). En la mayoría de las referencias encontramos como “indicador biológico” a algún integrante de la comunidad bentónica, por dos razones principales: 1) son organismos conspicuos y relativamente fáciles de recolectar; 2) puesto que muchos son sésiles, en general son indicadores de cambios drásticos en el ambiente costero, relacionados con contaminación de origen natural o antropogénica, y con cambios en las propiedades físico-químicas del agua en periodos de tiempo relativamente cortos; por ello las variaciones en este ambiente se hacen rápidamente evidentes a través de ellos. Los estudios pioneros de Petersen (1913), Thorson (1957) y Nesis (1965) se fundamentan en muestreos sobre grandes áreas geográficas, nombrando a las comunidades en términos de sus especies bentónicas más abundantes y estudiando su fluctuación a gran escala con base en ellos. Más adelante, Sanders (1960) y Parker (1975) se enfocaron en la descripción completa de los integrantes del bentos de cada localidad y atribuyeron el estatus de unidades ecológicas a estas comunidades. En dichas unidades ecológicas interactúan factores biológicos, físicos y químicos del ambiente que determinarán su distribución y su utilidad como indicadores biológicos. El concepto de indicador biológico en el ambiente pelágico tiene una larga historia que inició con la noción de que la composición de especies es informativa respecto de los movimientos de las masas de agua. En la perspectiva global, los patrones de distribución del plancton se correlacionan con la extensión espacial de los grandes giros de circulación oceánica. Esto ha sido establecido en múltiples trabajos de diferentes regiones oceánicas. Sin embargo, en las zonas costeras se presenta una fluctuación considerable en la fauna pelágica entre diferentes periodos que frecuentemente presentan un ritmo regular. Russell (1939) fue el primero en estudiar este fenómeno en las cercanías de las Islas

115

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JIMÉNEZ-ROSENBERG & ACEVES-MEDINA

Británicas, sugiriendo que formas particulares de organismos planctónicos son indicativas de las masas de agua presentes en algún momento en la costa. De esta manera, se estableció por primera vez que en el ambiente pelágico existen especies indicadoras que permiten la identificación de las fuerzas advectivas de las masas de agua en cualquier momento. Esta idea se volvió popular entre los investigadores para estudiar las variaciones en el océano. Sin embargo, comprender las interacciones entre el ambiente y los organismos que lo habitan requiere de estudios a largo plazo de condiciones biológicas, oceanográficas y climatológicas. Debido a lo anterior, bajo una perspectiva histórica, la recolección de datos a largo plazo de diferentes regiones juega un papel importante en el desarrollo de la investigación oceanográfica y en el uso del concepto de indicador biológico. Con el avance de los métodos para identificar indicadores biológicos y la acumulación de bases de datos, la lista de organismos que detallan características especiales en el ambiente ha cambiado. Se ha descubierto, por ejemplo que especies que eran consideradas indicadoras (principalmente por tener distribución muy restringida), ya no lo son, ya que su distribución geográfica fue subestimada. Eventualmente el estado físico y fisiológico de los organismos indicadores, como su longitud, peso, tasa reproductiva y de mortandad, junto con las respuestas conductuales, han sido incorporadas para construir índices biológicos que son usados, junto con otros índices y modelos ecológicos, para evaluar el estado del ecosistema y realizar predicciones de cambio a corto y mediano plazo (Miller, 2005). Concepto de indicador biológico en el ambiente pelágico Una vez reconocido que las comunidades de organismos se correlacionan con las distintas masas de agua, observamos que las variaciones en las condiciones físicas del océano están claramente involucradas en muchos aspectos de la variabilidad de las poblaciones biológicas, por lo que se requiere conocer las diferentes escalas de tiempo y espacio en las que éstas ocurren y cuáles son las variables oceanográficas que regulan la dinámica en las poblaciones. Se sabe que los ecosistemas marinos cambian en una variedad de escalas

de tiempo, desde horas, a centurias. Muchas de estas escalas de tiempo están forzadas por procesos relacionados con la atmósfera, por lo que se acepta que la variabilidad climática es un fuerte impulsor de cambios en las poblaciones de peces y sus pesquerías (Lehodey et al., 2006). Entre las variables oceanográficas más estudiadas que influencian el comportamiento biológico y la dinámica de poblaciones, se encuentran la temperatura del agua, la capa de mezcla, la profundidad de la termoclina, la velocidad de surgencia, los campos de corrientes oceánicas superficiales y la capa de hielo. Se pueden identificar correlaciones entre estas variables y cambios a largo plazo en los ecosistemas pero los mecanismos específicos involucrados son aún poco claros (Venrick et al., 1987; Beamish & Bouillon, 1993; Hollowed & Wooster, 1995; Francis & Hare, 1994; Hayward, 1997; Sugimoto & Tadokoro, 1997; Francis et al., 1998; McGowan et al., 1998; Weinheimer et al., 1999; Smith & Kaufmann, 1999; Sydeman & Allen, 1999, Brodeur et al., 1999). Esto se debe a que el ecosistema está simultáneamente influenciado por muchas variables, es sensitivo a cambios de diferente escala temporal y al forzamiento físico anómalo y, por si mismo, puede generar variabilidad intrínseca a grandes escalas de tiempo (Miller & Schneider, 2000; Lehodey et al., 2006; Hunt, 2008). Los organismos que habitan el ambiente pelágico se clasifican típicamente en dos grupos: plancton, el cual incluye a organismos generalmente microscópicos que derivan pasivamente o nadan débilmente en las masas de agua; y el necton, integrado por nadadores activos y/o que pueden desplazarse libremente en el ambiente pelágico (Neshiva, 1987). En el ambiente pelágico se han nominado indicadores biológicos dentro de las comunidades de mamíferos y aves marinas, peces e invertebrados. Estos indicadores han sido empleados para identificar ambientes o fenómenos oceanográficos, principalmente con base en la biogeografía de las especies, documentando relaciones entre distribución de hábitat, densidades locales y abundancias poblacionales a nivel global. Aves y mamíferos marinos Se ha detectado que la variación en las comunidades de aves marinas es debida principalmente a tres causas: (1) densidad de po-

INDICADORES BIOLÓGICOS

blación; (2) disponibilidad de hábitat para reproducción; (3) disponibilidad de alimento. Esto a su vez ha sido relacionado con fenómenos ambientales que provocan, por lo general, destrucción de hábitat y periodos prolongados tanto de escasez como de incremento en la disponibilidad de alimento para estas comunidades. El impacto humano traducido en contaminación, la depredación o competencia con especies introducidas y la transmisión de parásitos y enfermedades causan también cambios en las comunidades debido a mortalidad, sobre todo en cuanto a aves migratorias se refiere (Wilcove et al., 1998; Baker et al., 2002; Rolland et al., 2008). Con base en esto, las aves marinas han sido empleadas como indicadores específicos; un ejemplo de esto lo representa la identificación de cambios de régimen logrado con ayuda de las estimaciones poblacionales del cormorán (Phalacrocorax bougainvolli) en el Pacífico NW, a partir de censo de aves y abundancias de cosecha de guano (Chávez et al., 2003). En este caso, la identificación de cambios de régimen se realizó a partir de una base de datos recopilada desde 1900 hasta 1990; así, se identificaron fluctuaciones de abundancias poblacionales de esta ave, que coinciden con anomalías positivas y negativas de la temperatura atmosférica, de la temperatura superficial del mar, de la circulación atmosférica y de variaciones en el CO2 atmosférico. Se observa que sus fluctuaciones poblacionales coinciden además con las fluctuaciones en abundancia de su alimento principal, la anchoveta (Engraulis ringens), las cuales a su vez son opuestas a las que presenta la pesquería de sardina (Sardinops sagax). Las fluctuaciones en las poblaciones de estas tres especies, junto con las anomalías ambientales medidas por diferentes índices, han contribuido al manejo de estas pesquerías y a la creación de índices ecológicos que ayudan a predecir y entender variaciones ambientales de largo plazo (Lluch-Belda et al., 1992; Lehodey et al., 2006). Al igual que las aves, varias especies de mamíferos marinos han sido utilizadas como indicadoras del ambiente. Los mamíferos marinos son vulnerables a la sobreexplotación, tienen bajas tasas de crecimiento poblacional debido al retardado tiempo de madurez, presentan baja producción de crías y bajas tasas de mortalidad natural (Wade & Angliss, 1997). Adicionado a esto, sus poblaciones son muy sensibles a la actividad humana. Descensos

drásticos en su densidad poblacional por lo general indican degradación en ambientes costeros, oceánicos e incluso estuarinos, sobre todo en las zonas tropicales, ya que en los polos se encuentra la mayor abundancia poblacional de estos grupos y la actividad humana es reducida (Gales et al., 2003). Sin embargo, la contaminación detectada en los mares marginales del Ártico y el incremento de los contaminantes tóxicos son extremadamente peligrosos para los ecosistemas marinos y costeros, en especial para las comunidades de mamíferos marinos (Melentyev et al., 2005). La alta capacidad migratoria de los mamíferos marinos les permite responder de manera rápida a los efectos de la variabilidad ambiental (Harwood, 2001). Las fluctuaciones de la productividad primaria influyen sucesivamente en la disponibilidad de presas para los mamíferos marinos en sus áreas críticas de alimentación. La disminución de la capa de hielo por efectos del calentamiento global reduce la extensión del hábitat de muchos mamíferos marinos polares. El detrimento en la salud poblacional del oso polar (Ursus maritimus) ha sido asociado al rompimiento temprano de la capa de hielo del polo norte, al igual que las bajas en la abundancia poblacional y la tasa de nacimiento de las focas Phoca caspita, P. sibirica y P. sainensis, que requieren de ese sustrato para su apareamiento y reproducción (Harwood, 2001). Las condiciones de deshielo por el calentamiento global, provocan la presencia de aguas más cálidas circundando el polo norte, lo que a su vez provoca una disminución en la productividad primaria, el cambio en el flujo de remolinos y corrientes y la intromisión de contaminantes desde aguas cálidas. Se ha demostrado que debido a esto, las poblaciones de la foca de Groenlandia (Pagophillus groenlandicus) y del león marino de Séller (Eumetopias jubatus) han tenido un decremento en sus poblaciones debido a la mortalidad atribuido a una pobre nutrición (Millar et al., 2004; Melentyev et al., 2005; Guénette et al., 2006). Condiciones de calentamiento anómalo del agua originadas por El Niño frente a las costas de California han sido asociadas a la desnutrición y mortandad de crías del lobo marino californiano (Zalophus californianus) debido a que ocasiona que las presas principales de las madres en lactancia disminuyan en abundancia y se localicen en condiciones

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más oceánicas y/o profundas. La captura de estas presas, por tanto, implica un mayor gasto energético y que las crías lactantes se alimenten de calostro de menor valor energético y sean más propensas a debilitamiento y enfermedades (Melin et al., 2008). A pesar de estos ejemplos en los que se observan descensos poblacionales notables en un ecosistema particular, el uso de los mamíferos marinos como indicadores biológicos es poco popular, principalmente por que entre las mismas comunidades los organismos pueden reaccionar de manera distinta a las mismas alteraciones ambientales y a que en general son difíciles de estudiar, ya sea por métodos directos o indirectos. Peces El uso de los peces como indicadores biológicos generalmente requiere de tres componentes: 1) registros de presencia/ausencia de individuos; 2) cambios de abundancia en poblaciones locales; 3) modificaciones en las asociaciones de especies locales (Stephens et al., 1988). Las comunidades de peces han sido usadas desde el inicio de la investigación de la dinámica oceánica para indicar condiciones físicas de las masas de agua pero, sólo hasta hace relativamente poco, se empezó a considerar al cambio ambiental como causa del impacto en las pesquerías (McFarlane et al., 2000). Actualmente, gracias a la cantidad de información pesquera y programas de investigación enfocados al comportamiento poblacional de los peces, se sabe que los cambios en los patrones de abundancia, estado físico y distribución de sus poblaciones están ligados a cambios ambientales (Lehodey et al., 2006; Hsieh et al. 2009). Las estadísticas pesqueras de pelágicos menores han resultado especialmente útiles para detectar variaciones climáticas en el océano, debido principalmente a su crecimiento poblacional explosivo, a su rápido colapso, y a su alta biomasa poblacional, lo que hace que sus variaciones sean muy notables. Otra característica importante es el hecho de que sus escamas generalmente son depositadas y bien conservadas en sedimentos laminados que pueden ser extraídos del fondo oceánico, lo que permite realizar un seguimiento de la variabilidad en la densidad de población en periodos extensos de tiempo. Esto ha permitido establecer que sus fluctuaciones no son sólo atribuibles al esfuerzo pesquero,

sino también a la variabilidad ambiental (Lluch-Belda et al., 2003; Yatsu et al., 2005; Lehodey et al., 2006). En el Pacifico NE por ejemplo, hay evidencia de periodos de 25 años de duración con regimenes cálidos que se caracterizan por alta abundancia de sardina (Sardinops sagax y S. pilchardus) y regimenes fríos caracterizados por alta abundancia de anchoveta (Engraulis spp.) (Lluch-Belda et al., 1992); se ha comprobado que esto sucede en todas las áreas donde estas especies co-ocurren (Chávez et al., 2003). La repetida sustitución de las poblaciones de sardina por las de anchoveta a lo largo de la historia de estas pesquerías, permite concluir que el mecanismo responsable de esta variabilidad debe haber sido similar en todos los casos y, según algunos autores, relativamente simple y directo. Esta variabilidad es difícil de explicar por la presión del esfuerzo pesquero y se adjudica a cambios atmosféricos a gran escala o al forzamiento oceánico (Chávez et al., 2003; Yatsu et al., 2005). En su conjunto, el estudio de las pesquerías en una zona puede llevar a identificar cambios climáticos a mediana y gran escala. Sin embargo, el análisis debe de realizarse con cautela, ya que si bien las especies examinadas pueden reaccionar a cambios en el ambiente, no todas lo hacen en la misma forma, magnitud y/o tiempo (McFarlane et al., 2000; Lehodey et al., 2006). Además, diversos autores coinciden en que, si bien la variabilidad a gran escala de las pesquerías se atribuye directamente a fluctuaciones ambientales, la variabilidad a pequeña escala es atribuible más bien a efectos del esfuerzo pesquero (Chávez et al., 2003; Yatsu et al., 2005; Litzow & Ciannelli, 2007; Thatje et al., 2008). Invertebrados marinos Las poblaciones de invertebrados marinos por lo general responden rápidamente a la variación ambiental. Los calamares pelágicos, por ejemplo, presentan ciclos de vida anuales, lo que propicia respuestas rápidas a variaciones ambientales que son fácilmente detectables. Muchas especies están ampliamente distribuidas y son altamente migratorias, lo que provee de una respuesta rápida detectada en cambios en los patrones de distribución, especialmente cerca de los límites de sus rangos (Pecl & Jackson, 2008). Las poblaciones de calamares tienen una distribución de tallas muy variable con gran biomasa y diferente ta-

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maño poblacional, lo que permite medir cambios anuales en distribución, abundancia y talla, que, a su vez pueden ser relacionados con cambios en el ambiente (Dawe et al., 2001). Cada faceta del ciclo de vida de los calamares ha revelado la capacidad adaptativa de éste grupo, lo que les permite explotar “vacíos” creados en el ecosistema cuando los depredadores o competidores son eliminados por alguna causa natural o antropogénica (Pecl & Jackson, 2008). Un ejemplo clásico es lo registrado frente a las costas del Atlántico, en Canadá por Dawe et al. (2001), en donde variaciones en la pesquería del calamar de aleta larga (Loligo pealeii) y en las tallas y abundancia de la pesquería del calamar de aleta fina (Illex illecerbrosus) han sido interpretadas como señal de eventos oceanográficos o metereológicos anómalos, incluso antes de que sean detectados, o que podrían no ser detectados por otros métodos. Ambas especies comparten en gran extensión su área de distribución geográfica. Se ha encontrado evidencia biológica de expansión del área de desove del calamar de aleta larga más allá del límite norte de su distribución geográfica. Al mismo tiempo, se observa un aumento en la talla del manto del calamar de aleta fina, lo que sugiere una disminución en la competencia por alimento. Estos dos sucesos son coincidentes con el aumento en la temperatura superficial del mar, asociado al forzamiento atmosférico que afecta a ambas especies, provocando respuestas diferentes e incluso opuestas en ellas (Dawe et al., 2001). Los cefalópodos en general, poseen una intrínseca flexibilidad adaptativa al cambio climático (Rodhouse & Nigmatullin, 1996). Adicionalmente, no es necesario esperar décadas para determinar las causas de variabilidad en sus poblaciones. Para las especies en las que se cuenta con amplias bases de datos, los cambios serán inmediatamente obvios. En contraste, en organismos marinos con ciclos de vida largos, por lo general son necesarias décadas para establecer la causa y efecto de su variabilidad poblacional. Plancton Las variaciones en capturas de pesquerías de importancia comercial indican que los ecosistemas pelágicos marinos cambian en respuesta a cambios climáticos de meso y macroescala. Debido a que existen muchos

procesos que separan esta variabilidad climática de los niveles tróficos superiores, un estudio retrospectivo en los niveles tróficos inferiores permite elucidar los mecanismos ligados a la variación ambiental (Chiba et al., 2006). En particular, se ha probado que el plancton es un indicador biológico muy útil por dos razones principales. La primera es su condición de ser transportados por las corrientes hacia nuevos hábitat. Una vez ahí, las nuevas formas reemplazan a las antiguas, que a su vez se transportan hacia otros lugares. Cuando las condiciones en el ambiente físico se invierten, los organismos son transportados de regreso y sus poblaciones se reestablecen rápidamente. Un aspecto importante de esta flexibilidad, es que la mayoría de los organismos planctónicos crecen rápidamente con tiempos generacionales relativamente cortos, por lo tanto son resistentes incluso a cambios radicales en el océano (Miller et al., 1994, 2005; Hsieh et al. 2009). La segunda razón por la que las comunidades planctónicas son empleadas para entender la variabilidad ambiental, es que existe gran cantidad de información acumulada a través de largos periodos de tiempo y en un gran número de regiones oceánicas (Roemmich & Mcgowan, 1995; Chiba et al., 2006; Hsieh et al., 2009). A partir de esta información, la mayoría de los estudios previos de cambios a largo plazo en el ecosistema se concentraban sólo en el total de la biomasa planctónica. Actualmente se reconoce la importancia del estudio del plancton a nivel de comunidades, especies e, incluso, de características fisiológicas y ciclos de vida. Otras características que elevan la potencialidad de los integrantes del plancton, como indicadores biológicos, es que son organismos relativamente fáciles de capturar, sus comunidades están ampliamente distribuidas vertical y horizontalmente, y tienen motilidad limitada (Neshyba, 1987). Los componentes del fitoplancton han sido estudiados como indicadores de la concentración y composición de organismos planctónicos y detritus en el océano (Kleppel, 1987). Se ha encontrado una correlación directa entre una gran abundancia de fitoplancton y elevada productividad primaria en varias regiones oceánicas y con la presencia de nutrientes en las zonas costeras (Chen et al., 2007; Gaxiola-Castro et al., 2008). Estas investigaciones han permitido caracterizaciones ecoló-

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gicas espaciales y temporales en el ambiente oceánico. Recientemente se ha estudiado el potencial de los pigmentos tanto en el fitoplancton como en el zooplancton para aportar información de la transferencia de energía en las cadenas alimentarias, ya que sus interacciones autotróficas representan uno de los primeros y más críticos pasos de la biotransferencia entre los factores bióticos y abióticos del ambiente (e.g., ciclo del carbono). Por lo tanto, los pigmentos presentes en estos organismos proveen de una sensible información cuantitativa de cómo se realizan estas interacciones tróficas (Ramont, 1980; Chiba et al., 2006). Comunidades del zooplancton han ayudado a revelar patrones y sugerir mecanismos de variación decadal del ambiente (Roemmich & McGowan, 1995; Chiba et al., 2006), así como de variación estacional (Mackas et al., 2005; Gaxiola-Castro et al., 2008). En el análisis de las comunidades planctónicas se debe considerar que, la distribución de datos, sobre todo a nivel especifico, tiende a ser en agregaciones, por lo que es difícil evaluar sin sesgo sus patrones de distribución y abundancia. El enfoque multi-específico, al usar grupos de especies en lugar de especies individuales, reduce en parte este error estadísticamente, ya que aumenta el número de individuos a analizar como un conjunto y frecuentemente se observa mayor homogeneidad en la distribución de los datos. Ésta es una razón más del creciente interés en el estudio del potencial de las asociaciones planctónicas como indicadores biológicos. Dentro del zooplancton, las larvas de peces han demostrado ser útiles como indicadores biológicos de distintas características ambientales, tanto a nivel de especie, como a nivel de asociaciones (multiespecífico). A nivel especie se han logrado identificar variaciones de abundancia drásticas en el ambiente asociadas a eventos de mediana y gran escala, como las que ocurren debidas al fenómeno El Niño en la costa noreste del Pacífico (Moser et al., 1987; Moser & Smith, 1993; Logerwell & Smith, 2001; Funes-Rodríguez et al., 2002; Franco et al., 2006). El concepto de indicador biológico a nivel multi-específico se basa en la noción de que, al menos durante una etapa de su vida, grupos de especies coinciden reiteradamente en tiempo-espacio bajo ciertas condiciones am-

bientales. Bajo este enfoque, se han documentado pruebas de la utilidad de las asociaciones de larvas de peces como indicadores biológicos del ambiente en varias regiones oceánicas (e.g., Frank y Leggett, 1983; Lavet-Smith et al., 1987; Moser et al., 1987; Sabatés, 1990; Doyle et al., 1993; Leis, 1993; Moser & Smith, 1993; Olivar & Shelton, 1993; Richards et al., 1993; Dickey-Collas et al., 1996; Gray, 1996; Grioche & Koubi, 1997; Smith et al., 1999; Witting et al., 1999; Gray & Miskiewicz, 2000; Somarakis et al., 2000; Funes-Rodríguez et al., 2002; Aceves-Medina et al., 2004). Las asociaciones de larvas de peces son indicadores de las estrategias reproductivas de los adultos de las especies que las conforman. También son útiles para definir fronteras entre comunidades y regiones faunísticas dado que presentan una distribución más restringida que los adultos ya que los sitios de desove suceden en intervalos ambientales más estrechos y generalmente están sujetas a procesos hidrográficos de concentración y retención de larvas (Moser et al., 1987; Bailey & Picquelle, 2002). La recurrencia persistente en espacio y tiempo de las asociaciones de larvas de peces a condiciones ambientales específicas de diferentes regiones del mundo y las características inherentes a su cualidad planctónica, ha hecho que se considere a éstas como indicadores biológicos útiles de la dinámica oceánica. Sin embargo, el análisis de estas asociaciones se ha realizado hasta la fecha sin considerar el estadio de desarrollo de las larvas, por lo tanto sin considerar los distintos factores que afectan a la distribución de los organismos en cada uno de estos estadios. De manera que, aun siendo indicadores biológicos efectivos, el análisis tradicional de las asociaciones de larvas de peces podría estar enmascarando información relevante con respecto a la dinámica ambiental. Recientemente se intenta probar la hipótesis de que las asociaciones de larvas de peces muestran diferencias significativas en composición y distribución dependiendo de su estadio de desarrollo y que sus requerimientos y la forma en que son afectadas por el ambiente es distinta de acuerdo a las capacidades y características emergentes de cada etapa de crecimiento. Anteriormente se suponía que las larvas de peces, al pertenecer a la comunidad planctónica, eran nadadores pasivos, que dependían exclusivamente de las condiciones de las corrientes oceánicas para su desplaza-

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miento horizontal y vertical y para su posterior reclutamiento. Estudios dirigidos han probado la alta capacidad natatoria de larvas en estados avanzados de diferentes especies (Leis & Carson-Ewart, 2000). Se ha observado que éstas presentan cierta capacidad de desplazamiento horizontal y vertical que les permite incluso trasladarse entre corrientes locales adyacentes (Lavet-Smith et al., 1987; Sabatés, 1990; Leis, 1993; Richards et al., 1993; Gray & Miskiewicz, 2000). Así mismo, se ha observado que las larvas más desarrolladas presentan conductas encaminadas a la búsqueda del nicho del organismo juvenil (Lavet-Smith et al., 1987; Richards et al., 1993; Gray & Miskiewicz, 2000), por lo que las asociaciones de estas larvas podrían distribuirse en localidades con características distintas a las del sitio original de desove. En contraste con lo anterior, la advección aún se considera como la principal causa de desplazamiento de larvas de peces en estadio de desarrollo temprano, por lo tanto se espera que, debido su limitada capacidad de desplazamiento y por haber estado sujetas durante menos tiempo a posibles procesos de dispersión, las asociaciones de estas larvas reflejen con mayor fidelidad las características de la masa de agua en donde se llevó a cabo el evento de desove, considerándolas entonces, como indicadoras de estas masas de agua. Perspectivas en el uso de indicadores biológicos Según Miller (2005), la noción de especie indicadora debe ser totalmente efectiva y calibrada por muestreos de la distribución de las comunidades a gran escala. Es decir, que para comprobar la utilidad de cualquier organismo como indicador biológico se requiere de evidencia transformada en series de datos. Es por esto que a medida que se incrementen las bases de datos, mayor y más precisa será la información que, por un lado, nos ayude a identificar indicadores biológicos y por otro a comprender y utilizar la información que aportan. Actualmente, existe una tendencia a intensificar y sistematizar el esfuerzo de muestreo, ya sea a nivel local o regional. Los indicadores biológicos, además de ser útiles en la caracterización de ambientes marinos, se emplean cada vez con más frecuencia para identificar los efectos de las variaciones climáticas en el océano, las cuales son virtualmente imposibles de medir de una manera di-

recta. La tendencia general se ha ido enfocando en las comunidades de interés pesquero y la comunidad planctónica para la identificación y caracterización de estos eventos oceanográficos, sobre todo los de mediana y gran escala. Existen a la fecha varios índices e indicadores que evidencian el cambio en el ambiente oceánico a gran escala (Niemeijer & de Groot, 2008; Lamb et al., 2009; Pinto et al., 2009). Sin embargo, debido en parte a las particularidades ecológicas que representa cada especie y a dificultades técnicas y de muestreo, no se han desarrollado métodos estadísticos apropiados para identificar la potencialidad de una especie o de un grupo de especies como indicador biológico. En lugar de esto, han sido empleados métodos numéricos heurísticos que toman en cuenta principalmente la riqueza específica del área muestreada (e.g., análisis de especies dominantes; índice de valor biológico; análisis de diversidad y equidad). Estos métodos son, sin embargo, sensibles a varios factores, por ejemplo, debido a la falta de uniformidad en el esfuerzo de muestreo, a la común distribución en agregaciones de las especies pelágicas y a la presencia de especies raras, la riqueza específica en la que se basan estos métodos, puede no ser representativa (Hill, 1979; Lamb et al. 2009). Recientemente se han propuesto métodos basados en el análisis multifactorial para la identificación de indicadores biológicos. Uno de ellos, el más popular por la simpleza de su cálculo, es el método de valor indicativo (INDVAL), que se ha empleado con éxito en distintas comunidades oceánicas, en especial las que pertenecen al plancton. El INDVAL permite identificar a las especies que caracterizan una región, basándose en la riqueza especifica, la cual puede ser medida mediante distintos métodos, y en el patrón de presencia/ausencia de las especies, combinando una medida de especificidad y una de fidelidad, las cuales representan información independiente proveniente de la interpolación de series largas de bases de datos. Una vez obtenido el valor indicativo para cada una de las especies, se puede usar esta información para la identificación de asociaciones con potencial como indicadores biológicos, agregando al método un análisis de agrupación (Dufrêne & Legendre, 1997; Beaugrand et al., 2002).

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CONCLUSIONES Del análisis de la información publicada directa e indirectamente sobre los indicadores biológicos empleados para identificar y caracterizar la variabilidad en el ambiente pelágico, se puede concluir que: La evolución del concepto de indicador biológico y de los enfoques con que se aplica, ha permitido un mayor entendimiento de la dinámica ambiental al ser empleados estos organismos como una medida indirecta de la variación oceánica. Sin embargo, los indicadores biológicos por si solos no deben de ser empleados como sustitutos de otros procedimientos de evaluación ambiental e investigación. Comunidades y organismos de diferentes niveles tróficos han mostrado su utilidad como indicadores biológicos en el ambiente oceánico, empero el valor de la información que aportan está en función de la posibilidad ser extrapolada a diferentes escalas de espacio y/o tiempo, así como de la experiencia y objetividad del investigador. En el ambiente pelágico, la información recabada por las pesquerías y la obtenida a lo largo las investigaciones sobre el plancton ha mostrado la utilidad práctica y potencial de estas comunidades como indicadores biológicos. En consecuencia, la mayor parte de la investigación encaminada a conocer la variabilidad ambiental se enfoca sobre estos organismos. Los avances científicos y técnicos en las diferentes disciplinas oceanográficas y la tendencia a desarrollar programas de muestreo continuos en regiones extendidas del océano, han ampliado el número de variables a utilizar para la comprensión de la dinámica ambiental y, en consecuencia, la información disponible sobre organismos o comunidades susceptibles de ser empleadas como indicadores biológicos. Aun así, se considera que el conocimiento de los procesos físicos y biológicos en el océano está en su etapa formativa. AGRADECIMIENTOS Al David A. Siqueiros Beltrones, al Sergio Hernández Trujillo, al José de La Cruz Agüero y al Rogelio González Armas por sus recomendaciones, así como a las autoridades del CICIMAR-IPN, SIP, COFAA, CONACyT y del SNI, asi como a los proyectos SIP-2008-0918 y SIP-2009-0421 por el apoyo otorgado para

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CODES OF CONDUCT AND CERTIFICATION ISSUES FOR SHRIMP FARMING: A REVIEW Naegel, L. C. A.1 & I. Fogel2 1

Depto. de Desarrallo de Tecnologías. Cen tro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN). Apdo. Postal 592, La Paz, B.C.S. 23000, México. Tel: +52-612-122 53 66, Fax: +52-612-122 53 22. 2Centro de Investigaciones Biológicas del Noroeste (CIBNOR). Apdo. Postal 128, La Paz, B.C.S. 23000, México. Tel: +52-612-123 84 84. email: lnaegel@ipn.mx, ifogel@cibnor.mx ABSTRACT. The growing demand for fishery products from aquaculture, especially shrimp, led to fierce criticisms about the unsustainable production and socially exploitative management. The product demand is combined with enhanced consumer concern for food safety, and environmental and social issues. Additionally, there is increasing consumer demand for information about the origin and nature of products they consume and the safety of all inputs. From the shrimp pond farmer to the retailer, there is a growing desire to meet or exceed these consumer expectations, and to be seen to be applying responsible management techniques in the development of truly sustainable shrimp production systems. These demands led to the development of codes for better aquaculture practices for the shrimp industry to ensure a sustainable, environmentally friendly and socially equitable way to produce shrimp and for the consumer to be assured healthy food. Shrimp certification was introduced to respond to public perceptions and market requirements and increase public and consumer confidence in the production practices and the product. Currently there are a growing number of standards, "Codes of Practice," and certification schemes. Proliferation of Codes of Practice and certification schemes used by governments and the private-sector industry for sustainable shrimp farming poses a number of challenges. Shrimp producers and exporters in the developing world often struggle to adapt to new and changing rules as they try to bring their farm-raised shrimp to different overseas markets. Additionally, there is the risk that Codes of Practice and certification schemes could affect the competitive position of resource-poor shrimp farmers and prevent benefits from the price premium attained through certification. There is an urgent need for more globally accepted standards and certification guidelines, especially for the small-scale shrimp farmers, to provide guidance, serve as a basis for improved harmonization, and facilitate mutual recognition and equivalence of certification schemes.

Keywords: farmed shrimp, codes of conduct, certification. Códigos de conducta y certificación para el cultivo de camarón: una revisión RESUMEN. La creciente demanda de productos pesqueros derivados de la acuacultura, especialmente del camarón, ha traído una fuerte crítica sobre la producción no sostenible y de su manejo socialmente explotador. La demanda del producto se combina con una creciente preocupación del consumidor por salvaguardar su alimentación, así como de aspectos ambientales y sociales. Asimismo, aumenta la demanda del consumidor por información sobre el origen y la naturaleza de los productos que consume y la seguridad de los insumos utilizados en su producción. Desde el camaronicultor al intermediario, existe mayor necesidad de cumplir o exceder las expectativas del consumidor y mostrar la aplicación responsable de técnicas de manejo en el desarrollo de sistemas de producción de camarón verdaderamente sustentables. Estas demandas condujeron a la elaboración de códigos para una mejor práctica de acuacultura en la industria del camarón para asegurar una forma sustentable, amigable con el ambiente y socialmente equitativa de producir camarón y de garantizar al consumidor un alimento saludable. La certificación de camarón se introdujo con el propósito de responder a las percepciones del público y los requerimientos del mercado, así como a la confianza que se tiene en las prácticas de producción del producto. Actualmente van en aumento el número de estándares, de "Códigos de Práctica" y de esquemas de certificación. La proliferación de Códigos de Práctica y de esquemas de certificación utilizados por gobiernos y el sector privado para el cultivo sustentable de camarón, enfrentan numerosos retos.Los productores y exportadores de camarón de los países en desarrollo deben luchar para poder adaptarse a nuevas y cambiantes reglas cuando tratan de introducir su producto cultivado a mercados extranjeros. Aunado a esto, existe el riesgo de que los Códigos de Práctica y esquemas de certificación, basados principalmente en soluciones tecnológicas a nivel de granja, afecten la competitividad de los granjeros con pocos recursos prohibiéndoles los beneficios de los precios privilegiados por la certificación. Son urgentes los estándares y las normas de certificación de aceptación global, especialmente para los camaronicultores Fecha de recepción: 30 de octubre, 2009

Fecha de aceptación: 12 de noviembre, 2009

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de pequeña escala que les proporcionen una guía les sirvan de base para lograr una armonía óptima y les facilite el reconocimiento mutuo y la equivalencia de esquemas de certificación.

Palabras clave: Camarón cultivado, códigos de conducta, certificación. Naegel, L.C.A. & I. Fogel. 2009. Codes of conduct and certification issues for shrimp farming: a review. CICIMAR Oceánides, 24(2): 129-150.

INTRODUCTION

Development of Codes of Practice

In many parts of the developing world, marine shrimp farming is one of the fastest growing aquaculture sectors, but it is also one of the most controversial. It has provoked some of the most contentious environmental and social justice debates in Asia, Latin America, and recently, Africa. Rapid expansion of shrimp farming in many tropical countries has proceeded without established and effective regulatory apparatus to monitor and enforce environmental, social and health standards (Barnhizer, 2002).

The worldwide concerns stimulated a growing desire at several levels within the industry to meet or exceed consumer expectations and be seen as applying responsible production and management techniques. As the shrimp farming industry has come under considerable criticism, discussion of certification proceeded. Researchers, including Bailey (1988), Primavera (1993,1997), Wilks (1995), Stonich & Bailey (2000), Stonich & Vandergeest (2001) and non-government organizations, such as the London-based Environmental Justice Foundation, the U.S. Public Citizen Organization, and the Swedish Society for Nature Conservation (SSNC) portrayed shrimp farming as destructive to coastal ecologies and communities. These critical reports targeted consumers in northern countries. Campaigns range in approach from the Monterey Bay Aquarium (2007) whose Seafood Watch Program and Seafood guide tells consumers how they can help the coasts through appropriate seafood consumption to Greenpeace (1997, 1999), the London based Environmental Justice Foundation (2003, 2004) and the Washington based Solidarity Centre (2008) who are more critical in denouncing not only the environmental impacts of shrimp farming, but also human and labor rights abuses.

Among the points of controversy are clearance of mangrove areas for constructing shrimp ponds (Primavera, 1993; de Graaf & Xuan, 1998; Barbier & Cox, 2004; SSNC, 2005; C-Condem, 2007), salinization of groundwater and agricultural land as rice fields are converted to shrimp ponds (Flaherty et al., 1999), abandonment of shrimp ponds after drastic disease-caused collapses, or more gradual, year-to-year reduction in the productivity of the pond bottom (Dierberg & Kiattisimkul, 1996), turning coastal lowlands into shrimp ponds (Páez-Osuna, 2001), disagreements of property rights (Stevenson et al., 2003;de Walt et al., 2002), use of antibiotics and chemicals (Primavera et al., 1993; Holmström et al., 2003), pollution of coastal waters with pond effluents (Páez-Osuna et al., 1999), and negative socio-economic impacts of shrimp cultivation on local populations (Bailey, 1988; Primavera, 1997; Public Citizen, 2004). Additionally, there are heightened concerns after recent detection of illegal and potentially harmful chemicals in cultured shrimp, primarily from Asian sources. However, shrimp farming provides economic opportunities for many people and foreign exchange for poor countries. As industrialized countries have increased demands for sustainable aquaculture products, consumers are insisting on safe and healthy food, willing to pay for it, and seek information about the nature, origin, and safety of inputs and products they consume.

Based on changes in mangrove forest cover over two decades, Valiela et al. (2001) estimated, in countries where historical data permitted, that of the 35% of mangrove lost, aquaculture development accounted for just over half (18.2%) (13.3% for shrimp culture, and 4.9% for fish culture). In a cost-benefit analysis of a mangrove ecosystem threatened by shrimp farming, Gunawardena and Rowan (2005) showed that shrimp for export is under-priced, since the ecological and social costs were not considered. This under-priced export article is produced at the expense of domestic food security, the environment, and local economies. According to their analysis, if all costs were reflected in the price of shrimp, the market price would be more than five times higher than it is today for the environment to be sustained and local peoples to receive fair

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compensation for their inputs. Shrimp farming is a clear example of how the economic colonization of the southern hemisphere is still going on, finding new avenues through modern globalization, transport, and international trade (Uppsala University, 2008). For these reasons, van Mulekom et al. (2006) called for a halt to further expansion of shrimp ponds and a temporary halt to export-oriented and liberalization policies. Since most farmed shrimp is produced in southern countries, but consumed in northern ones, production/consumption can easily be framed as a global environmental justice problem, in which northern over-consumption drives environmental and social harm in the south (Vandergeest, 2007). As BĂŠnĂŠ (2005) described "â&#x20AC;Śalthough there is agreement between technical experts and scientists in the shrimp farming industry and environmental groups that better management practices in shrimp farming could solve some of the environmental and social problems, there are major differences in opinion about which direction is most useful and valuable, including: (a) Are the main issues the social and environmental disruptions induced by shrimp farming the biological and physical sustainability of the farm? (b) Should the causes of the problems be studied or are technological solutions to be sought first? (c) Is the cause of the problems political (distribution of power) or mainly technical, where the solutions lies esentially in selecting the appropriate farm locations and applying technological innovations? (d) Should extensive and integrated agriculture/aquaculture systems be promoted or intensive and closed systems? (e) Should resource-poor farmers or large-scale entrepreneurs be supported? (f) Should entrepreneurs in shrimp farming be blamed for environmental impacts or small-scale farmers? (g) Are local or international donor organizations, who finance expansion of shrimp ponds to the detriment of poor communities be blamed for the ecological and social problems of shrimp farming or should the blame be placed on resource-poor farmers?". With increasing concern about environmental sustainability and social impacts of the shrimp farming sector, combined with food safety of consumers, the Food and Agriculture Organization of the United Nations (FAO) prepared a voluntary guide for nations to develop a Code of Conduct for Responsible Fisheries and Aquaculture (CCRF). In 1995, the voluntary code was adopted by the FAO, providing a

framework for national and international efforts to ensure sustainable exploitation of aquatic resources in harmony with the environment (FAO, 1995). The CCRF is global in scope, and is directed toward the widest number of members and non-members of FAO, including fishing firms, governmental and nongovernmental regional and global organizations, and all persons concerned with conservation of fishery resources and management and development of fisheries, including shrimp farmers, processors, and marketers of fish products and other users of the aquatic environment in relation to fisheries (FAO, 1995). Article 9 of this guide deals with aquaculture; Article 9.4 explicitly states that States should promote (a) Responsible aquaculture practices in support of rural communities, producer organizations, and fish farmers; (b) Active participation of fish farmers and their communities in developing responsible aquaculture management practices; (c) Efforts that improve selection and use of appropriate feeds, feed additives, and fertilizers, including manures; (d) Effective farm and fish health management that favor hygienic measures and vaccines, safe, effective and minimal use of therapeutics, hormones and drugs, antibiotics, and other disease control chemicals; (e) Governments should regulate the use of aquaculture chemicals that are hazardous to human health and the environment; (f) Governments should require that disposal of wastes (offal, sludge, excess veterinary drugs, and other hazardous chemicals) does not constitute a hazard to human health and environment; and (g) Governments should ensure safety of aquaculture products and promote efforts that maintain product quality. In Article 10, the importance of integrating of aquaculture into coastal area management, taking into account the fragility of coastal ecosystems, the finite nature of their natural resources, and the needs of coastal communities is explained. Additionally, in this article, developing institutional and legal frameworks to determine the possible uses of coastal resources and govern access to them, governments should address the rights of coastal communities and their customary practices to encourage competition with sustainable development. In 1997, FAO published technical guidelines with annotations on the principles in article 9 about acceptable aquaculture of the Code of Conduct publication of 1995 (FAO, 1997). These annotations were intended for general

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guidance, and should have been taken as suggestions or observations to assist those interested in identifying their own criteria and options for actions, as well as for partners helping to support sustainable aquaculture development. As explained in this document: "â&#x20AC;Śgiven the diversity in aquaculture and the sometimes different perceptions of 'sustainability' more balanced and informed approaches are required to address developmental and environmental issues at any given location. Commitment for collaboration, constructive dialogue among possible partners, and participation of aquafarmers and their communities, are important when assigning responsibilities for sustainable aquaculture development" (FAO, 1997). Barg et al. (1999) reviewed the FAO code for sustainable cultivation of shrimp and reported on the assistance provided by FAO in the development of national codes of practice, technical guidelines, and best management practices for sustainable shrimp cultivation. In the context of a development project supported by FAO's Technical Cooperation Programme, technical assistance was provided to government authorities, as well as the private sector and other stakeholders in the development of a code of practice in Malaysia. Likewise, the development of national codes of practice was discussed during technical workshops in Sri Lanka and Bangladesh (Barg et al., 1999). The Southeast Asian Fisheries Development Centre focused attention on the original Article 9 of the Code of Conduct with the responsibility of individual States to implement the code and develop guidelines for the implementation of the code at a regional level. "Using these Regional Guidelines as a basis, States may take necessary steps to appropriately manage aquaculture within their jurisdiction by (a) Initiating necessary action identified in the Guidelines, (b) Preparing technical guidelines to further clarify the issues and specific subjects in the Guidelines, (c) Improving the national instruments, and (d) By promoting the required policy and technical research to obtain needed of detailed information" (SEAFDEC, 2001). In December 1997, the FAO convened a technical consultation in Bangkok on policies for sustainable shrimp cultivation, with the goal to collect background information, descriptions and analyze of development of shrimp cultivation and management, including legal and institutional aspects

and government policies of several of the main shrimp-producing countries, accounts of activities, the views of several intergovernmental and non-governmental organizations on shrimp cultivation, and a review of development economics and socio-economic issues (FAO, 1998a, 1999). During this consultation, some participants noted that achieving sustainable shrimp cultivation was dependent on effective government policy and regulatory actions, as well as the cooperation of the shrimp farming sector in utilizing appropriate technology in its planning, development, and operations. Participants recommended that the FAO convene expert meetings to elaborate on good management practices in shrimp cultivation and determine desirable elements of legal and other regulatory instruments for coastal aquaculture (FAO, 1998a). In 1998 a consultancy workshop took place in Rome, where mainly sustainability indicators (ecosystem and biophysical, economic and social, legal and institutional, and farm-level) for shrimp farming and a draft questionnaire addressed to governments of shrimp-farming countries (FAO, 1998b). This workshop was followed by one in December 2000 in Brisbane, Australia, with 71 experts from 19 countries, most from major shrimp-producing and consuming nations. The participants represented government and non-government organizations, shrimp producers and associations, and intergovernmental agencies, including the World Bank, World Wildlife Fund for Nature, the Global Aquaculture Alliance (GAA), Naturland, and the Industrial Shrimp Action Network (ISANet). The main objectives of the 'Expert Consultation' were to provide a recognized international forum for discussion on major aspects related to the promotion of sustainable shrimp culture practices, as well as related institutional and legal instruments for the development and implementation of good management practices leading to improvements in shrimp cultivation at the farm and institutional level (FAO and Dept. of Agriculture, Fisheries and Forestry, Australia, 2001). During this workshop, topics of discussion included how to identify, develop, and implement specific good management practices and good legal and institutional arrangements for sustainable shrimp culture. Objectives, rather than principles were formulated, so that progress could be measured against them: "(a) Use land and water which is

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suitable for sustained shrimp production, (b) Conserve sensitive aquatic habitats and important ecosystem functions, (c) Manage soil resources and earthwork to minimize impacts on surrounding environments, (d) Minimize impacts on local water resources, (e) Avoid release or escape of exotic species and transgenics into the environment, (f) Responsible use of chemicals that may impact adversely on ecosystems and human health, (g) Maximize efficiency of resource use and minimize waste outputs, (h) Reduce dependence on wild stocks for farmed shrimp production, (i) Optimize social and economic benefits to the wider community and country, (j) Conduct shrimp farm operations to minimize impacts on surrounding resource users, and (k) Ensure the rights and welfare of staff in farm operations" (FAO, Dept. of Agriculture, Fisheries and Forestry, Australia, 2001). Many thought that these objectives would automatically lead to successful operations; however, from a business perspective, good management practices should demonstrate a clear benefit, either in reduced costs and higher profits or in better reputation and reduced potential for conflict. To provide an analysis of shrimp farming and the environment and to make recommendations the World Bank sponsored a study (Hempel & Winther, 1997). This study confirmed that shrimp farming is a very diverse subsector of aquaculture, in terms of farming systems and geographic location, the environmental, social, and economic importance of cooperation and coordination of efforts to promote better management practices. These results led to a consortium comprising the following agencies: the Network for Aquaculture Centres for Asia and the Pacific, the World Bank, the World Wildlife Fund for Nature and the FAO. In 2004 joined the United Nations Environment Programme (UNEP) the consortium. The objective of the consortium was to analyze and share experiences on better management practices under various environmental, social, and economic conditions and to assess the cost-benefits for farmers to adopt these practices individually and in cooperation with other farmers. Their objectives were to: (a) Generate a better understanding of the key issues involved in sustainable shrimp aquaculture, (b) Encourage a debate and discussion around these key issues to lead to consensus among stakeholders, (c) Identify better management practices for

shrimp aquaculture, (d) Evaluate the cost for adoption of such strategies and other potential barriers to their adoption, (e) Create a framework to review and evaluate successes and failures which can inform policy debate on better management for sustainable shrimp aquaculture, and (f) Identify future development activities and assistance required for the implementation of a more sustainable shrimp culture industry (World Bank et al., 2002). This information was intended to help governments and the private sector develop support strategies and specific assistance measures for farmers to overcome the constraints that currently prevent them from adopting better management practices. The consortium generated improved information on key issues for sustainable development and management of shrimp farming; facilitated consensus building among stakeholders at international, regional, national, and local levels; identified management strategies for sustainable shrimp farming; provided a basis for informing policy makers on management strategies; and provided a platform for identification of future development activities and assistance for implementation of management strategies. The program involved thematic reviews covering the identification of better management practices and reviewed implementation through codes of conduct and practices; reviewed management strategies for preventing and treating shrimp viral diseases; social aspects and alleviation of poverty; and rehabilitation of mangroves and other coastal habitats. Case studies were prepared by more than 100 researchers from more than 20 shrimp-farming countries through consultations throughout Asia, Africa, and the Americas. Some of the reviews and case studies are available on the website: www.enaca.org/shrimp. These reviews and case studies provided the basis for the publication, International Principles for Responsible Shrimp Farming (FAO et al., 2006), which provided the technical basis upon which stakeholders could collaborate for more sustainable development of shrimp farming. For governments, they provided a basis for policy, administration, and legal frameworks that can be renewed, adjusted, funded, and implemented to address the specific characteristics and needs of the this sector to protect and enhance the industry, the environment, other resource users, and consumers. Strengthening of institutional arrangements, capacity, and partnership are also important to ensure cooperation

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and coordination of all relevant institutions with jurisdiction over natural resources, and animal and public health. The publication of "International Principles for Responsible Shrimp Farming" deals with: (a) Sitting of shrimp farms, (b) Design and construction of farms, (c) Minimizing the impact of water use, (d) Responsible use of broodstock and postlarvae, (e) Efficient use of feeds and feed management, (f) Health management, (g) Ensuring food safety and the quality of shrimp products, and (h) Social responsibility (FAO et al., 2006). Additionally, this document provided the basis for developing standards and certification systems. Codes of Conduct Some countries have developed national level codes of conduct (CoC) for production of farmed shrimp, such as Thailand's Good Aquaculture Practice and Australia's Environmental Code of Practice. Codes of Conduct at the national level a) The case of Thailand The Marine Shrimp Culture Research Institute of Thailand's Department of Fisheries (MSCRI, 2003) designed a flexible framework for a CoC in 2000 through consultation with industry associations, with the idea that farm group would be able to use the framework to design farm-specific codes appropriate to local circumstances, an approach that introduces a degree of mutability into the standards (Vandergeest, 2007). The Department of Fisheries encouraged adoption of voluntary management practices through Good Aquaculture Practices (GAP) to assure product safety and to facilitate shrimp exports by creating traceability and providing laboratory testing for chemical residues. The scheme intended to assure product safety. To obtain GAP certification, shrimp farmers register their farm and provide documentation to the local offices of the Department of Fisheries when they purchase postlarvae from hatcheries, and again when they sell their harvest. Additionally, officials visit these farms prior to harvest to measure water quality and test for antibiotic residues. They take notes on general farm appearance, cleanliness, and water/sediment disposal and make recommendations for improvement (Vandergeest, 2007). In Thailand, processors are no longer accepting shrimp witout GAP valid movement documents, which allow farmers to transport each batch of harvested shrimp to the market. This procedure serves

the traceability requirement (Pongthanapanich & Roth, 2006a, b). Field research in Southern Thailand by Vandergeest (2007) showed that a combination of community-based collective action and local governments are currently the most effective regulators of shrimp farming. As local communities need to live with shrimp farming on a day-to-day basis, know best the local social and environmental impacts, and are most motivated to contain these impacts, effective community actions need to be facilitated and supported by central government policies and agencies, including technical agencies like the Department of Fisheries and civil authorities. In a concerted voluntary effort by shrimp farmers, shrimp farming associations, various educational institutions and agencies that are concerned with the importance of biodiversity of the mangrove ecosystem, mangroves could have increased by 46% between 1995 and 2000 (Nissapawanich, 2007). The voluntary collaboration between the shrimp farming industry and the Department of Fisheries was the basis for successful implementation of the GAP certification scheme of Thailand. b) The case of Australia Another example is the Australian Prawn Farmers Association (APFA), which prepared a voluntary Code of Practice to maintain the integrity of the environment and enable the shrimp farming industry to become sustainable. This code aims to provide realistic objectives: fall within the legal requirements of environmental protection, be relevant to Australian prawn farmers, provide options for management, be flexible, provide a mechanism for environmental self-regulation, focus on outcomes, and be practical. The Environmental Code of Practice stated the following objective: "To protect Australia's environment while allowing for the development that improves the total quality of life, both now and in the future, in a way that maintains the ecological processes on which life depends." Participants in the Australian shrimp industry are encouraged to: (a) Support industry research into environmental issues, (b) Achieve, and where practical, go beyond compliance with all legislation and license conditions, (c) Ensure that products are produced, packaged, delivered, disposed of, and recycled in an environmentally responsible manner, (d) Minimize use of raw materials and energy, (e) Design production systems to minimize adverse environmental impacts, (f) Take into consideration environ-

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mental impacts of new projects at the planning stage, (g) Provide management and employees with appropriate levels of environmental training and education, (h) Require employees to accept environmental responsibilities as a part of their job description, and (i) Conduct environmental reviews at appropriate intervals. Farmers not fulfilling the requirements of the APFA will not receive legal assistance in environmental disputes (Donovan, 2001). Codes of Conduct at the international level At the international level, the Global Aquaculture Alliance (GAA) developed codes of conduct for Best Aquaculture Practices and promoted a certification scheme for shrimp production under the Aquaculture Certification Council (ACC). a) Certification schemes Increased awareness among consumers over how shrimp are farmed, environmental, social, and food safety concerns, as well as competition in the seafood trade have drivenes interest in certification. Certification gives an opportunity to large retail organizations seeking a competitive edge in product quality and corporate image. For example, US-based Wal-Mart (largest retail chain) and Red Lobster (restaurant chain) and UK-based Lyons Seafood (largest British supplier of shrimp) announced that they require all their suppliers to be certified by the ACC's BAP program. Certification schemes are best conducted by a recognized and independent third-party organization having a written or equivalent assurance that the product, process, or service conforms to specified requirements. Certification may include a range of inspection activities which could include continuous inspection in the production chain. Typical examples of conformity assessment activities are: sampling, testing and inspection, evaluation, verification and assurance of conformity (suppliers' declaration, certification); registration, accreditation, and approval in any combination. According to Funge-Smith et al. (2007), standards for shrimp certification programs should be developed through transparent involvement of all parties concerned, from the farmer to the consumer and compliance with the agreed standards should be verified and guaranteed by third-party inspection. Clay (2007) considers standards for shrimp certification programs should focus on key impacts.

Stakeholders in shrimp farming identified the following issues of high importance for certification: antibiotic and chemical use, disease transfer, land and water use, fishmeal/oil use, water pollution and user conflicts, which should be considered in standards for a shrimp certification program. The ranking of these key impacts, especially the social impacts, is still a special challenge for certification programs. As examples, goals, principles, and achievements of two international, non-governmental, certification bodies will be described, one promotes "best aquaculture practices" and the other "organic shrimp farming." Following the two descriptions, attempts to certify shrimp production through national organizations will be discussed. Lastly, the work of international organizations to develop more globally accepted norms for aquaculture certification will be described. Non-governmental certification bodies a) Global Aquaculture Alliance (GAA), Aquaculture Certification Council (ACC) and "Best Aquaculture Practic" The GAA, based in the United States, is an international non-governmental organization, supported by aquaculture businesses to counteract prominent critics, especially environmentalist groups, of shrimp farming in developing countries. Based on Article 9: Aquaculture Development in the Code of Conduct for Responsible Fisheries (FAO, 1995) and Technical Guidelines for Responsible Fisheries: Aquaculture Development (FAO, 1997), GAA developed its "Guiding Principles for Aquaculture" in 1997. GAA, in cooperation with The Network of Aquaculture Centres in Asia (NACA) and Auburn University, provided background information on the interactions between shrimp farming and mangroves. In 1998, the first issue of the Global Aquaculture Advocate newsletter was launched to keep subscribers informed about the issues facing the aquaculture industry and the activities of GAA. The Codes of Practice for Responsible Shrimp Farming, drafted by Boyd and reviewed by the GAA Technical Committee, followed in 1999 (Boyd, 1999). It contains nine series of recommended practices (mangroves, site evaluation, design and construction, feeds and feed use, shrimp health management, therapeutic agents and other chemicals, general pond operations, effluents and solid wastes, and community and employee relations)

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for the shrimp farming industry. The purpose of the Code was to provide a framework for environmentally and socially responsible shrimp farming that was voluntary, proactive, and standardized and intended as flexible guidelines that would be continuously improved as shrimp farming technology advanced. National codes of conduct and practices based on the GAA's Codes of Practice for Responsible Shrimp Farming were developed by the fisheries departments of the governments of Thailand, Nicaragua, Ecuador, and Honduras. The Bangladesh SSoQ program, Thai Code of Conduct, and the Australian Prawn Farmers Association incorporated the GAA's code of practice into their shrimp certification principles. In 2002, the GAA supported formation of the Aquaculture Certification Council (ACC), an independent and international nongovernmental organization to certify environmental, social, and food safety standards for shrimp hatcheries, farms, and processing plants. In 2004, the GAA developed its "Best Aquaculture Practices" (BAP) guidelines to address social, environmental, and food safety for shrimp aquaculture (GAA, 2004). For its third party certification system for farmed shrimp the ACC builds on the guidelines for Best Aquaculture Practices developed by the GAAÂ´s Responsible Aquaculture Program and the ACC certifies the shrimp hatchery, farm, and the processor based on these standards. ACC offers a "process" rather then a "product" certification. The ACC published guidelines for certification of aquaculture facilities (hatcheries, farms and processing plants), describing in detail the concerns and possibilities to mitigate negative aspects of shrimp farming related to the community (property rights and regulatory compliance, community relations, especially concerning access to mangrove areas, worker safety, and employee relations), environment (mangrove conservation and ecosystem protection, veterinary health and microbial sanitation, effluent and sediment management, soil/water conservation, source of postlarvae, storage and disposal of farm supplies), and food safety and quality assurance (standard sanitary procedures, hazard analysis and critical control point program, and product testing), and product traceability from the hatchery, farm, and processing plant (ACC, 2004). These guidelines were developed for industrial shrimp farms; resource-poor farmers have difficulties complying with the guidelines, especially with regard to effluent

monitoring and sediment management. The ACC specialist in certification receives training in the certification standards and performing environmental and social impact assessments. The first aquaculture facility certification training course was held in Ecuador; courses in Indonesia, Vietnam, Nicaragua, Thailand, and Mexico followed. By the end of 2006, ACC had certified 50 processing plants and nearly 100 other facilities (shrimp hatcheries and grow-out ponds) and the number of ACC auditors reached 112. b) Naturland, Germany (organic shrimp farming) Naturland is one of the certification bodies in the International Federation of Organic Agriculture Movements (IFOAM) and developed organic standards for several aquaculture commodities. It issued its standards for organic shrimp farming at the end of 1999 and started its first project with in Ecuador. This pilot project was an opportunity for shrimp farmers to choose responsible, safe, and sustainable production. Naturland's Standards for Organic Aquaculture (Naturland , 2004; 2006) included a specific section for pond culture of the Pacific whiteleg shrimp Penaeus vannamei. For conformity assessment of their certification scheme for hatcheries, farms, feed production, and shrimp processing plants, independent, and internationally accredited third party inspection organizations were given responsibility for certification. In collaboration with the Swiss Import Promotion Programme (SIPPO) and the Institute for Marketecology (IMO), Naturland developed the International standards for organic aquaculture, "Production of shrimp" (SIPPO et al., 2002). In 2004 and 2006, Naturland revised this standard, requiring amongst other issues that organic shrimp farms protect mangrove areas and not use antibiotics, inorganic fertilizer, and pesticides, stock ponds with postlarvae in very low densities, and use feed that was low in protein and fishmeal. Certified organic shrimp farms can now be found in Ecuador, Peru, Vietnam, Indonesia, Brazil, and Thailand. Certification through national organizations a) Department of Fisheries, Thailand With assistance from the World Bank and consultations with industrial associations, the Department of Fisheries designed a flexible certification framework, the Marine Shrimp

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Culture Industry of Thailand Code of Conduct, with the concept that groups of shrimp farmers would be able to use the framework to design farm-specific codes appropriate to local circumstances, an approach that introduces flexibility into the standards not found in transnational standards. The Thai code covers product safety, as well as environmental and social responsibilities. The overall framework was modeled on the standards of the GAA, with assistance from technical experts to assess environmental impacts. However, during the development of the standards, inputs from local communities on avoiding social conflicts between shrimp farmers and other coastal inhabitants were neglected (BĂŠnĂŠ, 2005; Vandergeest, 2007 ). Not surprisingly, participation in the Thai code framework has been low. In 2006, of approximately 35,000 shrimp farms and more than 1,500 hatcheries, only 146 farms and 140 hatcheries were certified. On the other hand, in the GAP scheme, which focuses on product safety, 28,719 farms and 1,679 hatcheries voluntarily joined (Pongthanapanich & Roth, 2006a, b). To increase the number of Thai code adopters, the benefits and costs of participation have to be clear. Resource-poor farmers are willing to miss possible additional income if they can avoid risk and uncertainty of outcome. The implementation of the Thai code must result in positive social and environmental impacts and synergies. Additionally, the constraints to implementation have to be understood and possibilities offered on how these constraints might be overcome, particularly among small-scale shrimp producers. Solutions could be planned, implemented, and enforced at the national and local levels. b) Shrimp Seal of Quality, Bangladesh In Bangladesh, the black tiger shrimp Penaeus monodon is cultured predominantly under extensive farming systems with low stocking densities, little or no external feed inputs, and tidal water exchange. Bangladesh has large areas of coastal tidal land, of which 143,000 h has been under brackish water shrimp aquaculture and more than 600,000 persons are directly or indirectly engaged in shrimp farming (Alam et al., 2005). In the mid-1990s, the shrimp industry of Bangladesh faced serious difficulties; it was hit by viral shrimp diseases and a ban on frozen shrimp exports for their failure to comply with European Union quality regulations after an inspection team from the European Union condem-

ned shrimp processing plants. Additionally, international buyers and consumers of shrimp were increasingly demanding that shrimp in Bangladesh be produced in compliance with recognized codes of conduct regarding human rights, fair labor practices, and environmental protection. To ensure the shrimp farming industry's survival and growth, the U.S. Agency for International Development provided $10 million in 2003 to the Government of Bangladesh agribusiness project to develop together a voluntary process certification with national and international stakeholders called the "Shrimp Seal of Quality" program (SSoQ) and establish and implement a domestic certification system. The SSoQ program attempted to create sustainable improvement in volume and value of Bangladesh shrimp exports. The program certifies that the operator has met the minimum requirements in food safety and quality assurance, traceability, environmental sustainability, labor practices, and social responsibility. The SSoQ approach, in the short and medium term, was to improve the quality of shrimp larvae to reduce the risk of losses from disease, introduce environmentally friendly farm management practices, and increase production and profit. Additionally, the SSoQ scheme introduced a program to certify shrimp producers, including hatcheries, farmers, transporters, and processors by creating a stable supply of quality shrimp from reliable suppliers for the export market (Kearney Gaillard et al., 2006). The SSoQ program is now a legally registered symbol that certifies that the farmed shrimp was produced and processed in strict compliance with the SSoQ's standards and codes of conduct. The codes of conduct incorporated the standards of the ACC and the ACC conducted a series of workshops, roundtable discussions, and training programs and defined minimal, internationally acceptable operations and management practices pertaining to technical, environmental, and social standards. The SSoQ program now provides training, technical support, laboratory services, and market research and development. An outside third party certifier monitors the certification standards to ensure that there is no cheating or corruption of the program. The SSoQ program ensures that Bangladesh continues to sell its shrimp in international markets (Fleming, 2004). In view of these positive developments in voluntarily adopting codes of conduct and certification schemes, one important point remains to be considered. By using codes of conduct and certification schemes

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developed by organizations supported by aquaculture businesses and scientists, there is the danger that the schemes protect industrial shrimp farming and neglects social aspects of resource-poor shrimp farmers and their communities. By interviewing government officers, shrimp farmers, traders, processors, and workers for non-government organizations, Islam (2008) found that the majority of the stakeholders were skeptical of the role and operation of the SSoQ. The farmers were not familiar with what happens after their shrimp is harvested, including the process of certification, demands of the international market, and the idea of a third-party certifier sidelining the government. Most stakeholders had the opinion that the SSoQ program undermines the capacities and knowledge of the local communities to manage the environment, that the SSoQ program is an agent of the buyers, potentially exclude small-scale farmers and provide privileges to large scale shrimp farmers. The local community believes that the Department of Fisheries is capable of full certification, as required by the buyers. In this respect, a recent, interesting publication about shrimp farming in Bangladesh should be mentioned. Alam et al. (2005), from the Asian Institute of Technology and the Network of Aquaculture Centres in Asia Pacific (Bangkok, Thailand) conducted a study in Bangladesh to assess the status and understand the degree of awareness of the FAO Code of Conduct for Responsible Fisheries among different stakeholders and its application in the area of shrimp culture. They found that virtually no significant efforts had been made to comprehend and develop the provisions of the Code, although Bangladesh is a signatory to it. They recommend that general awareness of the existence and significance of the FAO Code of Conduct and its scope and purpose have to be increased among the persons and institutions involved in shrimp aquaculture. It would require training of personnel of the Department of Fisheries to use, conserve, and manage shrimp aquaculture. Likewise, the other stakeholders of the sector need to be made fully aware of the code and to be motivated towards voluntary compliance. The small-scale shrimp farmer and the Codes of Conduct and Certification Schemes While recognizing the value of "Codes of Conduct" and certification schemes in shrimp

farming for increasing public and consumer confidence in shrimp production practices and products, some non-governmental certification schemes have resulted in higher costs for producers without delivering significant benefits to small-scale shrimp producers. Increasing international environmental and social awareness, coupled with the availability of certified products from well-organized, large scale, industrial shrimp producers may force lowering of prices of non-certified products. It will be more difficult for small-scale producers in developing countries to comply with Codes of Conduct and suffer a reduction of sales price. They usually lack the necessary awareness, organization, and reporting and marketing skills to participate in certification and labeling schemes. Additionally, if Codes of Conduct and certification schemes are over-prescribed, in the sense that they promote specific technical solutions rather than supporting a variety of solutions to achieve a specific outcome, then they will restrict innovation and discriminate unnecessarily against some producers. This is particularly the case for small-scale shrimp farmers where a particular Good Management Practice may have been handed down, based on a highly technological approach. Therefore, it is essential that Codes of Conduct and certification schemes be flexible and adaptable, while strongly promoting the sustainability of the operation (FAO, 2001). Additionally, there is a need for more globally accepted certification guidelines for shrimp production that could provide more guidance and serve as a basis for improved harmonization and facilitate mutual recognition and equivalence of certification schemes. While certification of shrimp aquaculture products has potential to provide opportunities and incentives for responsible development of shrimp farming, there are a number of issues that need to be considered. Particularly in Asia, the large number of resource-poor shrimp farmers and fragmented market chains will make establishment and operation of shrimp certification programs challenging. The certification and adoption of better aquaculture practices could provide benefits for both producers and consumers, but can also be barriers to participation of small holders in market chains. Because globalization and market trends have significant impacts on the way aquaculture products are produced, small-scale shrimp farmers face various barriers to participation in modern market chains.

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This includes the small volume from individual farms and large numbers of farmers with limited access to markets, and complex marketing channels make traceability difficult. Increasingly, integrated production-distribution structures, market risks, and more stringent market standards are all increasing vulnerability and pressure on small-scale shrimp famers; most international market trends in aquaculture are probably working against them. To overcome these barriers, small-scale shrimp farmers need much more focused technical and financial servicing. Support to establishing small-scale local farmer organizations, such as the Thai shrimp farmers associations and "aquaclubs," where shrimp farmers can work together to improve and adopt better aquaculture practices, can eventually be "cluster certified" and develop sufficient economies of scale and knowledge to participate in modern market chains. Additionally, organized shrimp farmers can speak with a stronger voice in negotiating prices for inputs, such as feed and seed and potentially have a better platform for more organized marketing and price negotiation when selling their product (Subasinghe & Phillips, 2007; Phillips et al., 2008). Since better management practices are the first step to increase productivity and profitability for small-scale farmers and, subsequently to certification, the Australian Centre for International Agricultural Research (ACIAR) funded a collaborative project in Indonesia between four small-scale farmer groups and Australian researchers. During the search for representative farmer groups, the team found localized geographical areas that carried higher risk of shrimp losses than other areas. Two factors appeared to be most important: high bio-security risk from wild shrimp and problematic soil types, particularly high sulfate and sandy soils (Callinan, 2008). This discovery illustrated one of the difficulties in forming "aqua-clubs" with small-scale shrimp farmers. FAO (2007b) recommended special considerations for small-scale farmers in aquaculture schemes: "a) the certification standard must be practical and accessible for small-scale producers, b) special efforts need to be undertaken to ensure that small-scale producers play a key role in setting of standards, c) small-scale farmers have special needs for education, capacity building, and the transfer of technology and technical information, d)

there is a need to develop a model and identify methods that facilitated the ability of small-scale producers to enter the certification scheme and become certified, e.g., a step-wise (i.e., phased) system might be more accessible to small-scale producers, and e) education, training and capacity building programs should be developed to help ensure that small-scale producers have the skill and expertise to apply best management practices up to the state of the art." Additionally, FAO recommended group certification as a means to foster and facilitate participation of small-scale producers, e.g., cooperatives, clusters, or unions of producers. Group members should agree to specific commitments in relation to compliance: a) shared obligations and benefits, b) use similar aquaculture systems, c) geographic proximity and/or used shared resources, such as water, d) certified entity as a group as a whole, e) internal cohesion/organization, so that sampling can be applied, f) organizational structure for the group, e.g., a board of directors, g) financial support structure for the group, e.g., member dues, h) transparency, accountability, and monitoring with group, i) capability to support a viable internal control system, e.g., a contract signed by each member, j) documented audits of all group member for compliance, carried out as a minimum annually by the internal control system, k) consequences for lack of compliance, at the group and individual level, reflecting the severity of the non-compliance, and if mitigation measures are not possible or appropriate, the entire group loses certification for serious non-compliance, and l) operational support for members, including training. Attempts to compare and harmonize the different standards and certification schemes The emergence of a wide range of codes of conduct and certification schemes for shrimp production, as well as different accreditation bodies was creating confusion amongst producers and consumers alike. The standards and certification schemes are not harmonized, which means that shrimp farmers and exporters in the developing world often must struggle to adapt to new and changing rules as they try to bring their farm-raised shrimp to different overseas markets. Recently the FAO and the World Wildlife Fund started meetings and dialogues with wide mul-

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ti-stakeholder participation to harmonize the standards and certification schemes. FAO In September 2006 the FAO Sub-Committee on Aquaculture requested FAO to convene expert workshops and encouraged FAO to play a lead role in facilitating the development of guidelines which could be considered when national and regional aquaculture certification guidelines are developed. To improve harmonization of certification and facilitate mutual recognition and equivalence of aquaculture certification schemes in more globally accepted norms for aquaculture production, an expert workshop convened in March 2007 in Bangkok to start a process for developing guidelines on aquaculture certification (FAO et al., 2007). The workshop was attended by 70 participants representing government authorities, farming and industry associations, NGOs, and the private sector. The objective of the workshop was to define general guidelines around which aquaculture certification schemes can be built, whether they be for systems, practices, or products. FAO compiled the results of the workshop and published a preliminary draft for comments and discussion during an expert workshop held from 31 July to 3 August 2007 in Fortaleza, Brazil (FAO, 2007a). In February 2008 FAO held an additional expert meeting in London as a follow-up to gather views and opinions of European stakeholders from across the seafood supply chain that were involved in aquaculture certification to explore opportunities for building partnerships to support the implementation of aquaculture certification in producing countries, with particular reference to the small-scale aquaculture sector and to continue the process of preparation of the international guidelines for certification of aquaculture products. Expert workshops followed in May in Beijing (China) and Silver Springs (Washington, USA). The draft revised during the workshops of the Guidelines for Aquaculture Certification and subsequently submitted by FAO to its member governments for evaluation and approval in a meeting of the FAO Aquaculture Subcommittee in October 2008 in Chile (FAO, 2007b, 2008). The guidelines should be applicable to aquaculture certification schemes that seek to address: a) social issues, b) environmental impacts, c) food safety, d) animal health and welfare, and e) economic and financial issues. During the workshops, it was stressed that

certification schemes should be in compliance with laws and regulations and should ensure that the interests of aquaculture producers, especially of small-scale producers are taken into account. Certification should ensure stakeholder involvement and community issues to minimize conflicts with local communities, including issues of land tenure, access to traditional fishing grounds, land and water use, and sitting and resource use, rights, and needs. Certification should take into account labor issues and work conditions and should ensure that aquaculture addresses the following minimum substantive criteria regarding environmental impacts: a) environmental assessment and monitoring, b) sources and types of environmental impacts, and c) special and cumulative impacts. Certification schemes should ensure that aquaculture addresses the following criteria regarding food safety: a) feed and feed additives, b) residues, and c) traceability. Certification schemes should ensure that aquaculture addresses the following criteria: a) health and welfare maintenance and bio-security and introduction of disease and transfer. Economic and financial issues should be taken into account at all stages of aquaculture to optimize economic benefits and avoid or minimize any negative economic or financial consequences. Corsin et al. (2007) assessed qualitatively ten out of more than 30 certification schemes applicable to aquaculture in the Asia-Pacific region. Among these ten were the above described schemes from the Global Aquaculture Alliance (GAA)/Aquaculture Certification Council (ACC), GlobalGAP, Naturland and Thai CoC. The descriptive analysis used a framework of 85 descriptors which included issues like the Code of Good Practice for setting social and environmental standards, developed by the International Social and Environmental Accreditation and Labelling Alliance (ISEAL), addressed the ISO Guides for Standardization and conformity assessment, the Article 9 on aquaculture development of the Code of Conduct for Responsible Fisheries (FAO, 1995), and the Principles for Responsible Shrimp Farming, developed by FAO 3 (2006). The methodology used for the qualitative assessment used a combination of descriptive methods coupled to a simple weighting method to indicate the degree of impact. Each descriptor was further examined for its impact on different stakeholder groups in terms of costs benefits. The stakeholders that were grouped together in the analysis included: certified farmers; workers in certified

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farms; neighboring farmers; other resource users; traders; processors; retailers; consumers; governments; the environment and animal welfare. The evaluation of costs and benefits based on the descriptors revealed that certification schemes tended to provide more benefits to consumers and governments, followed by the environment and neighboring certified farms, which benefited from the improved management in the certified farms. Certified farmers and their workers had negative values, mainly a reflection that compliance to standards generally represents a cost for certified businesses and, in consequence, for their employees. The highest value for certified producers was achieved by the Thai CoC, while the lowest value was obtained by GlobalGAP, which on the other hand had the highest consumer value, as a reflection of the number of issues covered by the scheme. When the costs and benefits were expressed as a proportion of the number of descriptors applicable for each scheme, a slightly different picture was observed; the Thai CoC was still the programme that most benefited producers. It was closely followed by most other schemes. World Wildlife Fund The World Wildlife Fund (WWF) has a history of developing certification standards. It helped develop and spin off the Forest Stewardship Council standards, and worked with Unilever in the United Kingdom to develop the Marine Stewardship Council and then spun it off as a separated entity. World Wildlife Fund's (WWF) interest in aquaculture began in 1994 with a study comparing the impacts of shrimp aquaculture and shrimp trawling to determine which system of producing shrimp was better. At that time WWF decided to focus its attention on identifying and dissemination on more sustainable shrimp aquaculture practices (WWF, 2007a). To identify and analyze the impacts of shrimp farming and Better Management Practices (BMPs) and to reduce them WWF joined the Consortium on Shrimp Farming and the Environment. Research by the Consortium indicated that shrimp aquaculture had only 8-10 major impacts that accounted for 80-90 percent of all problems and that any individual operation probably had only five or fewer activities that were responsible for the bulk of its impacts. BMPs can effectively address these impacts and a BMP-based certification program will effectively minimize the environmental impacts of shrimp farming (WWF, 2007b).

WWF has identified four main areas of concern which must be addressed by any certification program aiming to influence the long-term sustainability of the shrimp farming industry. These areas are: a): Environmental issues (farm design, feed management, water use and pollution, energy consumption, ecosystem and biodiversity, shrimp escapes), b) socioeconomic issues (labor, community impact and livelihoods), c) animal welfare and health (broodstock, disease, prevention and medication), and d) standard development and verification procedures (development, governance and criteria, conformity assessment and verification, standard subject and chain of custody). In a benchmarking study WWF evaluated eight shrimp certification programs. This study revealed most of the analyzed standards have significant shortcomings and lack an effective and credible regulatory framework, and only organic shrimp certification programs performed well. However, none of the standards analyzed was in full compliance with the criteria stated and defined, showing that there is a lot of room for improvement and further adaptation of regulatory frameworks of shrimp certification programs (WWF, 2007a). At the moment WWF is creating on the basis of the International Principles for Shrimp Responsible Shrimp Farming (FAO et al. 2006) its own framework for developing criteria, indicators and standards for shrimp farming. The criteria will aim to provide direction on how to reduce each impact and the indicators will address how to measure the extent of each impact. Standards will be quantitative performance levels that evaluate whether a principle is achieved. The global principles, criteria and indicators will be the same for every country, but the performance levels may differ among different countries and regions, among shrimp species having different requirements, and production systems with different performance levels (Rosenberry, 2007). WWF is working together with shrimp farmers in Madagascar and Belize to adapt shrimp standards and to create standards for certifying shrimp aquaculture products, and WWF will meet with shrimp farmers in Vietnam to receive input on the development of global aquaculture standards and how small-scale shrimp farmers can be brought up to the International Principles for Shrimp Responsible Shrimp Farming. Additionally through Shrimp Aquaculture Dialogues, where multi-stakeholders (shrimp producers, NGOs, academics, government officials, retailers) identify and agree on 6-8 key impacts of

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shrimp farming and from this baseline data for the key impacts are developed to use as benchmarks and measurable performance-based standards for certifying farmed shrimp products will be established. Dialogue participants are creating standards for shrimp farms in East Africa, Central America/Mexico and Asia. The first Dialogue meeting was held 2007 in Madagascar, and another meeting followed 2008 in Belize. By working in Asia, the Dialogue will ensure that the standards will address the needs of small-scale producers (WWF, 2007c). WWF will hand off the developed standards for shrimp farming to an independent standards-holding body , the compliance of the standards will be audited by a third party accredited entity, and auditing and certification of a single farm or production unit will be performed (Villalon, 2008). To influence the long-term sustainability of the shrimp farming industry WWF has identified main areas of concern which must be addressed by any certification program. These areas are: a) environmental issues (farm design, feed management, water use and pollution, energy consumption, ecosystem and biodiversity, shrimp escapes), b) socioeconomic issues (labor, community impact and livelihoods), c) animal welfare and health (broodstock, disease, prevention and medication), and d) standard development and verification procedures (development, governance and criteria, conformity assessment and verification, standard subject and chain of custody), e) food safety, and f) economic/financial issues. All these factors influence the sustainability of a given aquaculture system. Independent Organizations To facilitate the institutional design of a sustainable aquaculture ecolabel and to judge the credibility and effectiveness of existing or planed aquaculture labels, the Environmental Law Institute (ELI) and The Ocean Foundation (TOF) developed a Gold Standard for sustainable aquaculture ecolabeling (Environmental Law Institute/ The Ocean Foundation, 2008a, b). The Gold Standard provides an institutional design framework that is a necessary first step to the development of an ecolabel that certifies only facilities that achieve environmental, social, and economic sustainability. According ELI/TOF none of the existing initiatives explicitly base their certification requirements on sustainability of production, instead choosing to focus on reducing the harm caused by exis-

ting production systems. The success of ecolabels is determined by the degree to which they catalyze environmental and social improvement and convert sustainable production into standard practice. Environmental and socioeconomic improvement is a function of the number of producers who adopt the ecolabel's standards, which is in turn affected by consumer demand for certified products. Thus, the fundamental task of the ecolabel is to connect certified producers with institutional and individual consumers who buy their goods. The effectiveness of this process largely depends on the credibility of the label's institutional structures and substantive standards and the pragmatic benefits of ecolabeling for producers (Environmental Law Institute/ The Ocean Foundation, 2008a, b). ASEAN Shrimp Alliance The ASEAN shrimp Alliance (ASA) is working to establish a regional certification body to verify the production standards of shrimp raised in member countries for export. It aims at lessening pressure from shrimp importing countries, which have set different restrictive standards against imported shrimp. While the standards, considered by some as safeguard measures, share some similarities, they eventually add to shrimp farmerÂ´s costs. Some countries have imposed restrictive import standards not only to protect local consumers but also for commercial purposes. Tighter rules could end up pushing the prices of imported products. The organization aims to help improve shrimp farming among member countries and overcome export obstacles (InfoFish International, 2009). DISCUSSION Certification schemes are best conducted by a recognized and independent third-party organization having a written or equivalent assurance that the product, process, or service conforms to specified requirements. Certification may include a range of inspection activities which could include continuous inspection in the production chain. Typical examples of conformity assessment activities are: sampling, testing and inspection, evaluation, verification and assurance of conformity (suppliers' declaration, certification); registration, accreditation, and approval in any combination. However, probably the most difficulty in the future will be to avoid the confusion of the consumers being offered a great number of certified far-

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med shrimp with no clear information about what make them specifically different from each other. As guidelines for responsible aquaculture development are becoming commonplace, Ackefors and White (2002) presented a framework for developing best environmental practices concerning the environment, aquatic ecosystem, water management, physical and chemical factors, biotic factors, regulation, monitoring, feed and feeding, feed quality, feed management, reduction in organic wastes, pathogens, product quality, and consumer safety, and trends in consumer preferences. In their recommendations they concluded that a Code of Conduct must be designed around the interests of the farm animals themselves (their life histories, physiology, and behavior, together with culture technology and pre- and post-harvest handling), the environment of the farm site, as well as the interests of local people, considering positive and negative impacts on their social and economic environment. Today the various standards for shrimp farming and certification schemes include systems that are organized and driven in different ways, including national and international levels, private and public sectors, second and third party certification, and organic and non-organic practices. Some concentrate on environmental issues and sustainability and touch on community and employee relations, others seek accreditation or try to establish recommendations to develop their codes of practice or improve shrimp farming practices. All of this is leading to proliferation of certification standards and systems (Phillips et al., 2005). Ironically, when the various codes, declarations, and guidelines are examined they are more alike in their language and professed goals than they differ. "Words are nice, but effective government-mediated and enforced action that implement the principles of sustainability of shrimp farming is much better" (Barnhizer, 2002). Or as Greenpeace (1999) commented "With regard to laws that are said to be on the books in most countries where shrimp farming has become a problem, experiences have shown that what regulations there may be to enforce on shrimp farm operations will simply not be enforced in the main. There are many reasons why, from lack of resources, difficulties in implementation, to corruption, among others". The creation of an effective legal and regulatory system, and im-

proving monitoring and enforcement and the willingness to impose legitimate sanctions are critical parts of efforts to enhance the sustainability of shrimp aquaculture. A combination of political pressure in the producing countries through economic leverage wielded in the consuming countries could bring a change. Regulations may be put in place, implemented and enforced, but as long as the consumers in rich countries demand cheap shrimp or refuse to pay more for responsibly-produced shrimp, the pressure on tropical coasts and wetlands and the people dependent on their continued quality will remain high. One recourse is to call upon the conscience of the consumers. A stronger option is to ask the buyers not to buy under-priced farmed shrimp as long as the social and environmental costs are not considered (Barnhizer & de la Torre, 2003). Government departments reacted against this call for shrimp boycott by strengthening educational efforts at the farmer level and stringent quality controls at processing plants. The efforts by ThailandÂ´s Department of Fisheries were described above; the Agriculture, Fisheries and Conservation Department, Hong Kong, published series of Good Aquaculture Practices that registered shrimp farmers need to comply to be certified, and recently the government of Sonora, the most important shrimp farming state in Mexico, requires that shrimp farmers have to take courses in Appropriate Aquaculture Production Practices (BAPP) to be certified and by this to promote sustainable shrimp production methods and for the farmer to obtain a higher market price for their shrimp. Regional, national and international private and non government organizations increased their efforts to develop their own codes of practice and certification schemes for shrimp farming with the aim to make it clear that the certified shrimp not only complies with food quality and safety standards, but also that it is produced on the farm by minimizing detrimental environmental and social impacts, and ensuring a responsible approach to worker health and safety as well as animal welfare win the confidence of the consumer the certification body. The steady increase in the sales of certified shrimp shows that the efforts to develop for farmed shrimp codes of practice and certification schemes were successful. In areas such as food safety, animal health and environmental sustainability, government authorities have enacted laws and regulations

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and developed inspection and certification programs to enforce their application. To guarantee to the consumer a safer product and to reduce for the shrimp producer the costs for inspection the U.S. Food and Drug Administration (FDA) with colleagues in the EU and Australia have started a pilot project to develop common standards and certification, and shared inspections. Additionally FDA initiated on pilot-scale a third-party food safety certification programme for the shrimp industry, and is drafting guidelines for third-party certification schemes to ensure certified products meet FDA requirements. To participate in the programme one or more third-party certification agencies would be chosen (Anon., 2008). Reacting on long-time complaints from non-government organizations about the illegal construction of shrimp ponds in mangrove areas, especially in Ecuador, in October 2008 the president ordered that all shrimp farms located in bays and beaches have to undergo a census, have to pay taxes and reforest mangrove areas. About 40% of the land occupied by shrimp farms in Ecuador are illegal, since they have no official permission to use the land, are located at beaches and bays and have been accustomed to live in freedom from punishment (Anon. 2008a). Yes, even organic shrimp certifiers were blamed to have certified illegal farms constructed in mangrove areas (C-Condem, 2007). The step of the Ecuadorian government is important to enforce that all (also the wealthy shrimp pond owners) have to respect the law, since the anarchy hurts everybody. To facilitate the institutional design for sustainable shrimp farming and to judge the credibility and effectiveness of existing or planed certification schemes is the first step that only facilities can be certified complying with national/international laws, and that achieve environmental, social, and economic sustainability. As Ababouch (2008) reports that several recent developments are likely to lead to an expanded use of certification in shrimp farming. These include a) the increasing influence and concerns of civil society related to health, social and environmental issues, b) legal requirements on companies to demonstrate "due diligence in the prevention of food safety risks" c) growing attention to "corporate social responsibility"' and a drive by companies to minimize "reputational risks" d) globalization of supply chains and a trend towards

vertical integration through the use of direct contracts between suppliers and retailers, and e) expansion of supermarkets in food retailing both nationally and internationally. The ongoing work in FAO and WTO, organizations that provide an international framework to ensure transparency, will continue to promote the development of science-based standards, harmonization and equivalence, in coherence with WTO trade measures and the standards if international standards setting bodies such as the Codex Alimentarius and the World Animal Health Organization. This may lead to an environment in which private standards and certification schemes complement and add value to the work of governments rather than duplicating it. If supported with appropriate technical assistance, such developments are likely to have positive economic implications, especially for small-scale aquaculture producers in developing countries (Ababouch, 2008). Memoranda of understanding, mutual recognition and equivalence agreements, and unilateral recognition may be developed for recognition of equivalence of aquaculture certification schemes, all of which need to include appropriate controls and verification of the certification systems involved. Tools and technical assistance may be required to ensure fairness, transparency and uniformity in developing equivalence agreements and monitoring that facilitates the development and implementation of aquaculture certification schemes consistent with the accreditation and standards development procedures provided in the FAO Technical Guidelines on Aquaculture Certification, and FAO will facilitate and monitor implementation of them (FAO, 2008). In view of these positive developments in voluntarily or prescribed by governments adopting codes of conduct and certification schemes, one important point remains to be considered. By using codes of conduct and certification schemes developed by organizations supported by aquaculture businesses and scientists, there is the danger that the schemes protect industrial shrimp farming and neglects social aspects of resource-poor shrimp farmers and their communities. Standards and certification schemes should not only focus on the benefits and requirements of the consumer, but also especially the small-scale the producers, and their farm management practices.

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Increasing consumer awareness in developed country markets and new developed/developing countries and the willingness to pay more for certified products led to a proliferation of shrimp farming standards and certification at the national, regional and international level. The lack of equivalence arrangements in certification standards poses the risk that a certification scheme looses credibility by bad schemes or schemes that do not to live up to expectations. There is an urgent need for more globally accepted standards and certification guidelines, especially for small-scale producers, to provide guidance, serve as a basis for improved harmonization, and facilitate mutual recognition and equivalence of certification schemes. Additionally, the increasing number and different approaches for shrimp certification makes it difficult for producers and consumers to choose the right scheme. To solve these problems, the efforts of the FAO and the World Wildlife Fund are the most important for harmonizing the different standards and certification schemes for the benefit of producers and consumers. ACKNOWLEDGEMENTS Thanks to those who have taken time to critically review and improve several versions of this manuscript. Special thanks to Domenico Voltolina and Derek Hall for suggestions and for critical editorial comments. This study was supported by COFAA and EDI grants from the Instituto Politécnico Nacional of Mexico.of this manuscript. Special tanks to Domenico Voltolina and Derek Hall for suggestions and for critical editorial comments. This study was supported by COFAA and EDI grants from the Instituto Politécnico Nacional of Mexico. REFERENCES Ababouch, L. 2008. Certification in aquaculture: Additional value or cost? FAO Aquaculture Newsletter, 40: 36-37. Ackefors, H. & P. White. 2002. A framework for developing best environmental practices for aquaculture. World Aquaculture, 33(2): 54–59. Alam, S.M.N., C. Kwei Lin, A. Yakupitiyage, H. Demaine & M.J. Phillips. 2005. Compliance of Bangladesh shrimp culture with FAO Code of Conduct for responsible fisheries: a development challenge. Ocean & Coastal Management, 48: 177–188.

ACC

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Anon. 2008. Pilot project on third-party food safety certification. INFOFISH International 5: 44-45. Anon. 2008a. Ecuador: Ejecutivo anuncio decreto en sector camaronero. Oct. 8, 2008 http:/www.mercuriomanta.com. Bailey, C. 1988. The social consequences of tropical shrimp mariculture development. Ocean & Shoreline Management, 11: 31–44. Barbier, E. & M. Cox. 2004. An economic analysis of shrimp farm expansion and mangrove conversion in Thailand. Land Economics, 80: 389–407. Barg, U., R. Subasinghe, R. Willmann, K. Rana & M. Martinez. 1999. Towards sustainable shrimp culture development: Implementing the FAO Code of Conduct for Responsible Fisheries (CCRF), 64–81 In: B.W. Green, H.C. Clifford, M. McNamara & G.M. Montaño (eds.). Fifth Central American Symposium on Aquaculture, 18–20 August 1999, San Pedro Sula, Honduras. Barnhizer, D. 2002. Innovation and the implementation deficit: Assessing shrimp producing countries based on their effectiveness in implementing the FAO’s Code of Conduct for Responsible Fisheries and Related Guidelines and Standards in the Context of Shrimp Aquaculture. Report prepared for the World Bank, NACA, WWF, and FAO Consortium on Shrimp Farming and the Environment, Bangkok, Thailand. Barnhizer, D. & I. de la Torre 2003. Of standards, regulations, and market campaigns: Going beyond the rhetoric, 465-499. In: I. de la Torre & D. Barnhizer (eds.). The blues of a revolution: The damaging impacts of shrimp farming. The Industrial Shrimp Action Network (ISA

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Hempel, E. & U. Winther. 1997. Shrimp farming and the Environment. Draft report to the World Bank, KPMG Centre for Aquaculture and Fisheries. Trondheim, Norway. Holmström, K., S. Gräslund, A. Wahlström, S. Poungshompoo, B.E. Bengtsson & N. Kautsky. 2003. Antibiotic use in shrimp farming and implications for environmental impacts and human health. International Journal of Food Science & Technology, 38: 255–266. InfoFish International. 2009. ASEAN plans to set up body to certify shrimp. InfoFish International, 4: 26-28. Islam, M.S. 2008. From pond to plate: Towards a twin-driven commodity chain in Bangladesh shrimp aquaculture. Food Policy, 33: 209-223. Kearney Gaillard, T., S. Masarrat Quader & R. Linowes. 2006. The shrimp seal of quality program. Dhaka, Bangladesh, 10-15. In: R. Linowes (ed.) Portraits of business practices in emerging markets: Cases for management education. Volume 4. Institute of International Education, and USAID, Wahington, D.C. http://emdacasebook.iie.org/pdfs/4.10%20Shrimp%Ce rtification-Bangladesh.pdf. MSCRI (Marine Shrimp Culture Research Institute, Thailand Department of Fisheries), 2003. Code of Conduct. http://thaiqualityshrimp.com/eng/coc/home.asp Naturland. 2004. Naturland certified organic. Naturland standards for organic aquaculture, 16–19. In: Naturland e.V., Pond culture of shrimps (Western white shrimp Litopenaeus vannamei and others. Gräfelfing, Germany. http://www.naturland.de/englisch/n2/aquaculture_01_2004 Naturland. 2006. Richtlinien für die Ökologische Aquakultur. 18–21. In: Pond culture of shrimps (Western white shrimp Litopenaeus vannamei and others), Gräfelfing, Germany.

Nissapawanich, B. 2007. Shrimp industry refutes Wal-Mart claims. Infofish International, 5: 26–28. Páez-Osuna, F. 2001. The environmental impact of shrimp aquaculture: Causes, effects, and mitigating alternatives. Environmental Management, 28: 131– 140. Páez-Osuna, F., S.R. Guerrero-Galván & A.C. Ruíz-Fernández 1999. Discharge of nutrients from shrimp farming to coastal waters of the Gulf of California. Marine Pollution Bulletin, 38: 585–592. Phillips, M.J., R. Subasinghe & A. Padiyar. 2005. Shrimp farming, the environment and trends towards certification: What are the issues and where are we going? 18–24. In: S. Subasinghe, T. Singh & A. Lem (eds.). The production and marketing of organic aquaculture products. Proceedings of the Global Technical and Trade Conference, 15–17 June 2004, Ho Chi Minh City, Vietnam. INFOFISH Kuala Lumpur, Malaysia. Phillips, M., R. Subasinghe, J. Clausen, K. Yamamoto, C.V. Mohan, A Padivar & S. Funge-Smith. 2008. Aquaculture production, certification and trade: Challenges and opportunities for the small-scale farmer in Asia. Aquaculture Asia Magazine, 13: 5–8. Pongthanapanich , T. & E. Roth. 2006a. Toward environmental responsibility of Thai shrimp farming through a voluntary management scheme. htttp://www.busieco.ou.dk/ime/PDF/ime/pongthanapanich 70.pdf Pongthanapanich, T. & E. Roth. 2006b. Country review: Voluntary management in Thai shrimp farming. Aquaculture Economics & Management, 10: 265–287. Primavera, J.H. 1993.. A critical review of shrimp pond culture in the Philippines. Reviews in Fisheries Science, 1: 151–2001.

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Primavera, J.H. 1997. Socio-economic impacts of shrimp culture. Aquaculture Research, 28: 815–827. Primavera J.H., C.R. Lavilla-Pitogo, J.M. Ladja & M.R. Dela-Peña. 1993. A survey of chemical and biological products used in intensive prawn farms in the Philippines. Marine Pollution Bulletin, 26: 35–40. Public Citizen. 2004. Shell game: The environmental and social impacts of shrimp aquaculture. A special report by Public Citizen’s Food Program. Washington, D.C.

Stevenson, J.R., X.T. Irz, J.H. Primavera & G. Sepulveda. 2003. Coastal aquaculture systems in The Philippines: Social equity, property rights and disregarded duties. In: CD-Rom Proceedings of: Rights and Duties in the Coastal Zone: Multidisciplinary Scientific Conference on Coastal Management, 12–14 June 2003. Beijer Institute of Ecological Economics, Stockholm, Sweden. Stonich, C.S.& C. Bailey. 2000. Resisting the blue revolution: Contending coalitions surrounding industrial shrimp farming. Human Organization, 59: 23–36.

Rosenberry, B. 2007. World Wildlife Fund developing global standards for aquaculture. Shrimp News International. http://www.shrimpnews.com/WorldWildlifeFundStandards.html

Stonich, C.S. & P. Vandergeest. 2001. Violence, environment, and industrial shrimp farming, 261-286. In: N. Lee Peluso & M. Watts (eds.) Violent environments. Cornell University Press, Ithaca and London.

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Subasinghe, R.P. & M.J. Phillips. 2007. Aquaculture certification: A challenge for the small farmer? FAO Aquaculture Newsletter, 38: 34–36.

SIPPO (Swiss Import Promotion Programme), Naturland & IMO (Institute for Marketecology. 2002. International standards for organic aquaculture. Production of shrimp. 9–18. Zürich, Switzerland and Gräfelfing, Germany. http://www.sippo.ch/files/publications/fish_shrimp2002.pdf Solidarity Centre. 2008. The degradation of work. The true cost of shrimp. http://www.solidaritycenter.org/files/pubs_TrueCost-of_Shrimp.pdf SSNC (Swedish Society for Nature Conservation). 2005. Eco-labelling of shrimp farming in Ecuador – Mangrove devastation, illegal farms and exclusion of local inhabitants. Stockholm, Sweden.

Uppsala University. 2008. Global trade in tiger shrimp threatens environment. http:// www.sciencedaily.com/releases/2008/02/080214114510.htm. Vandergeest, P. 2007. Certification and communities: Alternatives for regulating the environmental and social impacts of shrimp farming. World Development 35: 1152–1171. Valiela, I., J.L. Bowen & J.K. York. 2001. Mangrove forests: One of the world´s threatened major tropical environments. BioSciences, 2001: 807-815. Villalon, J.R. 2008. Aquaculture dialogues: A model process. http://library.enaca.org/certification/washington08/presentation-villalo.pdf

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Van Mulekom, L., A. Axelsson, E.P. Batungbacal, D. Baxter, R. Siregar, I. de la Torre & SEAFish for Justice. 2006. Trade and export orientation of fisheries in Southeast Asia: Under-priced export at the expense of domestic food security and local economies. Ocean & Coastal Management, 49: 546–561.

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NOTAS

CICIMAR Oceánides, 24 (2): 153-159(2009)

ANALYSIS OF THE VERTICAL DISTRIBUTION OF THE ABUNDANCE OF SMALL PELAGIC FISH LARVAE IN THE GULF OF CALIFORNIA USING SUBMARINE VIDEOCAMERAS Análisis de la distribucion vertical de la abundancia de larvas de peces pelágicos menores en el Golfo de California mediante videocámaras submarinas RESUMEN. Se utilizaron dos tipos de videocámaras submarinas para estudiar la distribución y abundancia vertical de larvas de los peces pelágicos menores Engraulis mordax, Etrumeus teres y Sardinops sagax a 1 m de resolución, en una localidad en el norte del Golfo de California con condiciones de calma y alta densidad de sardinas adultas. La mayor abundancia promedio (900 larvas m -1 min -1) se encontró inmediatamente arriba de la termoclina (33 m) y la picnoclina (36 m), aparentemente no asociada al máximo de clorofila detectado en superficie, ni a la mayor densidad de peces adultos (10 -20 m). Las observaciones con video permitieron determinar la distribución vertical a una resolución imposible de obtener mediante muestreos con redes; sin embargo, esta es una técnica poco útil en zonas con elevada velocidad de las corrientes. Aceves-Medina, G1 , C.J. Robinson2, R. Palomares-García, 1, & J. Gómez-Gutiérrez1. 1 Centro Interdisciplinario de Ciencias Marinas, Departamento de Plancton y Ecología Marina, Av. IPN s/n, Col. Playa Palo de Santa Rita, A.P. 592, La Paz, Baja California Sur, C.P. 23096, México. 2Laboratorio de Ecología de Pesquerías, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, A.P. 70–305, C.P. 04510, México, D.F. Aceves-Medina, G, C.J. Robinson, R. Palomares-García & J. Gómez-Gutiérrez. 2009. Analysis of the vertical distribution of the abundance of small pelagic fish larvae in the Gulf of California using submarine videocameras. CICIMAR Oceánides, 24(2): 153-159.

Marine pelagic fish larvae inhabit a three-dimensional space where there are pronounced vertical and horizontal gradients in temperature, light, food supply, and currents. These vertical environmental gradients can affect the vertical distribution, abundance, survival, and aggregation behavior of ichthyoplankton (Leis, 2004). Using current technological Fecha de recepción: 07 de mayo, 2009

capabilities, the environmental gradients can be measured in small spatial scales (centimeters to meters) but the acquisition of biological information that would match such small spatial scales is highly challenging to obtain. Most ichthyoplankton studies depend on nets that provide integrated samples (at specific strata) to infer broad fish egg and larvae vertical distribution patterns (Wiebe & Benfield, 2003). Light traps are occasionally used but such studies take two or at most three levels per sampling location with considerable different species composition than zooplankton collected with nets (Brogan, 1994a, b). Modern “high-tech” nets that open and close the nets electronically like the MOCNESS or BIONESS systems provide multiple stratified levels per trawl (up to 20 nets but usually nine are used ) (Wiebe & Benfield, 2003). However, those systems are expensive, time consuming, and provide little evidence of in situ behavior of the early life history of demersal, benthic, and pelagic fishes due to their relatively coarse vertical sampling resolution (several meters width strata). Thus, the acquisition of in situ high resolution information on vertical distribution and abundance of fish larvae has been for long time recognized as a critical methodological problem in zooplankton ecology (Wiebe & Benfield, 2003). Hydroacoustic surveys can provide detailed records of zooplankton density in vertical space scales of centimeters (> 20 cm) (Gómez-Gutiérrez & Robinson, 2006). However, it is virtually impossible to identify the species based exclusively on the echo-information without complementary information from nets and/or video cameras to detect and identify the numerically dominant organisms from the sound scattering layers (Wiebe & Benfield, 2003). Unfortunately, fish larvae usually have low absolute densities in the zooplankton community. The lack of rigid structures or a not yet developed swim bladder to be detected by echosounder sound, make the use of hydroacoustic techniques particularly unsuitable to estimate distribution and abundance of fish larvae. Greene and Wiebe (1990) and BenFecha de aceptación: 28 de septiembre, 2008

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field et al. (1996) demonstrated the utility of Remote Operated Vehicle (ROV) video observations to study micro distribution of zooplankton and micronekton that numerically dominate the zooplankton community structure. In November 2005 an oceanographic cruise was carried out to estimate distribution and abundance of small pelagic fish (19 oceanographic stations) measuring the oceanographic conditions and biological samples from plankton and micronekton (Aceves-Medina et al., 2009). Here we show that under exceptional calm observational conditions (current speeds <50 cm s-1), submarine video camera observations can be useful to describe high resolution fish larvae vertical distribution (<1 m) estimating their abundance and observing their in situ behavior, previously observed only under laboratory conditions (Hunter, 1981). In future studies, such in situ ROV video camera observations may help to understand the fish larvae habitat preferences during their transient meroplanktonic phase. Two high resolution submarine video cameras were deployed to observe zooplankton and micronekton at 46 locations where an hydro-acoustic survey (SIMRAD EY60, 120 kHz, split beam) showed dense sound scattering layers at the north and central part of the Gulf of California (November 2005) (Fig. 1). The video-camera system used included: 1) a ROV, Seabotix, equipped with color and black & white video cameras, underwater lamp, and temperature and depth sensors and 2) a Multi SeaCam camera (Deep Sea Power & Light, lens f = 2.8 mm, field depth 0.1 m to infinite) equiped with a submarine lamp Ikelite of 50 Watts attached either to the ring of a 5-m length conical zooplankton net (with black mesh nets 333 µm, 0.25 diameter and 0.75 cm length cod-end) or to a metallic base with a 20 kg weight. At an oceanographic station (E41), located at 30.05°N, 112.54°W and carried out between November 25 (22:00 h) and November 26, (02:15 h), 2005 (Fig. 1), we detected a dense sound scattering layer using a scientific echosounder that simultaneous ROV video-camera observations identified as zooplankton aggregations and dense schools of

Figure 1. Sampling stations during the oceanographic cruise (November 18 to December 2, 2005) showing the location of the sampling station E41.

adult Pacific sardines (Sardinops sagax) (Fig. 2a). Zooplankton samples collected with a 1-m ring diameter drifting net (DN, 10 min duration) equipped with the Multi SeaCam videocamera showed the presence of larvae and adults of small pelagic fish. The net was sent to the depths of high plankton densities (detected as a dense sound scattering layer with the echosounder), sampling from the surface to 40 m depth water column as homogeneously as possible while the ship was drifting. During this period the video camera attached to the net showed large numbers of static and actively swimming white and opaque slender fish larvae (Fig. 2b). The zooplankton sample obtained was analyzed immediately onboard. The fish larvae collected and observed on the video were identified as members of the family Clupeidae and Engraulidae. Later we sent the ROV to a maximum depth of 50 m to variable downward and upward speed of about 2 m min-1 (Fig. 2b). All were seen at real time using a 91 cm flat Sony color television and recorded on a DVD for further counting of fish larvae. Exceptionally calm in situ conditions allowed notably clear zooplankton observations in the station E 41, but we did not measure the in situ current speed. Based on our previous experience of three oceanographic cruises at Bahía Magdalena, where Acoustic Doppler Current Profiler, hydroacoustic and video-cameras

DISTRIBUTION OF FISH LARVAE USING VIDEOCAMERAS

Figure 2. Measured variables at oceanographic station E41: a) Acoustic vertical profiles of abundance of small pelagic fish adult as detected by acoustics (black bars), dissolved O2 profiles (dotted line), temperature (continuous line), and ROV images of adult pacific sardines (Sardinops sagax) feeding near surface. Video complement gaps on acoustic information in surface; b) Vertical profile of fish larvae time-de-1pendent abundance using the ROV (grey bars, inds. min ), vertical profile of Chl-a (dashed line), sea water density (solid line) and, ROV images of sardine and/or anchovy larvae; c) Vertical distribution of accesory photosynthetic pigments.

were used simultaneously, we observed zooplankton clearly at current speed < 50 cm s-1 (Gómez-Gutiérrez & Robinson, 2006; Robinson et al., 2007). Thus, in the E41 station it is likely that current speed was < 50 cm s-1.

Using the ROV videotape, two independent observers simultaneously counted the number of larvae detected per 1-m layer bin guided by the depth displayed on the screen of the video while a third person controlled the video recorder at slow motion. Because the video-camera moved at different speeds at each depth layer, larval abundance was standardized as average number of fish larvae per meter width layer per minute (inds. m-1 min-1) dividing the number of larvae observed at each 1 m stratum in the time spent by the camera at such 1 m stratum. The average and standard deviation of fish larvae counted by each observer was not significant different (t-test, p<0.05; Observer 1 = 5.6 larvae m-1 min-1 with a standard deviation of 2.44 larvae m-1 min-1 and observer 2 = 6.7 larvae m-1 min-1 with a standard deviation of 2.41 larvae m-1 min-1). Additionally, we did a standard oblique Bongo trawl (333 and 505 µm mesh net) and a 10 minutes surface horizontal trawl (SN) with a conic 0.6 m diameter net (505 µm mesh net). These plankton nets had digital flow meters to estimate the filtered water volume. All the fish larvae were sorted out from the complete Bongo 505 µm and surface nets samples and standardized as inds. m-3. For the fish larvae collected with the drifting net (non quantitative sample) the abundance was reported as total number of larvae collected in the tow and expressed in relative abundance (%) (Table 1). At each oceanographic station, including the E41 station, we did a CTD cast (General Oceanics Mark III) to 200 m depth and sampled seawater with 5 L Niskin bottles at 0, 5, 10, 25 and 50 m depth to measure dissolved oxygen concentration with an oxymeter YSI-1556. From each Niskin bottle we filtered 350 ml of water with GF/F filters (0.7 µm) and froze them with liquid nitrogen to estimate photosynthetic and accessory pigment concentration using High-Performance Liquid Chromatography with Fluorescence Detection (HPLC-FD) (Vidussi et al., 1996). All these observations were similarly done in the rest of the 18 oceanographic stations, but only at E41 station the low current speed conditions and the large density of fish larvae (of a relatively large size) allowed to do detailed observations of behavior and visual estimations of small pelagic fish larvae densities.

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Table 1. Fish larvae species abundance -3collected at station E41. (BN) = Bongo 505-Âľm net; (SN) = surface neuston net with standardized abundance to inds. m . (DN) = Total number of larval collected with drifting net expressed in relative abundance (%). Abundance per net type Family

Mictophidae

-3

Fish larvae species

Ind m or total number

Benthosema panamense

Relative abundance

472.1

284.3

119

52.3

69.0

48.4

27.1

12.7

39.0

Engraulidae

Engraulis mordax

244.0

52.2

Scombridae

Scomber japonicus

79.6

11.6

8.8

2.8

2.9

Clupeidae

Etrumeus teres

5.3

29.0

0.6

7.0

2.4

Clupeidae

Sardinops sagax

37.1

11.6

4.1

2.8

2.0

Gobiidae

Lythrypnus spp.

15.9

11.6

1.78

2.8

1.6

Citharichthys xanthostigma

10.6

5.8

1.2

1.4

2.4

Paralichthyidae

5.8

1.4

Serranidae

Pronotogramus multifasciatus

Mictophidae

Triphoturus mexicanus

10.6

Triglidae

5.3

0.6

0.4

Synodus sp.

5.3

0.6

0.4

Fistularia corneta

5.3

0.6

0.4

Triglidae Synodontidae Fistularidae

1.2

Nomeidae

Cubiceps paucirradiatus

5.3

0.6

Albulidae

Albula sp.

5.3

0.6

Video records indicated that most small pelagic fish larvae were static with their thin body straight (suggesting an energy saving strategy behavior under calm current speed conditions), but in response to mechanical and/or light stimulation from the videocamera they invariably escaped adopting a typical Sshape with short undulating swimming movements, followed by a sudden stretching movement that displaced the larvae forward (Fig. 2b). Similar behavior was observed in sardine larvae under laboratory conditions (Hunter, 1981). The fish larvae collected simultaneously with the drifting net (equipped with the video-camera) at the core of high larvae density had a standard length range of 17-21 mm. Fish larvae of this size range swam independently of each other with considerable distance between them with no evidence of schooling behavior. This suggests schooling behavior may develop in larger fish larvae. Ichthyoplankton taxonomic composition from the three zooplankton nets included 14 species from 12 families (Table 1). The myctophid

Benthosema panamense (48%-69%), northern anchovy Engraulis mordax (12%39%), jack mackerel Scomber japonicus (2.8%- 8.8%), round herring Etrumeus teres (0.6%-7.0%), and Pacific Sardine Sardinops sagax (2.03%-4.12%) accounted for 93%-95% of the total fish abundance for each type of net (Table 1). We did not collect eggs with any net used that otherwise would suggest recent spawning of the adult sardines observed at E41 oceanographic station or nearby locations. From all fish larvae species collected, only E. mordax, E. teres, and S. sagax matched the size and body shape observed in the videos. From the zooplankton samples the relative abundance of small pelagic fish larvae were E. mordax (77 %), E. teres (13%, particularly abundant in the neustonic sample), and S. sagax (10%) (Table 1). ROV videos (starting at 22:00 h local time) showed dense adult Pacific sardine schools feeding near the surface with the highest densities in the strata between 5 - 20 m depth and lower densities at

DISTRIBUTION OF FISH LARVAE USING VIDEOCAMERAS

deeper strata (Fig. 2a). Because the transducer of the echosounder was located 4-m below the sea surface and accounting for near field effect, acoustic data are available only for layers > 6 m depth. Using criteria of scattering volume < -50 dB and 50 pings of echogram analysis to detect juvenile and adult small pelagic fish schools (Robinson et al., 2007), the hydroacoustic information recorded at the E41 station confirmed the video-camera observations that most of the adult fish abundance (inds. ha-1) was located between 10 and 20 m depth (Fig. 2a). Fish larvae were not detected with the ROV video-camera in the first 4 m depth. Larvae were detected in low time-dependent densities (46 fish larvae m-1 min-1) between 5 - 26 m (Fig. 2b). The average of fish larvae time-dependent abundance increased to 103 fish larvae m-1 min-1 between 27 - 31 m depth showing the highest average densities (650 900 fish larvae m-1 min-1) between 32 - 33 m depth. The density of fish larvae decreased progressively at deeper strata (Fig. 2b). From the video-camera information it is not possible to estimate volume or area sampled. Thus, fish larvae abundance as a function of time is not comparable to densities estimated with traditionaly net methods (inds. m-3 or inds. m-2). The video count method can estimate unusually high maximum extrapolated larvae fish densities (compared with net collection) when the video camera spent little time at each 1-m depth bin and abundance was extrapolated to one minute (i.e. 1200 larvae m-1 min-1). This methodological problem can be solved if the video camera is deployed slowly (<1 m min-1) to avoid extrapolation of larval density to 1 minute intervals of observations per 1 m stratum. The apparently inverse vertical distribution pattern of adults and larvae, corroborated with video observations (Fig. 2b), might suggest high larval mortality from predation by the schools of adult sardines located near surface waters or spatial ontogenetic segregation to avoid cannibalism. Near surface feeding of S. sagax and E. mordax during night time is a common observation at several sea regions (Krutzikowsky & Emmett, 2005; Robinson et al., 2007). Although several studies have not been detected large fish larvae (like those ob-

served in the video camera) in the stomach of adult small pelagic fish, Hayasi (1967) detected intensive cannibalism on eggs and small larvae of anchovies and sardines, and Buttler (1991) showed robust statistical evidence of cannibalism on anchovy and sardine larvae. Because small pelagic fish are not selective filtering feeders, it has been largely discussed if the northern anchovy can filter their own eggs and early larvae, thus they also may feed on larger fish larvae (Buttler, 1991). Hunter & Kimbrell (1980) reported that because of the thin integument of fish larvae and the rapid adult digestion rates, fish larvae are rarely found in the stomach content of adult anchovies. Our most likely explanation is that the vertical distribution pattern of small pelagic fish larvae in E41 responds to a complex vertical and horizontal ontogenetic segregation among fish eggs, larvae, and adults, as a potential strategy to avoid cannibalism. The highest small pelagic fish larvae abundance was detected just above the thermocline and pycnocline (Fig. 2 a, b), but not associated with dissolved oxygen concentration (4 - 4.4 mg L-1 in the first 25 m depth, equivalent to 75% oxygen saturation, and decreased to 3 mg L-1 at deeper strata) nor the depth of the chl-a maximum concentration detected at surface (Fig. 2c). In the southwestern part of the Gulf of California (Bahía de La Paz) the higher concentrations of fish larvae, including Opisthonema spp., was located above the pycnocline, which is the strata with maximum stability (16 - 48 m) (Sánchez-Velasco et al., 2007). In the coast of California the higher abundance of S. sagax was detected between 22 and 45 m depth (Watson, 1992). The average depth of maximum chl-a concentration in the first 75 m depth in the 26 oceanographic stations was 4 m (standard deviation = 5.6 m and about 50% of the stations had a maximum chl-a concentration at surface). This is a relatively shallow depth considering that November is a transition period where the mixing layer begins to develop. In July 2007 the maximum of chl-a was 19 m depth and in January 2007 30 m depth (Gómez-Gutiérrez et al., in press) suggesting that during November irradiance likely caused a smaller photo-inhibition process than in July. The fucoxantine and 19-hexanoy-

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loxyfucoxanthin (19-Hf) phytoplankton pigments (indicators of diatoms and cyanobacteria–prochlorophyta, respectively) (Jeffrey, 1974; Goericke & Repeta, 1993) had a pattern similar to chl-a suggesting that those groups were the most abundant phytoplankton components at this location (Fig. 2c). We did not detect significant association between the maximum densities of fish larvae and phytoplankton, which in theory should provide a suitable environment for feeding larvae (Fig. 2b). To our knowledge, except Sánchez-Velasco et al. (2007), there is no other study of vertical distribution of fish larvae in the Gulf of California to compare with our observations. Submarine videos allowed us to observe in situ small pelagic fish larvae in static resting behavior and vertical distribution at an unprecedented resolution (1 m depth). However, video-camera observations may overestimate fish larval densities compared with conventional net method estimations and was practically useless in the other 45 locations where we used the ROV during the oceanographic cruise (Fig. 1) because intense current speed conditions prevailed that prevented us to do reliable identification of zooplankton. High current speeds (>50 cm-1 s-1) may restrict video-camera observations to enclosed regions or video recording during transient calm sea conditions that can be specifically selected from tide tables to increase the probability of obtaing adequate observational conditions and increase the number of behavioral observations of fish larvae in situ. Even with these technical limitations, it is clear that video records are valuable complement of standard net sampling methods in the study of in situ fish larvae behavior that can not be obtained by other means in the field. ACKNOWLEDGEMENTS We thank the crew of the R/V ‘El Puma’, for their cooperation in collecting information. G.A.M., J.G.G, and C.J.R. are SNI fellows and G.A.M., J.G.G, and P.G.R. are COFAA-IPN and EDI-IPN fellows. Centro Interdisciplinario de Ciencias Marinas-IPN projects SIP-20090303, 20090267, 2008490 and 2009090, CONACYT-FOSEMARNAT 200401-144, CONACYT-SAGARPA 2005-717,

CONABIO, and Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México supported this study. We also thank four anonymous referees for their valuable critics to the manuscript. REFERENCES Aceves-Medina, G., R. Palomares-García, J. Gómez-Gutiérrez, C.J. Robinson & R.J. Saldierna-Martínez. 2009. Multivariate characterization of spawning and larval environment of small pelagic fishes in the Gulf of California. J. Plankt. Res., 31: 1283-1297. Benfield M.C., C.S. Davis, P.H. Wiebe, S.M. Gallager, R.G. Lough & N.J. Copley. 1996. Video Plankton Recorder estimates of copepod, pteropod, and larvacean distributions from a stratified region of Georges Bank with comparative measurements from a MOCNESS sampler. Deep-Sea Res. II, 43: 1925-1945. Brogan, M.W. 1994a. Two methods of sampling fish larvae over reefs: a comparison from the Gulf of California. Mar. Biol., 118: 33-44. Butler, I.L. 1991. Mortality and recruitment of Pacific sardine, Sardinops sagax caerulea, larvae in the California Current. Can. J. Fish. Aquat. Sci., 48: 1713-1723. Brogan, M.W. 1994b. Distribution and retention of larval fishes near reefs in the Gulf of California. Mar. Ecol. Prog. Ser., 115: 1-13. Goericke, R. & D. Repeta. 1993. Chlorophylls a and b and divlnyl chlorophylls a and b in the open subtropical North Atlantic Ocean. Mar. Ecol. Progr. Ser., 101: 307-313. Gómez-Gutiérrez, J. & C.J. Robinson. 2006. Tidal current transport of epibenthic swarms of the euphausiid Nyctiphanes simplex in a shallow subtropical bay in Baja California Sur, México. Mar. Ecol. Progr. Ser., 320: 215-231. Gómez-Gutiérrez, J., Tremblay, N., Martínez-Gómez, S., Robinson, C.J., Del

DISTRIBUTION OF FISH LARVAE USING VIDEOCAMERAS

Ángel-Rodríguez, J., Rodríguez-Jaramillo, C. & Zavala-Hernández, C. In press. Biology of the subtropical sac-spawning euphausiid Nyctiphanes simplex in the northwestern seas of Mexico: Vertical and horizontal distribution patterns and seasonal variability of brood size. Deep-Sea Res II. Greene, C.H. & P.H. Wiebe. 1990. Bioacoustical oceanography: new tools for zooplankton and micronekton research in the 1990s. Oceanography, 3: 12-17. Hayassi, S. 1967. A note on the biology and fishery of the Japanese anchovy, Engraulis japonicus (Houttuyn). Calif. Coop. Oceanic Fish. Invest. Rep., 11: 44-57. Hunter, J.R., 1981. Feeding ecology and predation of marine fish larvae, 33-79. In: R. Lasker (Ed.) Marine fish larvae. Morphology, ecology, and relation to fisheries. University of Washington Press. Seattle. Hunter, J.R. & Kimbrell, C.A., 1980. Egg cannibalism in the Northern anchovy, Engraulis mordax. NOAA Fish. Bull. U.S., 78: 811-816. Jeffrey, S.W., 1974. Profiles of photosynthetic pigments in the ocean using thin-layer chromatography. Mar. Biol., 26: 101-110. Krutzikowsky, G.K. & R.L. Emmett. 2005. Diel differences in surface trawl fish catches off Oregon and Washington. Fish. Res., 71: 365-371.

Leis, J.M. 2004. Vertical distribution behaviour and its spatial variation in late-stage larvae of coral-reef fishes during the day. Mar. Freshwater Behav. Physiol., 37: 65-88. Robinson, C.J., S. Gómez-Aguirre & J. Gómez-Gutiérrez. 2007. Pacific sardine behaviour related to tidal current dynamics in Bahía Magdalena, México., J. Fish. Biol., 71: 1-19. Sánchez-Velasco, L., S.P.A. Jiménez-Rosenberg & M.F. Lavín. 2007. Vertical distribution of fish larvae and its relation to water column structure in the southwestern Gulf of California. Pac. Sci., 61(4): 533-548. Vidussi, F., H. Claustre, J.N. Bustillos-Guzman, C. Cailliau & J.C. Marty. 1996. Rapid HPLC method for determination of phytoplankton chemotaxonomic pigments: separation of Chl-a from divinyl-chlorophyll a and zeaxanthin from lutein. J. Plankt. Res., 18: 2377-2382. Watson, W. 1992. Distribution of larval Pacific sardine, Sardinops sagax, in shallow coastal waters between Oceanside and San Onofre, California: 1978-1986. Calif. Coop. Oceanic Fish. Invest. Rep., 33: 89-99. Wiebe, P.H. & M.C. Benfield. 2003. From the Hensen net toward four-dimensional biological oceanography. Prog. Oceanogr., 56: 7-136.

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SEA STARS (ECHINODERMATA: ASTEROIDEA) IN ROCKY REEFS OF GUADALUPE ISLAND, NORTHWEST MÉXICO Estrellas de mar (Echinodermata: Asteroidea) en arrecifes rocosos de Isla Guadalupe, Noroeste de México RESUMEN. El objetivo del trabajo fue describir la estructura comunitaria de las estrellas de mar en Isla Guadalupe, (28° N - 29° N), situada al oeste de la Península de Baja California. La zona fue visitada en Septiembre de 2008 y se hicieron 64 censos en 16 sitios (3,200 m2 revisados), tanto en áreas someras (0 a 10 m) como profundas (11 a 20 m). A partir de los conteos se calcularon los descriptores comunitarios de densidad y riqueza, diversidad (H') y uniformidad (J'). En la isla solo fueron observadas las especies Astrometis sertulifera, Pisaster giganteus y Linckia columbiae. El número total de individuos encontrados fue de siete y dada la baja abundancia, no se detectaron diferencias significativas entre sitios o niveles de profundidad con ninguno de los índices. No hay explicación para el bajo número de estrellas de mar en la zona de trabajo, pero considerando los bajos números de las poblaciones y que Isla Guadalupe es una Reserva de la Biosfera, se recomienda no otorgar permisos para extracción de estrellas de mar en la zona, dado que las especies encontradas forman parte del mercado de especies de ornato. Reyes Bonilla, H., S. González Romero & A. Mohedano Navarrete. Universidad Autónoma de Baja California Sur. Departamento de Biología Marina. A. P. 19-B, CP 23080. La Paz, B.C.S., México. Tel. (612) 123-8800 Fax:(612)123-8819. email: hreyes@uabcs.mx Reyes Bonilla, H., S. González Romero & A. Mohedano Navarrete. 2009. Sea stars (Echinodermata: Asteroidea) in rocky reefs of Guadalupe Island, Northwest México. CICIMAR Oceánides, 24(2):161-165.

Information on reef-associated sea stars (Echinodermata: Asteroidea) in the Mexican Pacific is detailed for tropical environments as evidenced by numerous species listings (Honey-Escandón et al., 2008), taxonomic monographs (Cintra-Buenrostro, 2001), and data on community structure (Herrero-Pérezrul et al., 2008). However, there is still a dearth of information for temperate Pacific reefs of México, Fecha de recepción: 10 de agosto, 2009

as there is not a single paper covering aspects of abundance or distribution of this fauna, but isolated references and records from dredges and trawls mostly conducted in the early and mid-1900s (Maluf, 1988). The study of sea stars in subtropical and temperate environments is relevant because their usually high numbers and biomass, combined with their varied diet that allows them to integrate several trophic guilds (from detritivores to carnivores), makes them a key element in energy transfer along trophic webs (Micheli & Halpern, 2005). The objective of this paper is to improve our understanding of the temperate starfish assemblages in western México by analyzing the community structure of this taxon at the oceanic Guadalupe Island (Fig. 1), located 270 km west of the Baja California Peninsula. This area was declared a Biosphere Reserve in 2005, and has become famous by the presence of healthy populations of marine mammals, birds and white sharks, as well as an important fishing ground for abalone, lobster, sea cucumbers and other resources (Santos del Prado & Peters, 2008). The field work was performed during a six days visit (September 19-24, 2008). We conducted visual surveys in 16 sites around the island (Fig. 1). At each site we counted sea stars inside 25 x 2 m belt transects, placed parallel to the coastline and at two depth levels: “shallow” (-2 to -10 m depth), and “deep” (-11 to -20 m); as the protocol involved two transects at each deph/site, there was a total of 64 census, covering a total reef surface of 3,200 m2. From these data we calculated the following ecological indices: population density abundance (individuals per 50 m2 transect), richness (number of species per transect), Shannon's diversity (H´, base 10), and Pielou evenness (J´) as well as their average and standard errors for the island. We planned to perform statistical tests with all ecological variables in order to compare among sites and between depth levels, however the number of starfishes found in the transects was so low (see below) that it precluded the application of any test.

Fecha de aceptación: 07 de octubre, 2009

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the south (Santos del Prado & Peters, 2008), a probable consequence of the direct effect of the California Current. Finally, when considering depth levels L. columbiae and P. giganteus were found only between 2 and 10 m, while A. sertulifera appeared only in the deep zone (> 10 m).

Figure 1. Guadalupe island, México, indicating the locations that were surveyed in September 2008. Boxes indicate the sites where sea stars were observed.

We observed only three species of sea stars at Guadalupe Island: Linckia columbiae Gray, 1840, Astrometis sertulifera (Xantus, 1860) and Pisaster giganteus (Stimpson, 1857). According to Maluf (1988) the first two taxa have a distribution span from California (U.S.A) to the Galápagos Islands (Ecuador), and the latter ranges from Vancouver Island (Canada) to Cedros Island (México). Only seven individuals were found in the 64 transects (average of 0.109 ± 0.050 ind/50 m2); four of them were A. sertulifera, which was the most abundant species (0.062 ± 0.038 ind/50 m2) and appeared at La Vela and La Costilla (northeast sector of the island). Of the remainder, L. columbiae (average of 0.016 ± 0.016 ind/50 m2) were seen at Punta del Tiburón (west), and P. giganteus (average of 0.031 ± 0.021 ind/50 m2) at Punta del Tiburón and Campo Norte. Latitude may have influence on the presence of the sea stars as no individuals were sighted south of 29° N (Fig. 1). This trend points out to a common preference of these asteroids to live in lower temperatures because sea surface temperature in Guadalupe Island is about 1 °C colder in the north than in

The figures presented above are remarkably low. As a comparison, L. columbiae has a density of 0.13 ind/ 50 m2 in the Galápagos Islands (Edgar et al., 2004), about eight times higher than at Guadalupe, and P. giganteus populations in California can be at least one order of magnitude denser (Bomkamp et al., 2004). It is very difficult to assess why sea stars were so uncommon at Guadalupe Island since P. giganteus and A. sertulifera are voracious carnivores of mollusks, sea urchins and even fishes (Schmitt, 1982), all of which are abundant in the study area, whilst L. columbiae is a detritivore (Cintra-Buenrostro et al., 2008). Lack of suitable habitat for the species is not the answer as they are generalists and can be found in mussel beds, kelp beds, and even in rock barrens (Ricketts et al., 1992). Another possibility is that Guadalupe Island is located quite near of the northern or southern distribution limit of the three species (Maluf, 1988), and the suboptimal environmental conditions may cause physiological problems as those reported to occur in northern populations of the tropical seastar Phataria unifascialis (Gray, 1840) in the Gulf of California (Morgan & Cowles, 1997). Regarding predators, Newsome et al. (2009) indicated that P. giganteus is preyed upon by California sea otters, Enhydra lutris (L. 1758), but nevertheless this mammal is absent at Guadalupe Island, and there is no report of another significant sea star consumer known for this location. Finally, it is possible that the seastars carry out a bathymetric migration either for food, reproduction, or to avoid warmer water in summer, as all the species found are able to inhabit reefs deeper than -100 m (Maluf, 1988), and temperature in shallow water can increase several degrees during summer. We suggest that the most feasible explanation to our findings is that the low population density observed results from the erratic recruitment that characterizes sea stars, a con-

SEA STARS OF GUADALUPE ISLAND

dition which brings years of remarkable abundance, and others where local populations can become almost extinct (Uthicke et al., 2009). It is noteworthy that in other isolated islands of western México like Socorro and San Benedicto (Revillagigedo Archipelago, 18° N; Reyes-Bonilla, 1995) and in the Marías Islands (20°N; HRB pers. observ., 2007), the number of starfishes is also quite low. Possibly the success of the cohorts varies depending on the strength of the California Current and the presence (or lack of) eddies around the island, physical factors that eventually determine if larvae move away, or remain in site. The question merits further investigation but nevertheless, the low numbers of sea stars indicate that the ecological relevance of this group in rocky reefs of Guadalupe Island should be low, a clear contrast to what is known about the ecological importance of A. sertulifera and P. giganteus in southern California coastal reefs, where their numbers are much higher.

Ensenada, Tijuana, and also in flea markets of San Diego (pers. observ.). Piña Espallargas et al. (2002) and Lunn et al. (2008) documented some aspects of its trade. Considering the extremely low number of individuals seen during field work, we recommend the ban of any permission for capture of seastars at the island, as Addessi (1994) has documented how sensitive P. giganteus and A. sertulifera are to human perturbation, to the point of having populations disappear at Catalina Island, California.

Returning to the data analysis, we found out that the “shallow” depth level had slightly higher density than the “deep” one, but the figures were quite similar (0.12 ± 0.07 ind/50 m2 against 0.09 ± 0.06 ind/50 m2). Average asteroid species richness at Guadalupe Island was very low (0.09 ± 0.04 sp/50 m2), as well as diversity (H´) and evenness (J´) (0.011 + 0.011 decits/50m2, and 0.016 ± 0.016 units respectively) because the three indices had values of zero or one (for richness) in most transects but one, placed at 14.5 m deep at Punta del Tiburón, where one individual of L. columbiae and one of P. giganteus were found (resulting in H´= 0.17 ± 0.17 decits/50 m2, and J´= 0.25 ± 0.25 units). An examination of the literature confirmed that only the sea star assemblage from La Entrega, Oaxaca (Zamorano & Leyte-Morales, 2005) has so low richness, abundance, diversity and evenness values in western México reefs (Caso et al., 1996; Reyes-Bonilla et al., 2005).

ACKNOWLEDGMENTS

As indicated, Guadalupe Island is a Biosphere Reserve but notwithstanding the federal law allows for commercial fishing in the area, albeit limited in volume. Of the three seastar observed, Linckia columbiae and Pisaster giganteus are usually sold as souvernirs in curio stores at cities like Mazatlán,

Our study indicated that seastar populations in shallow rocky reefs of Guadalupe Island are remarkably low, and consequently the community structure of this group is quite simple, characterized by minimal richness and diversity. The ecological role of this taxon must be limited in this oceanic island, and we recommend that federal authorities ban any kind of extraction of specimens in order to not affect the populations.

This study was conducted with support from the administration of the Reserva de la Biosfera Isla Guadalupe (Nadia Citlali Olivares Bañuelos, Director), and Sociedad Cooperativa de Producción Pesquera de Participación Estatal Abuloneros y Langosteros S.C.L. Arturo Ayala and Israel Sánchez (UABCS) collaborated in the field work, and Juan José Alvarado (UABCS-Universidad de Costa Rica) and two anonymous referees provided recommendations to improve the content and presentation of the paper. REFERENCES Addessi, L. 1994. Human disturbance and long term changes on a rocky intertidal community. Ecol. Appl., 4: 786-797. Bomkamp, R.E., H.M. Page & J.E. Dugan. 2004. Role of food subsidies and habitat structure in influencing benthic communities of shell mounds at sites of existing and former offshore oil platforms. Mar. Biol., 146: 201-211. Caso, M.E., A. Laguarda-Figueras, F.A. Solís-Marín, A. Ortega-Salas & A. de la Luz Durán-González. 1996. Contribución al

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conocimiento de la ecología de las comunidades de equinodermos de la Bahía de Mazatlán, Sinaloa, México. An. Inst. Cienc. Mar Limnol. UNAM, 22: 101-119. Cintra-Buenrostro, C.E. 2001. Los asteroideos (Echinodermata: Asteroidea) de aguas someras del Golfo de California, México. Oceánides, 16: 49-90. Cintra-Buenrostro, C.E., H. Reyes-Bonilla & M.D. Herrero-Pérezrul. 2008. Oceanographic conditions and diversity of sea stars (Echinodermata: Asteroidea) in the Gulf of California, México. Rev. Biol. Trop., 53(sup. 3): 245-261. Edgar, G.J., S. Banks, J.M. Fariña, M. Calvopiña & C. Martínez. 2004. Regional biogeography of shallow reef fish and macroinvertebrate communities in the Galápagos Archipelago. J. Biog., 31: 1107-1124. Herrero-Pérezrul, M.D., H. Reyes-Bonilla, A. González-Azcárraga, C.E. Cintra-Buenrostro & A. Rojas-Sierra. 2008. Equinodermos, 339-361. En: Danemann, G.D. & E. Ezcurra (Eds.). Bahía de Los Angeles: recursos naturales y comunidad. Línea base 2007. INE/PRONATURA Noroeste. México, 740 p. Honey-Escandón, M., F.A. Solís-Marín & A. Laguarda-Figueras. 2008. Equinodermos (Echinodermata) del Pacífico mexicano. Rev. Biol. Trop., 56 (sup. 3): 57-73. Lunn, K.E., M.J. Villanueva-Noriega & A.C.J. Vincent. 2008. Souvenirs from the sea: an investigation into the curio trade in echinoderms from Mexico. TRAFFIC Bull., 22 (1): 19-32. Maluf L.Y. 1988. Composition and distribution of the central eastern Pacific echinoderms. Nat. Hist. Mus. Los Angeles County, Tech. Rep., 2: 1–242.

Micheli, F. & B. S. Halpern. 2005. Low functional redundancy in coastal marine assemblages. Ecol. Lett., 8: 391-400. Morgan, M.B & D.L. Cowles, 1997. The effects of temperature on the behaviour and physiology of Phataria unifascialis (Gray) (Echinodermata, Asteroidea): implications for the species distribution in the Gulf of California, Mexico. J. Exp. Mar. Biol. Ecol., 208: 13-27. Newsome, S.D., M.T. Tinker, D.M. Monson, O.T. Oftedal, K. Ralls, M.M. Staedler, M.L. Fogel & J.A. Estes, 2009. Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris). Ecology, 90: 961-974. Piña-Espallargas, R., H. Reyes-Bonilla, G. Ortuño-Manzanares, N.E. García-Núñez, L. Mendoza-Vargas & L.V. González-Ania. 2002. Recurso especies marinas de ornato, 877-914. En: Evaluación de los recursos marinos de México. SEMARNAT, México, D.F. Reyes-Bonilla, H. 1995. Asteroidea and Echinoidea (Echinodermata) from Isla San Benedicto, Revillagigedo Archipelago, Mexico. Rev. Inv. Cient. U.A.B.C.S., 6: 29-38. Reyes- Bonilla, H., A. González-Azcárraga & A. Rojas Sierra. 2005. Estructura de las asociaciones de las estrellas de mar (Asteroidea) en arrecifes rocosos del Golfo de California, México. Rev. Biol. Trop., 53 (sup. 3): 233-244. Ricketts, E.F., J. Calvin & J.W. Hedgpeth. 1992. Between Pacific tides. 5th ed. Stanford University Press, Stanford. 680 p. Santos-del Prado, K. & E. Peters (Eds.). 2008. Isla Guadalupe; restauración y conservación. Instituto Nacional de Ecología, México. 324 p.

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Schmitt, R.J. 1982. Consequences of dissimilar defenses against predation in a subtidal marine community. Ecology, 63: 1588-1601. Uthicke, S., B. Schaffelke & M. Byrne. 2009. A boom-bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol. Monog., 79: 3-24. Zamorano, P. & G.E. Leyte Morales. 2005. Cambios en la diversidad de equinodermos asociados al arrecife coralino de La Entrega, Oaxaca, MĂŠxico. Ciencia y Mar, 9(27): 19-28.

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FIRST RECORD OF Ceratium dens (DINOPHYCEAE) IN THE GULF OF CALIFORNIA Primer registro de Ceratium dens (Dinophyceae) en el Golfo de California RESUMEN. El dinoflagelado Ceratium dens, originalmente descrito del Océano Índico, se registra por primera vez en el Golfo de California y en el Pacífico Mexicano. Se examinaron todos los registros disponibles de C. dens. La distribución geográfica de esta especie es principalmente en aguas tropicales y subtropicales. La presencia de C. dens durante el otoño de 2009 en las aguas del Golfo de California parece relacionarse con condiciones del Evento de El Niño. Gárate-Lizárraga, I. Laboratorio de Fitoplancton. Departamento de Plancton y Ecología Marina. Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), A.P. 592, Col. Centro, C. P. 23000, La Paz, B.C.S., México, email: igarate@ipn.mx Gárate-Lizárraga, I. 2009. First record of Ceratium dens (Dinophyceae) in the Gulf of California. CICIMAR Oceánides, 24(2): 167-173.

Nine samples of sub-surface phytoplankton were collected in using a 20 mm mesh net and five samples with a 160 mm mesh net, during phytoplankton surveys in front of the Petroleos Mexicanos dock inside Bahía de La Paz (24° 13.2’ N and 110° 19.1’ W). Samplings were performed in September 22, October 20, and November 3, 2009. Likewise, three surface samples were collected to estimate phytoplankton abundance. Seawater surface temperature was measured with a bucket thermometer. Samples were preserved with an acidic Lugol solution and with 4% formaline. Phytoplankton abundance was estimated using sedimentation chambers and a inverted microscope. Photographic records were made using Olympus BX-41 and Zeiss Axiovert 40 C microscopes with included camera. Sample analysis yielded 25 identified taxa of the genus Ceratium: Ceratium balechii, C. breve var. parallelum, C. breve var. schmidtii, C. contortum var. contortum, C. contortum var. karstenii, C. declinatum f. normale, C. deflexum, C. dens, C. extensum, C. falcatum, C. Fecha de recepción: 01 de octubre, 2009

furca, C. fusus, C. gibberum var. dispar, C. gravidum, C. horridum, C. humile, C. macroceros, C. macroceros var. gallicum, C. massiliense, C. platycorne, C. ranipes, C. trichoceros, C. tripos var. atlanticum, C. tripos var. pulchellum, C. symetricum var. coarctatum. From these, C. dens was recorded for the first time inside Bahía de La Paz and the Gulf of California. Identification of this species was made following its original description (Ostenfeld & Schmidt, 1901). Ceratium dens Ostenfeld & Schmidt, 1901 Basionym: Ostenfeld & Schmidt, 1901 (p. 165, fig. 16). Sinonym: C. dens var. reflexa Schmidt, 1901 (p. 214, fig. 2). Records: Jörgensen (1911, p. 31, fig. 58); Wood (1954, p. 280, fig. 204), Sournia (1967, p. 457, fig. 80). Sampling station: In front of Petróleos Mexicanos dock, Bahía de La Paz (Figs. 1-11 and 15). Sample analysis: Quantitative analysis of bottle samples yielded 2000 cells L-1 of C. dens during September and it was not found in bottle samples during October and November. Collected samples with both nets were exhaustively analyzed and 62 specimens of C. dens were found during September surveys, 40 specimens during October and 34 during November. This species appeared in solitary not in chains, coinciding with observations in Japan (Fukuyo, 2000), where solitary cells were also observed (Fig. 13). Two-cells chains were observed in Philippines (Borja, 2002; Fig. 14) and chains with up to 15 cells were recorded in the Mozambique Channel (Sournia, 1967). Specimens of C. dens forming chains of three to eight cells (Figs. 16-17; this study) were observed in Fort Lauderdale, Florida, USA (26° 05.01’ N and 80° 02.86’ W) during February 2007. Dimensions: Specimens showed a total length of 140 to 394 mm and 85 to 110 mm of transdiameter (n=55). Specimens from Fort Fecha de aceptación: 11 de noviembre, 2009

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Lauderdale, Florida, showed a total length of 264 to 494 mm (n=11) and 100 to 110 mm of transdiameter (n=4). Characteristics: A large and robust form with a more pronounced width than height of the cell body. Thecae structure is marked, showing curved and strong lines, with evident pores. The apical horn is strong, winged and cilindrical; wider at the base and usually longer than the left antapical horn. In some specimens (Figs. 3, 6 and 9) the antapical horn is longer than usual and slightly bent to its right. The left antapical horn is notably short, straight or slightly curved, with a short sharp closed tip, either straight or slightly curved. The right antapical horn is longer than the left one and continues from the base with an inclination forward diverging from the apical horn, and sometimes it is thinner than the other horns. The curvature of the right antapical horn is variable (Figs. 1-11). This varability in the horn direction was also observed by Ostenfeld and Schmidt (1901, p. 165, fig. 16), who illustrated two especimens of C. dens, one with the left antapical horn pointing backwards (left drawing) and another with the left antapical horn pointing to the left or laterally (right drawing). This variation led Schmidt (1901: p. 214, Fig. 2) to describe a new variety, C. dens var. reflexa, which differs from the type variety only in the left antapical horn direction, which is bent backward. Nevertheless, the validity of C. dens var. reflexa became doubtfull (Böhm, 1931) due to the variation that this species shows in the direction and size of the horns (Figs. 1-11). In this study, besides the forms described by Ostenfeld and Schmidt (1901), another form was found showing a less robust body, a longer (» 380 mm) and slightly curved to the right antapical horn and the left antapical horn curved upward (Figs. 3, 6 and 9). Another specimen showed an intermediate form, with robust body, left antapical horn curved upward and the right antapical horn with different inclination angles (Figs. 7 and 8). Most of the cells showed a straight horn; albeit, in some specimens it was pointed to the right (Fig. 7). Distribution in the Mexican Pacific: This finding represents the first record of Ceratium dens for the Mexican Pacific. The name C. dens was wrongfully used by different authors

(Licea-Durán, 1995; Meave del Castillo & Hernández-Becerril, 1998; Cortés-Altamirano & Núñez-Pasten, 2000) to designate Ceratium balechii, a species that was stablished by Meave del Castillo et al. (2003). The confusion was caused by the similarity of C. balechii with other species (Meave del Castillo et al., 2003). The wide distribution that this species shows and the quantity of examined samples, allowed Meave del Castillo et al. (2003) discard the occurrence of C. dens in the Mexican Pacific. The dinoflagellate species list published by Okolodkov and Gárate-Lizárraga (2006), which included the analysis of more than 600 phytoplankton samples, shows no presence of C. dens along the Mexican Pacific. Despite this, this study shows for the first time the presence of C. dens in the southwest portion of the Gulf of California. General Distribution: Ceratium dens was first described for the Red Sea and the Gulf of Aden within the Indian Ocean (Ostenfeld & Schmidt, 1901). Karsten (1907) also reported it for the Indian Ocean. Bohm (1931) recorded it for the Malacca (Malaysia) coast. Steemann-Nielsen (1934) found it in samples collected inside the Torres Strait, located between Australia and Papua, New Guinea, all records for the Western Pacific. In another study for the Indian Ocean and East Asia, C. dens was recorded in the Mozambique Channel, in a coastal station in South Africa, in the Gulf of Thailand, in the South China Sea, Malaysia, the Sulu Sea and in the Celebes Sea (Steemann-Nielsen, 1939). Pavillard (1935) observed it close to the Marquesas Islands, located in the East Central Pacific. In a study on Indian Ocean dinoflagellates, Taylor (1976) also considered this species as rare, but, he pointed out that it was present in the coastal station of the east portion of Bengal Bay and Andaman Sea and in three stations of the Arabic Sea. From the work of Taylor (1976) there are other records for the Indian Ocean (Subrahmanyan, 1968; Angot, 1970; Krishnamurthy et al., 1980; Dowidar, 1983, Eashwar et al., 2001) and a few reports for the Japan coasts (Fukuyo, 2000) and the Philippines (Borja, 2002). Steidinger and Williams (1970: p. 152, pl. XV, fig. 40) pointed out that Ceratium sp. resembled C. dens but that it could be a developmental sta-

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Figures 1-11. Different Ceratium dens specimens collected in BahĂa de La Paz during the autumm 2009; 1, 7, 9: Ceratium dens lateral view; 2, 3, 4, 5, 6, 8, 10, 11 Ceratium dens dorsal view; 12 Arrow shows a Blastodinium sp. parasiting Paracalanus sp. Photographs from Figs. 1-9 and 11 were live specimens. Figs. 1-7 and 10 were collected in September 22, 2009. Figs. 8 and 9 specimens were collected in October 20, 2009 and Fig. 11 specimen was collected in November 3, 2009.

ge of another species. Figures 16 and 17 in this study could be the first record for C. dens in the Atlantic Ocean. Taylor (1987) considered C. dens as a true case of endemism (spe-

cies present exclusively in one region), because it has been observed from the north of the Indian Ocean to the southeast of Asiatic waters. This fact is presented in Figure 18, which

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Figures.13-17. Different specimens of Ceratium dens from around the world: 13) Japan (Taken from Fukuyo, 2000); 14) Philippines (Taken from Borja, 2002); 15) Gulf of California (this study); 16-17) Fort Lauderdale, Florida, USA. Figs. 13-16 ventral view and Fig. 17 dorsal view. Bar scale 100 µm.

shows the worldwide distribution of C. dens. Its presence in East Pacific could indicate that it is an invasive species, but new surveys are needed to corroborate this hypothesis. Steemann-Nielsen (1934) and Wood (1954) considered C. dens a rare species, characteristic of warm waters and an indicator of sea currents. In the sampling station of this study the sea surface temperature was 29.5 °C (September), 29 °C (October) and 27 °C (November). It is possible that C. dens is an indicator species for warm waters such as the Costa Rica Current, also known as Western Mexican Current, which is present during this season (Badan-Dangón, 1989). Nevertheless, this can not be assured since C. dens has not been present in many studies on the diversity of the genus Ceratium carried out from the Baja California Peninsula to Perú (Hernán-

dez-Becerril, 1988; Gárate-Lizárraga et al., 1990; Gárate-Lizárraga & Verdugo-Díaz, 2001; Vargas-Montero & Freer, 2004; Okolodkov & Gárate-Lizárraga, 2006; Sánchez et al., 2007). The first record of C. dens in the Eastern Pacific was in the Marquesas Islands (Pavillard,1935) during the El Niño 1932-1933. It is possible that the presence of C. dens in the mouth of the Gulf of California during September-November 2009 could be also related to the El Niño event (2009-2010) (http://cpc.noaa.gov/products/analysis_monitoring/enso-update/). On the other hand, the occurrence of the dinoflagellate Blastodinium sp., a parasite of the copepod Paracalanus sp. (Fig. 12), Schuettiella mitra and Centrodinium pulchrum whose distribution is mainly tropical, confirms the presence of tropical waters in the south portion of the Gulf of California during

FIRST RECORD OF Ceratium dens

Figure 18. Worldwide distribution of the dinoflagellate Ceratium dens (n): Sources: Ostenfeld & Schmidt (1901), Karsten (1907), Jörgensen (1920), Steemann-Nielsen (1934; 1939), Pavillard (1935), Wood (1954), Subrahmanyan (1968), Sournia (1967), Argot (1970), Taylor (1976), Krishnamurthy et al. (1980), Dowidar (1983), Eashwar et al. (2001), Borja (2002), this study.

the study period. The exhaustive review of specialized literature on the distribution of the genus Ceratium suggests that this finding is the first record of C. dens in the coastal portion of the Eastern Pacific. ACKNOWLEDGEMENTS Thanks to the Instituto Politécnico Nacional for the financial support for this work through the projects SIP-20090299, SIP-20090303. To Wayne Coats, Tsvetan Bachvaroff and Sara Handy (Smithsonian Environmental Research Center, Edgewater, MD, USA) for measurements and photographs 16 and 17 of C. dens specimens, which have not been published. To Patricia Ceballos and René Torres-Villegas (CICIMAR-IPN) for the microscopy equipment. To Yuri Okolodkov (ICIMAP, Universidad Veracruzana), Malte Elbrächter (Deutsches Zentrum für Marine Biodiversitätsforschung, Forschunginstitut Senckenberg, Germany) and Clara Ramírez-Jáuregui (ICMyL-UNAM, Mazatlán) for the specialized literature. Also for the editorial review of the manuscript by two anonymous re-

fferees. The author is recipient of COFAA and EDI grants. REFERENCES Angot, M. 1970. Le phytoplancton des environs de Nossi-Bé (Madagascar) et ses variations au cours de 1965. Am. Univ. Madagascar, 7: 165-178. Badan-Dangon, A. 1998. Coastal circulation from the Galápagos to the Gulf of California, 315–344. In: A.R. Robinson, Brink, & K.H. (Eds.), The Sea, vol. 11. J. Wiley and Sons, New York. Böhm, A. von. 1931. Distribution and variability of Ceratium in the Northern and Western Pacific. Bernice P. Bishop Mus. Bull. 87: 1–46, pl. 1. Borja, M.V. 2002. Classification of marine dinoflagellates in the Philippines, 131–167. In: Gonzales, C., S. Sakamoto, E. Furio, T. Ogata, K. Kodama & Y. Fukuyo (Eds.). Practical guide on paralytic shellfish poi-

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