Influencia de dietas de fitoplancton en la tasa de ingesta y producción de huevos de Acartia clausi y A. lilljeborgii (Copepoda: Calanoida) de la Bahía de La Paz, Golfo de California
Christine Johanna Band–Schmidt1*, Rocío Pacheco–Chávez1 and Sergio Hernández–Trujillo1
1 Departamento de Plancton y Ecología Marina. Centro Interdisciplinario de Ciencias Marinas (CICIMAR–IPN), Apdo. Postal 592, La Paz, B.C.S. 23000, México. * Correo electrónico: cbands@ipn.mx.
Recibido: 8 de noviembre de 2006
Aceptado: 1 de octubre de 2007
ABSTRACT
Different phytoplankton diets were tested on Acartia clausi and A. lilljeborgii from Bahía de La Paz to determine their effect on survival, egg production, and ingestion rate. Female copepods were fed diatom strains (Chaetoceros sp., Cylindrotheca closterium, Odontella longicruris, and Dytilum brightwelli), dinoflagellate strains (Scrippsiella sp., Gyrodinium sp., Prorocentrum micans, and P. rhathymum), and one Raphidophyceae (Chattonella sp.). After 24 h of incubation in darkness at 24 °C, survival with various phytoplankton diets was above 91%. Gyrodinium sp. produced the lowest survival in both copepod species (44.5% in A. clausi and 89.6% in A. lilljeborgii). Dinoflagellate diets provided the highest egg production. A. clausi had higher egg production when fed with P. rhathymum, P. micans, Gyrodinium sp., Scrippsiella sp., and Chattonella sp. A. lilljeborgii had a higher egg production with Scrippsiella sp., P. micans, Gyrodinium sp., and Chaetoceros sp. Ingestion rates were higher in both Acartia species with two diatom diets (O. longicruris and Chaetoceros sp.), P. rhathymum and Chattonella sp. These results suggest that both Acartia species respond to nutritional quality of phytoplankton in a short time. Higher ingestion rates did not necessarily result in higher egg production, suggesting that the link between ingestion and egg production may be in what is eaten, rather than in how much. The response in egg production seems to be species specific, but in general was higher with dinoflagellate diets, suggesting a higher food quality compared with diatoms (excepting Chaetoceros sp.).
Key words: Acartia clausi, Acartia lilljeborgii, Bahía de La Paz, egg production, grazing rate.
RESUMEN
Se probaron diversas dietas de fitoplancton en Acartia clausi y A. lilljeborgii de la Bahía de La Paz, para determinar su efecto en la supervivencia, producción de huevos y tasa de ingesta. Se alimentaron hembras de copépodos con cepas de diatomeas (Chaetoceros sp., Cylindrotheca closterium, Odontella longicruris y Dytilum brightwelli), de dinoflagelados (Scrippsiella sp., Gyrodinium sp., Prorocentrum micans y P. rhathymum) y una rafidofita (Chattonella sp.). Después de 24 h de incubación en oscuridad a 24 °C, la supervivencia con las diversas dietas fue mayor a 91%. Sólo al alimentar a A. clausi con Gyrodinium sp. la supervivencia fue baja (44.5%). Con las dietas de dinoflagelados se obtuvo la mayor producción de huevos. A. clausi presentó una mayor producción de huevos al alimentarse con P. rhathymum, P. micans, Gyrodinium sp., Scrippsiella sp. y Chattonella sp. A. lilljeborgii presentó una mayor producción de huevos con Scrippsiella sp., P. micans, Gyrodinium sp. y Chaetoceros sp. La tasa de ingesta en ambas especies de Acartia fue mayor con dos dietas de diatomeas (O. longicruris y Chaetoceros sp.), P. rhathymum y Chattonella sp. Estos resultados sugieren que ambas especies de Acartia responden en un lapso corto de tiempo a la calidad nutricional del fitoplancton. Las mayores tasas de ingesta no necesariamente resultaron en una mayor producción de huevos, sugiriendo que la relación entre la tasa de ingesta y la producción de huevos pudiera estar relacionada con la calidad alimenticia, más que con la cantidad ingerida. La respuesta en la producción de huevos en ambos copépodos parece ser específica para cada especie, sin embargo en general, las dietas de dinoflagelados parecen tener una mayor calidad nutricional comparadas con las diatomeas con la excepción de Chaetoceros sp.
Palabras clave: Acartia clausi, Acartia lilljeborgii, Bahía de La Paz, producción de huevos, tasa de ingesta.
INTRODUCTION
]]> Copepods are the dominant mesozooplankton in marine environments, representing up to 80% of its total biomass (Kiørboe, 1998). In Bahía de La Paz, few dominant species have been reported. Acartia clausi (Giesbrecht, 1892) and A. lilljeborgii (Giesbrecht, 1889) are the most abundant species throughout the year and are important contributors to secondary production of the bay (Palomares–García et al., 2003).Several studies have demonstrated that egg production rate in copepods can be used to estimate feeding conditions (Dagg, 1977; Saiz et al., 1993), but few studies have been done in subtropical zones to support this hypothesis. Egg production is regulated by several environmental factors, such as temperature (Koski & Kuosa, 1999), salinity (Pagano et al., 2004), female size (Koski & Kuosa, 1999), diurnal rhythms (Pagano et al., 2004), food abundance (Kleppel, 1993; Pagano et al., 2004), food type (Murray & Marcus, 2002; Ceballos & Ianora, 2003), and food quality (Kleppel & Burkart, 1995).
In situ daily egg production rates of A. clausiand A. lilljebor–gii have been estimated on a seasonal basis in Bahía de La Paz, however the factors influencing variations in production rates have not been defined (Palomares–García et al., 2003; Pacheco–Chávez et al., 2005). During winter, average daily egg production rates for A. clausi and A. lilljeborgii were 12 ± 4 eggs female–1 day–1 and 23 ± 6 eggs female–1 day–1, respectively, and increased with high nutrient and chlorophyll a (Chl a) concentrations in a well–mixed water column (Palomares–García et al., 2003). Pacheco–Chávez et al. (2005) found in autumn an egg production for A. lilljeborgii and A. clausi of 16.8 ± 7.8 eggs female–1 day–1 and 8.7 ± 4.9 eggs female–1 day–1, respectively. Daily egg production increased with Chl a concentration during autumn, but no correlation was found in spring and winter. These results suggest that seasonal changes in phytoplankton species composition could be influencing egg production.
The determination of grazing rates and egg production of copepods with different phytoplankton species can lead to 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. The goal of this study was to determine the effect of different phytoplankton diets (dinoflagellates, diatoms, and one raphidophyte) on survival, ingestion rate, and egg production, in Acartia clausi and A. lilljeborgii from Bahía de La Paz under laboratory conditions.
MATERIALS AND METHODS
Clonal cultures of several algae (Odontella longicruris (Greville) Hoban, Chaetoceros sp., Cylindrotheca closterium (Ehrenberg) W. Smith, Ditylum brightwellii(West) Grunow in Van Heurck, Prorocentrum rhathymum Loeblich, Shirley et Schmidt, P. micans Ehrenberg, and Chattonella sp. were obtained from Bahía de La Paz on the western side of the Gulf of California. Scrippsiella sp. and Gyrodinium sp. were collected in Bahía de Topolobampo on the eastern side of the Gulf of California. Vegetative cells were collected by vertical tows with a 20–µm phytoplankton net. The cell concentrate was sieved through a 60–um mesh screen to eliminate larger organisms. The concentrate was 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 according to Anderson et al. (1984) and maintained at 24 ± 1°C with 150 umol photons m–2 s–1 overhead illumination supplied with cool–white fluorescent lights.
Culture media were prepared with seawater obtained from Ensenada de La Paz, a lagoon at the southern end of Bahía de La Paz (~35 psu). Seawater used for the preparation of culture media was filtered through GF/F filters with 0.7 µm pore size and sterilized in an autoclave at 121°C at 1.1 kg cm–2 for 20 minutes. Cultures from wells were transferred to 50–mL culture tubes for maintaining the strains.
Dinoflagellate and Raphidophyte strains were grown in modified f/2 medium (Anderson et al., 1984) and silica was added for diatom strains. Batch cultures were grown in 1–L polycarbonate vials and maintained under conditions described above. All strains were offered as diets during exponential growth phase.
Carbon content was estimated from cell volume, based on length and width measurements of 30 cells from each strain according to Strathmann (1967). Cell volume and carbon content of phytoplankton diets are presented in Table 1. Cell volume varied from 31 to 60,421 µm3. Initial carbon concentration varied between 800 and 1,000 ug C L–1. Only Gyrodinium sp. was used with an initial concentration of 400 ug C L–1.
]]> Copepods were collected superficially with a 333–um plankton mesh net from Bahía de La Paz. Plankton samples were transferred to the laboratory in iceboxes filled with seawater. In the laboratory, adult females of Acartia clausi and A. lilljeborgii were separated under a stereoscopic microscope and acclimated for two hours in filtered seawater, at 24 °C and 35 psu.For the different phytoplankton diets that were tested, 30 adult females were transferred to 1–L plastic flasks with 500–ml filtered seawater through GF/F filters and incubated in darkness at 24 °C at 35 psu for 24 h. There were three replicates of each treatment within each trial. To determine the phytoplankton growth rate, two flasks without copepods were incubated under the conditions previously described. At the beginning and end of each trial, 2–ml sub–samples of phytoplankton were fixed in Lugol's iodine solution (Throndsen, 1978). Large cells were counted on 1–ml Sedgwick–Rafter counting slides; a Neubauer counting slide was used for smaller cells. At least 400 cells were counted for each sample. Cell density was used to calculate exponential growth rates according to Guillard (1973), and female ingestion rates according to the equation of Frost (1972):
l = ((V x g) / N ) x C
g = (lnCi – lnCf)/(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 (hours), and k = phytoplankton growth rate/hour. Additionally, copepods in filtered seawater without phytoplankton were incubated by triplicate; these represented the initial reproductive conditions of females and were used as control values for each experiment.
After incubation for 24 h, adult females in each bottle were gently separated through a 200–um mesh screen; eggs and nau–plii were collected in a 50–um mesh screen. Surviving females, eggs, and nauplii were counted.
The percentage data were arcsine–transformed, whereas values for ingestion rates and egg production were log–transformed prior to statistical analyses. An ANOVA test was applied (p < 0.05), followed by Tukey's post hoc analyses. All statistical analyses used the STATISTICATM v.6 (StatSoft, Inc.).
RESULTS
After incubation for 24 h, survival of adult females of Acartia lilljeborgii and A. clausi, fed with different phytoplankton diets was above 91.3% (Table 1). When A. clausi and A. lilljeborgii were fed Gyrodinium sp. survival was significantly lower (44.5% and 89.6% respectively). Due to the elevated mortality obtained with this diet, higher cell concentrations of Gyrodinium sp. could not be used. Average survival of adult females of A. lilljeborgii with the other diets was higher (95.7%) than for A. clausi (90%).
]]> Different responses in egg production in A. clausi and A. lilljeborgii were observed with the same diet (Fig. 1). In general, the highest production was obtained with dinoflagellates. A. lill–jeborgiihad significantly superior production rates when fed with Scrippsiella sp. (38.8 ± 5.5 eggs female–1 day–1), Prorocentrum micans (34.6 ± 2.0), and Gyrodinium sp. (23.3 ± 10.5) compared to P. rhathymum and Chattonella sp. Of the diatoms diets, Chaetoceros sp. (25.1 ± 5.8 eggs female–1 day–1) produced a significantly higher production rate than the other diatom diets. With the Raphidophyceae, Chattonella sp., a mild production occurred (<5.7 eggs). A. clausi also had significantly higher egg production with dinoflagellates (20.5 to 47.1 eggs female–1 day–1), particularly with P. rhathymum (47.1 eggs female–1 day–1). With A. clausi, Chattonella sp. favored a greater egg production (25.0 ± 1.2 eggs female–1 day–1) than with A. lilljeborgii. When fed diatoms, A. clau–si had a moderate egg production (≤11.5 eggs female–1 day–1), only when fed Chaetoceros sp. a significantly higher egg production than other diatoms diets was observed.Ingestion rates were significantly higher in both copepods when fed Chaetoceros sp., Odontella longicruris, Prorocentrum rhathymum, and Chattonella sp. (Fig. 2). In both copepods, the lowest ingestion rates (below 300 ng C copepod–1 hr–1) occurred with Cylindrotheca closterium, Dytilum brightwelli, Scrippsiella sp., and Gyrodinium sp. Ingestion rates were different with a Prorocentrum micans diet; A. lilljeborgii had a superior average ingestion rate than A. clausi.
Both Acartia species had greater ingestion rates (above 700 ng C copepod hr–1) with particle sizes from 9 to 40 x 103 µm3 (Fig. 3). When particle sizes were larger or smaller, ingestion rates were below 300 ng C copepod–1 hr–1, with the exception of the Chaetoceros sp. diet.
DISCUSSION
This is the first study in the Subtropical Pacific where several regional phytoplankton strains were used to determine the survival, ingestion rate, and egg production in two of the most abundant Acartia species in the region: A. clausi and A. lilljeborgii. Worldwide, several studies on egg production have been performed in A. clausi, however scarce information exists on A. lilljeborgii, a species with a more tropical–subtropical distribution. Our results clearly show the heterogeneous effects of phytoplankton diets on both copepods specifically on survival, egg production, ingestion rate, and cell size vs. ingestion rates in darkness at 24 °C.
No significant differences were observed in the survival of A. lilljeborgiiand A. clausi with the different phytoplankton diets, with the exception of Gyrodinium sp. which produced a high mortality. In general, there was a high survival (>91.3%) in the different experiments and in filtered seawater (data not shown). High survival of copepods in filtered seawater also occurred in Temora longicornis O. F. Müller and Pseudocalanus elongatus (Boeck, 1865) (Koski & Klein–Breteler, 2003). In general, the lower average survival of A. clausi (90%) compared with A. lilljeborgii (95.7%) with different diets suggests that A. clausi is more sensitive to secondary metabolites of phytoplankton or to incubation conditions. Koski & Klein–Breteler (2003) believe that low or high survival in copepods is species specific. High mortality when fed Gyrodinium sp. suggests rejection, possibly due to the presence of toxic substances. The possible toxicity of our Gyrodinium strain requires further research.
In general, the highest egg production occurred with dino–flagellate diets (Scrippsiella sp., Gyrodinium sp., Prorocentrum micans, P. rhathymum), and with one diatom (Chaetoceros sp.). Egg production was dependent on food type and with some diets species–specific responses were observed, Chattonella sp. and P. rhathymum induced high egg production only in A. clausi; Chaetoceros sp. and Scrippsiella sp. induced a higher egg production in A. lilljeborgii. The response of egg production to diet in A. clausi and A. lilljeborgii occurred in a short time, confirming observations of Tester & Turner (1990). Greater egg production with dinoflagellate diets suggests that these species could have a higher food quality if they were non toxin producers or if copepods were insensitive to toxic metabolites. A. clausi is capable of ingesting the toxic dinoflagellate Gymnodinium catenatum Graham with no apparent adverse effects in the ingestion and egg production rates (Palomares–García et al., 2006). A. clausi also ingested more toxic cells of Alexandrium minutum Halim as its concentration increased; with this diet hatching success and nauplii production decreased (Frangópulos et al., 2000).
]]> Egg production rates were significantly reduced with diatom diets, with the exception of Chaetoceros sp. Based on egg production rates, Ditylum brightwelli, Cylindrotheca closterium, and Odontella longicruris were clearly inadequate for both copepod species. Several laboratory studies showed that diatoms, at high concentrations (≥103 cells ml–1), are deleterious to copepod reproduction (Ban et al., 1997). Ingestion of diatoms by adult female copepods can be followed by low egg production and low hatching success, including abnormal egg and nauplii development (Hyung–Ku & Poulet, 2000; Lee et al., 1999). Other studies demonstrated that some diatoms species produce toxic unsaturated aldehydes that block embryogenesis (Ceballos & Ianora, 2003) or deform nauplii (Ianora et al., 2004).Studies of the effect of Raphidophyte species on copepod production are scarce. Many marine Chattonella species are ichthyotoxin producers, related to reactive oxygen species (Oda et al., 1994), brevetoxins (Onoue & Nozawa, 1989), and polyunsaturated fatty acids (Skeen et al., 2002). The response of Acartia omorii, A. tonsa, and A. hudsonica to different toxic Raphidophyte species varies from not eating, rejection of food, and reduced fecundity (Uye & Takamatsu, 1990). A. lilljeborgii and A. clausi did not reject the diet of Chattonella sp. and a reduction in egg production was only observed in A. lilljeborgii. Production of toxic metabolites needs to be confirmed in this species.
In general, A. clausi and A. lilljeborgi seem to be very efficient in transforming ingested material into egg production, this has also been observed in A. tonsa, which rapidly adapts energetically to changing food conditions and seems well adapted to the fluctuating but occasionally high food concentrations characteristic of coastal waters (Kiørboe et al., 1998). This could also be the case for A. clausi and A. lilljeborgii which have a coastal distribution (Mauchline, 1998).
In general, average egg production was higher than production obtained under field conditions in Bahía de La Paz for both Acartia species, probably caused by the amount of cells ingested. Highest average egg production was 11.9 eggs female–1 day–1 in Bahía de La Paz for A. clausi (Palomares–García et al., 2003). For A. lilljeborgii, the rates were from 6.1 to 15.3 eggs female–1 day–1 (Gómez–Gutiérrez & Peterson, 1999; Palomares–García et al., 2003).
Ingestion rates varied significantly with diet, varying from 19 to 917 ng C copepod–1 hr–1, and seem to be related to cell size. Both Acartia species had higher ingestion rates with Odontella longicruris, Chaetoceros sp., Prorocentrum rhathymum, and Chattonella sp. Cell volume could have influenced higher ingestion rates (ranging from 9,000 to 40,000 µm3), with the exception of Chaetoceros sp., however this species forms long chains and, in culture forms dense aggregations that probably facilitated ingestion. It is possible that small cells (<500 µm3) and large cells (>60,000 µm3) are difficult to capture and/or manipulate (Frost, 1977; Hansen et al., 1994). The similar size–limits for ingestion of particles could indicate that both Acartia species share the same trophic level.
Clearly, ingestion and egg production rates in Acartia clausi and A. lilljeborgii are dependent on food type. Higher ingestion rates not necessarily resulted in higher reproductive rates. These results suggest that, under natural conditions, egg production of A. clausi and A. lilljeborgii probably could increase when higher abundances of dinoflagellates are found in the bay.
ACKNOWLEDGEMENTS
The authors wish to thank J. Cruz and M. Cerro for technical assistance. This project was financed by Instituto Politécnico Nacional (CGPI grants 20040722, 20040626, 20050133, and 20050143) and CONACYT research projects 52724. Authors CJBS and SHT have EDI and COFAA fellowship.
]]> 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. Journal of Phycology 20: 418–425. [ Links ]
Ban, S., C. Burns, J. Castel, Y. Chaudron, E. Christou, R. Escribano, S. Fonda–Umani, S. Gasparini, F. Guerrero–Ruiz, M. Hoffmeyer, A. Ianora, H. K. Kang, M. Laabir, A. Lacoste, 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. Marine Ecology Progress Series 157: 287–293. [ Links ]
Ceballos, S. & A. Ianora. 2003. Different diatoms induce contrasting effects on the reproductive success of the copepod Temora stylifera. Journal of Experimental Marine Biology and Ecology 294: 189–202. [ Links ]
Dagg, M. 1977. Some effects of patchy food environments on copepods. Limnology and Oceanography 22: 99–107. [ Links ]
Frangópulos, M. C., C. Guisande, I. Maneiro, I. Rivero & J. Franco. 2000. Short– and long–term effects of the toxic dinoflagellate Alexandrium minutum on the copepod Acartia clausi. Marine Ecology Progress Series 203:161–169. [ Links ]
Frost, B. W. 1972. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnology and Oceanography 17: 805–815. [ Links ]
Frost, B. W. 1977. Feeding behavior in Calanus pacificus in mixtures of food. Limnology and Oceanography 22: 472–491. [ Links ]
Gómez–Gutiérrez, J. & W. T. Peterson. 1999. Egg production rates of eight calanoid copepod species during the summer 1997 at Newport Oregon, U.S.A. Journal of Plankton Research 21: 637–657. [ Links ]
Guillard, R. R. L. 1973. Division rates. In: Stein, J. R. (Ed.). Handbook of Phycological Methods, Cambridge University Press, Londres, pp. 289–312. [ Links ]
Hansen, B., P. Verity, T. Falkenhaug, K.S. Tande & F. Norrbin. 1994. On the trophic fate of Phaeocystis pouchetti (Harriot). V. Trophic relationships between Phaeocystis and zooplankton: an assessment of methods and size dependence. Journal of Plankton Research 16: 487–511. [ Links ]
Hyung–Ku, K. & S. A. poulet. 2000. Reproductive success in Calanus helgolandicus as a function of diet and egg cannibalism. Marine Ecology Progress Series 201: 241 –250. [ Links ]
Ianora, A., A. Miralto, S. A. Poulet, Y. Carotenuto, I. Buttino, G. Romano, R. Casotti, G. Pohnert, T. Wichard, L., Colucci–D'amato, G. Terrazzano & V. Smetacek. 2004. Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429: 403–407. [ Links ]
Kiørboe, T. 1998. Population regulation and role of mesozooplankton in shaping marine pelagic food webs. Hydrobiologia 363: 13–27. [ Links ]
Kleppel, G. S. 1993. On the diets of calanoid copepods. Marine Ecology Progress Series 99: 183–195. [ Links ]
Kleppel, G. S. & C. A. Burkart. 1995. Egg production and the nutritional environment of Acartia tonsa: the role of food quality in copepod nutrition. ICES Journal of Marine Science 52: 297–304. [ Links ]
Koski, M. & W. C. M. Klein–Bretler. 2003. Influence of diet in copepod survival in the laboratory. Marine Ecology Progress Series 264: 73–82. [ Links ]
Koski, M. & H. Kuosa. 1999. The effect of temperature, food concentration and female size on the egg production of the planktonic copepod Acartia bifilosa. Journal of Plankton Research 21: 1779–1789. [ Links ]
Lee, H. W., S. Ban, Y. Ando, T. Ota & T. Ikeda. 1999. Deleterious effect of diatom diets on egg production and hatching success in marine copepod Pseudocalanus newmani. Plankton Biology and Ecology 46: 104–112. [ Links ]
Mauchline, J. 1998. The Biology of Calanoid Copepods. In: Blaxter, J. H. S., A. J. Southward & P. A. Tyler (Eds.). Advances in Marine Biology. Volume 33. Academic Press, San Diego. 710 p. [ Links ]
Murray, M. M. & N. H. Marcus. 2002. Survival and diapause egg production of the copepod Centropages hamatus raised on dinoflagellate diets. Journal of Experimental Marine Biology and Ecology 270: 39–56. [ Links ]
Oda, T., A. Ishimatsu, S. Takeshita & T. Muramatsu. 1994. Hydrogen peroxide production by the red tide flagellate Chattonella marina. Bioscience Biotechnology and Biochemistry 58: 957–958. [ Links ]
Onoue, Y. & K. Nozawa. 1989. Separation of toxins from harmful red–tides occuring along the coasts of Kagoshima Prefecture. In: Okaichi, T., D. M. Anderson & T. Nemoto (Eds.). Red Tides Biology, Environment Science, and Toxicology. Elsevier, New York, pp. 371–374. [ Links ]
Pacheco–Chavéz, R., A. Zárate–Villafranco, G. Esqueda–Escárcega, J. R. H. Alfonso, S. Hernández–Trujillo & G. Aceves–Medina. 2005. Comparison of daily egg production rates of Acartia clausi and Acartia lilljeborgiiduring autumn, winter and spring in Bahía de La Paz, Mexico. Abstracts. Plankton Symposium III, Figueria da Foz, Portugal. p. 67. [ Links ]
Pagano, M., E. Kouassi, R. Arfi, M. Bouvy & L. Saint–Jean. 2004. In situ spawning rate of the calanoid copepod Acartia clausi in a tropical lagoon (Ebrié, Côte d'Ivoire): diel variations and effects of environmental factors. Zoological Studies 43: 244–254. [ Links ]
Palomares–García, R., A. Martínez–López & R. De Silva–Dávila. 2003. Winter egg production rates of four calanoid copepod species in Bahía de La Paz, Mexico. In: Hendrick, M. E. (Ed.). Contributions to the Study of East Pacific Crustaceans. Instituto de Ciencias del Mar y Limnología. UNAM, México, pp. 139–152. [ Links ]
Palomares–García, R., J. Bustillos–Guzmán, C. J. Band–Schmidt, D. López–Cortés & B. Luckas. 2006. Effect of the toxic dinoflagellate Gymnodinium catenatum on the grazing, egg production, and hatching success of the copepod Acartia clausi. Ciencias Marinas 32: 111–119. [ Links ]
Saiz, E., P. Tiselius, P. R. Jonsson, P. Verity & G. Paffenhöffer. 1993. Experimental records of the effects of food patchiness and predation on egg predation of Acartia tonsa. Limnology and Oceanography 38: 280–289. [ Links ]
Skeen, A. R., C. R. Tomas & W. J. Cooper. 2002. The production of hydrogen peroxide by Heterosigma akashiwo under varying N:P ratios. In: Steidinger, K. A., Landsberg, J. H., Tomas, C. R. & G. A. Vargo (Eds.). 10th International Conference on Harmful Algae, St. Pete Beach, Florida, E.U.A., pp. 77–79. [ Links ]
Strathmann, R. R. 1967. Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnology and Oceanography12: 411–418. [ Links ]
Tester, P. A. & J. T. Turner. 1990. How long does it take copepods to make eggs? Journal of Experimental Marine Biology and Ecology 141: 169–182. [ Links ]
Throndsen, J. 1978. Preservation and Storage (Chapter 4). In: Sournia, A. (Ed.). Phytoplankton Manual. UNESCO, Paris, pp. 69–74. [ Links ]
Uye, S. & K. Takamatsu. 1990. Feeding interactions between planktonic copepods and red–tide flagellates from Japanese coastal waters. Marine Ecology Progress Series 59: 97–107. [ Links ] ]]>