versão impressa ISSN 0188-8897
Hidrobiológica v.18 n.1 supl.1 México ago. 2008
Influence of phytoplankton diets on the ingestion rate and egg production of Acartia clausi and A. lilljeborgii (Copepoda: Calanoida) from Bahía de La Paz, Gulf of California
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 BandSchmidt1*, Rocío PachecoChávez1 and Sergio HernándezTrujillo1
1 Departamento de Plancton y Ecología Marina. Centro Interdisciplinario de Ciencias Marinas (CICIMARIPN), Apdo. Postal 592, La Paz, B.C.S. 23000, México. * Correo electrónico: email@example.com.
Recibido: 8 de noviembre de 2006
Aceptado: 1 de octubre de 2007
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.
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.
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 (PalomaresGarcía 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. lilljeborgii have been estimated on a seasonal basis in Bahía de La Paz, however the factors influencing variations in production rates have not been defined (PalomaresGarcía et al., 2003; PachecoChávez et al., 2005). During winter, average daily egg production rates for A. clausi and A. lilljeborgii were 12 ± 4 eggs female1 day1 and 23 ± 6 eggs female1 day1, respectively, and increased with high nutrient and chlorophyll a (Chl a) concentrations in a wellmixed water column (PalomaresGarcía et al., 2003). PachecoChávez et al. (2005) found in autumn an egg production for A. lilljeborgii and A. clausi of 16.8 ± 7.8 eggs female1 day1 and 8.7 ± 4.9 eggs female1 day1, 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 20µm phytoplankton net. The cell concentrate was sieved through a 60um mesh screen to eliminate larger organisms. The concentrate was placed in a 250ml culture container filled with filtered seawater. In the laboratory, phytoplankton vegetative cells were isolated with micropipettes under an inverted microscope. Single cells and chains were transferred to 96well plates with modified f/2 medium according to Anderson et al. (1984) and maintained at 24 ± 1°C with 150 umol photons m2 s1 overhead illumination supplied with coolwhite 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 cm2 for 20 minutes. Cultures from wells were transferred to 50mL 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 1L 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 L1. Only Gyrodinium sp. was used with an initial concentration of 400 ug C L1.
Copepods were collected superficially with a 333um 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 1L plastic flasks with 500ml 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, 2ml subsamples of phytoplankton were fixed in Lugol's iodine solution (Throndsen, 1978). Large cells were counted on 1ml SedgwickRafter 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 ml1), Ci = initial cell concentration (cells ml1), Cf = final cell concentration (cells ml1), 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 200um mesh screen; eggs and nauplii were collected in a 50um mesh screen. Surviving females, eggs, and nauplii were counted.
The percentage data were arcsinetransformed, whereas values for ingestion rates and egg production were logtransformed 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.).
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. lilljeborgiihad significantly superior production rates when fed with Scrippsiella sp. (38.8 ± 5.5 eggs female1 day1), 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 female1 day1) 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 female1 day1), particularly with P. rhathymum (47.1 eggs female1 day1). With A. clausi, Chattonella sp. favored a greater egg production (25.0 ± 1.2 eggs female1 day1) than with A. lilljeborgii. When fed diatoms, A. clausi had a moderate egg production (≤11.5 eggs female1 day1), 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 copepod1 hr1) 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 hr1) 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 copepod1 hr1, with the exception of the Chaetoceros sp. diet.
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 tropicalsubtropical 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 & KleinBreteler, 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 & KleinBreteler (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 dinoflagellate 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 speciesspecific 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 (PalomaresGarcía 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 ml1), 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 (HyungKu & 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 female1 day1 in Bahía de La Paz for A. clausi (PalomaresGarcía et al., 2003). For A. lilljeborgii, the rates were from 6.1 to 15.3 eggs female1 day1 (GómezGutiérrez & Peterson, 1999; PalomaresGarcía et al., 2003).
Ingestion rates varied significantly with diet, varying from 19 to 917 ng C copepod1 hr1, 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 sizelimits 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.
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.
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