Feeding, reproduction and toxin accumulation by the copepods Acartia bifilosa and Eurytemora affinis in the presence of the toxic cyanobacterium Nodularia spumigena

Abstract

Feeding, reproduction and accumulation of cyanobacterial toxins by the calanoid copepods Acartia bifilosa and Eurytemora affinis were studied during a cruise in the northern Baltic Sea. The experiments were carried out using both mixtures of natural plankton communities, mixtures containing the toxic Nodularia spumigena, and diets containing only the toxic cyanobacterium. Both copepod species had a high survival and fed actively on N. spumigena, both as a single food source and when offered in mixtures. Feeding on N. spumigena resulted in the detection of nodularin equivalents in the animals. However, there was a negative relationship between the gross growth efficiency and accumulated toxins, which indicates that the food quality was not ideal, possibly related to a high metabolic cost to cope with ingested toxins. Overall low egg production rates by both species and low egg hatching success by A. bifilosa in natural seawater suggested that the copepods were food-limited in the environment. The presence of Brachiomonas submarina offered in combination with N. spumigena enhanced A. bifilosa egg production, but not egg hatching success. Egg hatching success was not affected by increasing concentrations of N. spumigena in the diet. Instead, lack of food seemed to be a more important factor. Similar responses by E. affinis populations from sites with different history of toxin occurrence suggest that tolerance to cyanobacterial toxins has evolved in the Baltic Sea. This has possibly been guaranteed by genetic exchange between the 2 populations. These results suggest that N. spumigena is not directly harmful to copepods if an alternative food source is available, even though reproduction is not sustained if the species is offered as a single diet. Moreover, even if both copepods might act as a link transporting toxins to higher trophic levels, a very small fraction of the estimated ingested toxin was found in the animals, therefore the relative importance of this pathway seems limited.

Consequences of acclimation to Microcystis on the selective feeding behavior of the calanoid copepod Eudiaptomus gracilis

“…Summary results of the factorial ANOVA from the mixed food grazing experiments showing the effect of acclimation, Microcystis strain (MC), and the proportion of Microcystis in food (% Mic) on the copepod feeding selectivity coefficient for Chlamydomonas (a c ) across (a) all treatments including both strains of Microcystis, and the effect of acclimation and % Mic on the a c for (b) only MC+ treatments, or (c) only MC2 treatments. (evolutionary) time scales can cause genotypic differences in zooplankton tolerance to cyanobacteria (DeMott et al 1991;Kurmayer and Juttner 1999;Kozlowski-Suzuki et al 2003). Thus, depending on their evolutionary exposure to Microcystis, other E. gracilis genotypes could respond differently than observed here.…”

“…Better tolerance could be from adaptations in feeding behavior or physiological change resulting in reduced detoxification costs (DeMott et al 1991;Kozlowski-Suzuki et al 2003). In the relatively nonselective grazer Daphnia, the tolerance to toxic Microcystis increased during an individual's lifetime, probably due to the induction of a detoxification mechanism, which could also be transferred from mother to offspring (Gustafsson et al 2005).…”

“…Such increases in postexposure tolerance were observed in selective-feeding calanoid copepods that were able to co-exist with Microcystis (Ger et al 2010a,b). However, zooplankton grazing behavior is species-specific, so information from other species is necessary to describe the variability in adaptive responses of copepods to cyanobacteria (Kozlowski-Suzuki et al 2003). Some copepods are more tolerant to MC+ Microcystis than MC2 strains, presumably due to better avoidance of the MC+ strain (Ger et al 2010a,b).…”

Transfer of diazotrophic nitrogen to mesozooplankton in Kiel Fjord, Western Baltic Sea: a mesocosm study

“…This is believed to be associated with the generally poor food quality of cyanobacteria (Ahlgren et al 1992) and/or the production of the hepatotoxin nodularin by N. spumigena (Sellner 1997). The reasons for occasional observations of active mesozooplankton feeding on N. spumigena (Kozlowsky-Suzuki et al 2003) have been associated with aging, since aged filaments reduce toxin production (Carmichael 1994, Sellner 1997) and, at the same time, become 'nutritionally upgraded' by the development of a dense epizootic coating (Hoppe 1981).…”

Spatial Interaction Among Nontoxic Phytoplankton, Toxic Phytoplankton, and Zooplankton: Emergence in Space and Time

“…Observations both in vitro and in situ have reported the presence of allelopathy among marine algae [e.g., [10][11][12][13][14]. Algal toxicity is known to have a significant impact on phytoplanktonzooplankton interactions [11,15,16]. Recently, through an integrated study combining a field observation and mathematical modeling, along with coauthors, I have attempted [e.g., [17][18][19] to explore the role of toxin-producing phytoplankton (TPP) in determining the dynamics and maintaining diversity of the overall phytoplankton and zooplankton species in the Bay of Bengal.…”