Ecological and evolutionary interactions between the copepod Acartia tonsa and the dinoflagellate Cochlodinium polykrikoides

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Jiang, Xiaodong
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The dinoflagellate Cochlodinium polykrikoides Margalef has formed dense blooms and caused severe fish kills on a global scale in recent decades. The effects of C. polykrikoides on survival, feeding, and fecundity of the copepod Acartia tonsa Dana were examined to determine if it is harmful to grazers. C. polykrikoides significantly reduced copepod survival, feeding, and fecundity within the range of bloom densities. Two bioassay experiments suggested that copepod mortality was due to multiple harmful compounds produced by C. polykrikoides. Although Cochlodinium polykrikoides is harmful to Acartia tonsa at high cell densities, the mixed-diet experiments indicated that C. polykrikoides was nutritious to A. tonsa at low densities. The density-dependent nutritional value of C. polykrikoides to A. tonsa was also demonstrated by the survival experiments. These results suggest a putatively `harmful' alga is not always deleterious to grazers and its ecological effects may be distinctly different during bloom and non-bloom periods. The beneficial effects of Cochlodinium polykrikoides at low cell densities put forth a new question as to how C. polykrikoides cells avoid being completely decimated by grazers before they gain a window of opportunity for bloom formation. Field populations of C. polykrikoides displayed a significantly larger variation in chain length compared to laboratory cultures without grazers. Chain length of C. polykrikoides was significantly increased when exposed to Acartia tonsa adults for 48 h or to fresh (<24 h post-isolation) exudates of A. tonsa. Chain length of C. polykrikoides was correlated with A. tonsa abundance in the field. These results suggest that dissolved chemical cues released by A. tonsa induce chain formation in C. polykrikoides. Ingestion rates of A. tonsa on the 4-cell chains of C. polykrikoides were lower than on single cells, suggesting chain formation may be an effective anti-grazing defense. To quantitatively assess the population dynamics of zooplankton during harmful algal blooms, high-frequency (sampling interval 2 d) time series of Acartia tonsa abundance, egg production rate, and egg hatching success were documented during a Cochlodinium polykrikoides bloom. Embryonic mortality (combined egg-through-the-second-naupliar-stage, egg-N2) was higher than birth rate on most sampling days, resulting in the consistent decline of A. tonsa abundance. Embryonic mortality was correlated with cell density of C. polykrikoides with a 4-d delay. Birth rate was negatively dependent on adult abundance of A. tonsa, but not on cell density of C. polykrikoides. Therefore, the population dynamics of A. tonsa was regulated by algal-density-dependent mortality and copepod-density-dependent birth rate. The potential for evolutionary responses of the copepod Acartia tonsa to the harmful dinoflagellate Cochlodinium polykrikoides was investigated using a common garden experiment and an artificial selection experiment. Copepod resistance to C. polykrikoides was evaluated by egg production rates when feeding on C. polykrikoides relative to the non-toxic flagellate Rhodomonas lens. After six years from the first occurrence of C. polykrikoides in eastern bays of Long Island, A. tonsa populations from bloom areas were significantly more resistant to C. polykrikoides than conspecifics from nearby non-bloom areas. In the laboratory, A. tonsa taken from a non-bloom area gradually increased the resistance when exposed to C. polykrikoides. Copepod resistance in the selection line became three times greater than the control line after four generations. Following a two-generation relaxation of selection, the elevated resistance in A. tonsa was completely lost. The annual occurrence of C. polykrikoides blooms has resulted in the divergence of A. tonsa populations in eastern bays of Long Island from their conspecifics in nearby non-bloom waters. The rates of gain and loss of resistance in A. tonsa to C. polykrikoides were comparable, suggesting these evolutionary changes could occupy the same time scale. The rapid gain and loss of resistance to harmful algae highlight the need to consider the evolutionary responses of grazers in understanding and management of harmful algal blooms
The Graduate School, Stony Brook University: Stony Brook, NY.
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