The ecology and feeding biology of thecate heterotrophic dinoflagellates
Jacobson, Dean M.
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LocationPerch Pond, Falmouth, MA
A group of thecate heterotrophic dinoflagellates (THDs), principally in the diverse and ubiquitous genus Protoperidinium, was investigated both from an ecological and an organismal perspective. When this study was initiated, nothing was known about their feeding mechanisms, rates or food preferences. The population dynamics of these microheterotrophs were studied in a temperate estuary over a 13 month period, along with co-occurring diatoms, ciliates and pigmented (photosynthetic) dinoflagellates. The timing of several peaks in Protoperidinium abundance coincided with those of diatom blooms, suggesting a possible trophic dependance. During such peaks the biovolume or biomass of the THD community exceeded that of both pigmented dinoflagellates and ciliates. Occurrence patterns of individual THD species were closely related to water temperature; this may indicate the involvement of benthic resting cysts in population succession. Small-scale vertical distributional patterns of THDs were also studied in an embayment with an average depth of 5 m. While two autotrophic dinoflagellate species displayed distinct daily vertical migration patterns, THD species did not; most species maintained a constant 2-5 m depth of maximum abundance, while two others had surface maxima. Feeding behavior, as observed in 19 THD species (Oblea rotunda, Zygabikodinium lenticulatum and 17 species of Protoperidinium) fits the following pattern: a THD cell attaches a slender filament to a prey item (usually a diatom) while it is engaged in a characteristic, spiralling "dance". Subsequently, a pseudopod or "pallium" (a term defined here) emerges from the flagellar pore and envelops the prey within a minute. Ten to sixty minutes later the pallium is retracted and the prey (now a nearly-empty frustule) is discarded. Most species feed only on diatoms, but O. rotunda, Z. lenticulatum (both diplopsaloid species) and P. pyriforme also preyed upon dinoflagellates. Ingestion and growth rates were determined in the laboratory where cultures of Protoperidinium hirobis were fed the diatom Leptocylindrus danicus. Feeding cycles were repeated as often as every 1.5 to 2 hours. Maximal ingestion rates of 23 diatoms*day-1 supported unexpectedly high specific growth rates of up to 1.1*day-1 (1.7 divisions*day-1). Half-maximal growth and grazing rates occurred at approximately 1000 diatoms cells*ml- 1. Peak division frequencies occurred at night, although feeding rate was nearly constant on a diel basis. The ultrastructure of the feeding apparatus was studied in Protoperidinium spinulosum. The pallium, when deployed, is composed of a complex system of membranous channels, vesicles, and a few microtubular ribbons radiating from the flagellar pore. Inside this pore, the pallium is continuous with the contents of an elongate microtubular basket that extends towards the nucleus. The apical end of this basket opens adjacent to the nucleus; at this point its contents become continuous with the central cytoplasmic region. This region is distinguished from the relatively dense, peripheral cytoplasm by the presence of either large electron-lucent vesicles (containing, perhaps, digestive enzymes) or numerous small lipid droplets. Examination of a pre-feeding cell has revealed the likely source of the pallium membranes: dense membranous whorls lie within the microtubular basket. A narrow pseudopodal appendage in two non-feeding cells may constitute the tow filament used in prey capture. A complex myonemaI system, including osmiophilic ring, striated collars and connecting bands is described. The microtubular basket and osmiophilic ring structures were also found in Protoperidinium hirobis, Protoperidinium punctulatum and Oblea rotunda. This thesis has done much to further the understanding of a prevalent component of the protozooplankton, the thecate heterotrophic dinoflagellates. This progress, which was due in a large part to the culture success reported herein, includes new insights into the abundance, feeding behavior, food preferences, feeding rates, and ultrastructural basis of feeding in this preeminent group of the thecate heterotrophic dinoflagellates, the genus Protoperidinium.
Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution February 1987
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