The role of heterotrophic microflagellates in plankton communities
1984-06,
Caron, David A.
The distribution and feeding behavior of bacterivorous micro flagellates
(2-20 μm protozoa) and their ingestion by copepods were examined in an attempt
to assess the importance of these protozoa as a trophic link between
planktonic bacteria and zooplankton. The abundance of microflagellates
relative to other picoplankton (0.2-2.0 μm) and nanoplankton (2-20 μm)
populations in water samples in the North Atlantic and in Lake Ontario and on
macroaggregates in the North Atlantic was determined using direct
microscopical and culture estimation techniques. Seasonal, vertical and
geographical changes in the density of microflagellates were generally not
greater than one order of magnitude. Microscopical counts of heterotrophic
nanoplankton (presumably microflagellates) typically ranged from a few hundred
to a few thousand m1-1 for a variety of planktonic environments. They
constituted approximately 1/3 to 1/2 of the nanoplankton in the euphotic zone
and dominated the nanoplankton in the aphotic zone. Most Probable Number
(MPN) estimation of the density of bacterivorous protozoa indicated that
microflagellates were, on average, an order of magnitude more abundant than
bacterivorous ciliates and amoebae. MPN and direct microscopical counts of
microflagellates differed by as much as 104. This discrepancy was smaller
in eutrophic environments (e.g. Continental Shelf and Lake Ontario) and on
macroscopic detrital aggregates.
All microbial populations enumerated were highly concentrated on
macroscopic detrital aggregates relative to their abundance in the water
surrounding the aggregates. Enrichment factors (the ratio of abundance of a
population on a macroaggregate to its abundance in the surrounding water)
increased along a eutrophic-to-oligotrophic gradient because of the combined
effects of an increased abundance of microorganisms on macroaggregates in
oligotrophic environments and a decreased abundance in the surrounding water
in these same environments. Average enrichment factors for direct
microscopical counts of heterotrophic nanoplankton (range = 17-114) were not
as large as enrichment factors observed for MPN estimates of the number of
bacterivorous microflagellates (range = 273-18400). Microflagellates
numerically dominated the bacterivorous protozoa cultured from macroaggregates
by one to two orders of magnitude, but ciliates and amoebae were also highly
enriched on macroaggregates. Microenvironments are therefore a potentially
important aspect for the ecology of planktonic microorganisms. Observations
on the microbial colonization of mucus sloughed by ctenophores and discarded
appendicularian houses suggest that these materials may be important sources
of macroaggregates.
Batch and continuous culture experiments were conducted with clonal
cultures of microflagellates to test their ability to grow on various types
and densities of bacteria. The doubling time of Monas sp. 1 ranged from 43 hr
(when fed the cyanobacterium Synechococcus Strain WH 8101) to 6.9 hr (when fed
the heterotrophic bacterium Serratia marinorubra). Cell yields (i.e. the
conversion of bacterial biomass into protozoan biomass) of Monas sp. 1 fed two
species of heterotrophic bacteria were greater than yields for the
microflagellate fed two species chroococcoid cyanobacteria (range = 7-68%).
Cell yields of two other species of microflagellates (Monas sp. 2 and
Cryptobia maris) were 48% and 61%, respectively, on the bacterium Pseudomonas
halodurans. Microflagellates grew in continuous culture at concentrations of
bacteria which were lower than bacterial densities required for the growth of
ciliates as shown by other investigations. Therefore, microflagellates appear
to be well-adapted for grazing bacterioplankton.
Microflagellates were also investigated for their ability to graze
bacteria attached to particles. Bodo nanorensis and Rhynchomonas nasuta both
showed a marked ability to graze attached bacteria and a limited ability to
graze unattached cells. These results suggest that microflagellates may also
be important consumers of bacteria attached to particles in the plankton and
may explain the highly elevated densities of microflagellates on
macroaggregates.
Grazing experiments performed with the copepod Acartia tonsa indicated
that heterotrophic microflagellates were ingested by the copepods at rates
comparable to the ingestion of phytoplankton of similar size. The presence of
heterotrophic microflagellates did not depress filtration rates of the
copepods, and one species (Cryptobia maris) appeared to be selectively
grazed. Survival of A. tonsa on a diet of heterotrophic microflagellates was
similar to survival on a diet of phytoplankton and was significantly longer
than survival of starved Controls or copepods fed only bacteria.
Due to their ability to grow at in-situ densities of planktonic bacteria,
their relatively high cell yields, and their acceptability as food for
zooplankton, it is concluded that bacterivorous microflagellates may
constitute an important trophic link between bacteria and zooplankton. This
link may provide a mechanism whereby organic material and energy from the
detrital food chain can be returned to the classical phytoplankton-copepod-fish food chain.