The physiological ecology of the red-water ciliate mesodium rubrum

Abstract

Red-tides caused by the phototrophic marine ciliate Mesodinium rubrum occur each summer in the Southampton Water estuary and were investigated in the spring/summer of 1985 and in June 1986. The initiation of these blooms appeared not to be light or nutrient mediated, but coincided with periods of water column stability in both years. Stability was promoted both by thermal and salinity gradients, and also by low mixing during neap tides. Blooms were characterized by chlorophyll a concentrations of over 100 /ig I'1, cell numbers of 2-3 x 106 I"1 and near surface oxygen levels of over 150% saturation. Bloom initiation was accompanied by rapid removal of ammonia from the water column, followed by depletion of nitrate when ammonia had become exhausted; however, a considerable quantity of nitrate remained in the water column even at the peak of the bloom. The maximal biomass of M. rubrum appeared to be light limited in the estuary; self-shading by high cell densities of the ciliate imposed an upper limit of ca. 300 mg chla m"2. Irradiance, even at 1 m depth, was only just sufficient (20-30 fj.E nv2 s"1) for photosynthesis to cover estimated respiratory demands. Bloom decline appeared to coincide with a decrease in water column stability, though with a lag period. Vertical distribution of M. rubrum was shown to be strongly aggregated in the upper 3 m; however, a 12 h tidal survey revealed an avoidance of flushing from the estuary by means of swimming downwards during periods of surface turbulence, such as that generated during ebb tide. Vertical distribution examined under more stable conditions in a brackish lake, Inre Verkviken, on the Aland Islands (Finland) in May 1991 suggested that, in the absence of turbulence, multiple population peaks occurred between the surface and 15 m depth. Since nutrients were limiting at the surface, and light was limiting in the nutricline, these peaks could represent migrating groups of either light or nutrient deficient cells, though not necessarily migrating on a diel cycle. Considerable morphological variation occurred in the Southampton Water population just prior to and during red-tides. Irregularly shaped cells and fragments were commonly observed during red-tides and could have been cells undergoing multiple fission. This may explain the wide size distribution of this species observed during blooms. Non-bloom populations examined from several locations tended to be divided into two groups, of both small and large cells, but also with co-occurring intermediate forms. Few factors could be identified which might limit the growth of individuals or populations, however, theoretical considerations suggested that M. rubrum and other fast swimming ciliates and dinoflagellates expend a significant proportion of their energy budgets on locomotion. A technique is described which precisely determines respiration rates of planktonic protists, based upon trapping the release of I4CO2 from prelabelled cells. Since M. rubrum could not be cultured or prelabelled with I4CO2, the technique was utilised on two other planktonic ciliates, Strombidium capitatutn and Favella ehrenbergi. Specific respiration rates of individual cells were in the range 0.5 - 2.0% cell C h"1, although smaller cells had higher rates of up to 5% cell C h1. Using evidence from this thesis and a review of the literature, a tentative hypothesis is presented that M. rubrum is respiration limited in well mixed environments; that is, the cost of swimming may consume much of the photosynthate produced by the endosymbiont. When the water column stabilises and swimming activity is reduced, then much of the saved energy is channelled into cell growth.

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