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On the ecology of hyperscum-forming Microsystis aeruginosa in a hypertrophic African lake.

dc.contributor.advisorBreen, Charles Mackie.
dc.contributor.authorZohary, Tamar.
dc.descriptionThesis (Ph.D.)-University of Natal, Pietermaritzburg, 1987.en
dc.description.abstractLight is the primary source of energy in most of earth's ecosystems . In freshwater ecosystems the major interacting factors that determine the abundance and species composition of planktonic phototrophs, the primary utilizers of light, are nutrients, temperature and light. With increasing eutrophication and declining geographical latitude, nutrient availability becomes in excess of the organisms' requirements, water temperature is more favourable for growth, and community structure depends to a greater extent on light availability. This study focuses on the population dynamics of the bloom-forming cyanobacterium Microcystis aeruginosa Kutz. emend. Elenkin in subtropical Hartbeespoort Dam, South Africa. The objectives of the study were: to investigate the annual cycle, and the factors leading to the dominance and success of the cyanobacterium in this hypertrophic, warm monomictic lake, where light availability is the major factor limiting phytoplankton growth rates; to study the surface blooms and ultimately hyperscums that this species forms; and to assess the ecological significance of hyperscums. A 4. 5-years field study of phytoplankton abundance and species composition in relation to changes in the physical environment, was undertaken. The hypothesis was that M. aeruginosa dominated the phytoplankton population (> 80 % by volume) up to 10 months of every year because it maintained itself within shallow diurnal mixed layers and was thus ensured access to light. It was shown that wind speeds over Hartbeespoort Dam were strong enough to mix the epilimnion (7 - 18 m depth) through Langmuir circulations only 12 % of the time. At other times solar heating led to the formation of shallow ( < 2 m) diurnal mixed layers (Z[1]) that were usually shallower than the euphotic zone (Zeu; x = 3.5 m), while the seasonal mixed layer (zrn) was always deeper than Zeu. From the correspondence between vertical gradients of chlorophyll a concentrations and density gradients, when M. aeruginosa was dominant, it was implied that this species maintained the bulk of its population within Z[1]. Under the same mixing conditions non-buoyant species sank into dark layers. These data point out the importance of distinguishing between Zrn and Z[1], and show the profound effect that the daily pattern of Z[1], as opposed to the seasonal pattern of Zrn can have on phytoplankton species composition Adaptation to strong light intensities at the surface was implicated from low cellular chlorophyll a content (0.132 μg per 10[6] cells) and high I[k ](up to 1230 μE m⁻² S¯¹). Ensured access to light, the postmaximum summer populations persisted throughout autumn and winter, despite suboptimal winter temperatures, by sustaining low losses. Sedimentation caused a sharp decline of the population at the end of winter each year and a short ( 2-3 months) successional episode follCMed, rut by late spring M. aeruginosa. was again dominant. The mixing regime in Hartbeespoort Dam and the buoyancy mechanism of M. aeruginosa led to frequent formation of surface bloons and ultimately hyperscums. Hyperscums were defined as thick (decimeters), crusted, buoyant cyanobacterial mats, in which the organisms are so densely packed that free water is not evident. In Hartbeespoort Dam in winter M. aeruginosa formed hyperscums that measured up to 0.75 m in thickness, covered more than a hectare, contained up to 2 tonnes of chlorophyll a, and persisted for 2 - 3 monnths. Hyperscum formation was shown to depend upon the coincidence of the following preconditions: a large, pre-existing standing crop of positively buoyant cyanobacteria; turbulent mixing that is too weak to overcome the tendency of the cells to float, over prolonged periods (weeks); lake morphometry with wind-protected sites on lee shores; and high incident solar radiation. The infrequent occurrence of hyperscums can be attributed to the rare co-occurrence of these conditions. Colonies in the hyperscum were arranged in a steep vertical gradient, where colony compaction increased exponentially with decreasing distance form the surface. This structure was caused by evaporative dehydration at the surface, and by the buoyancy regulation mechanism of M. aeruginosa., which results with cells being unable to lose boyancy when deprived access to light from above. The mean chlorophyll a concentration and water content were 3.0 g 1¯¹ and 14 % at the surface crust, 1.0 g 1¯¹ and 77 % at a few mm depth, and 0.3 g 1¯¹ and 94 % at 10 cm depth, where M. aeruginosa cell concentration exceeded 109 ml¯¹. A consequence of the high cell and pigment concentrations was that light penetrated only 3 mm or less, below which anaerobic, highly reduced conditions developed. Nutrient concentrations in hyperscum interstitial water, collected by dialysis, increased dramatically with time (phosphate: 30-fold over 3 months; ammonia: 260-fold). Volatile fatty acids, intermediate metabolites in anaerobic decomposition processes, were present. Gas bubbles trapped within the hyperscum contained methane (28 %) , and CO[2] (19 %), the major end products of anaerobic decomposition, and no oxygen. The structure and function of M. aeruginosa in hyperscum was examined in relation to the vertical position of colonies and the duration of exposure to hyperscum condition. Colonies and cells collected from 10 em depth in the hyperscum were similar in their morphology (light and fluorescent microscopy) and ultrastructure (transmission and scanning electron microscopy) to those of colonies from surface blooms in the main basin of the lake. With declining depth over the uppermost 10 mm of the hyperscum cells appeared increasingly dehydrated, decomposed and' colonized by bacteria. studies employing microelectrode techniques demonstrated that photosynthetic activity of colonies at the surface of a newly accumulated hyperscum rapidly photoinhibited, substrate-limited, and then ceased within hours of exposure to light intensities > 625 μE m⁻² S¯¹. Photooxidative death followed. The dead cells dehydrated to form the dry crust, from underneath. and space was thus created for colonies rising Cells collected from 10 cm depth retained their photosynthetic capacity ([14]C-uptake experiments) throughout the hyperscum season, although a considerable decline in this capacity was noted over the last (third) month. Altogether the data indicated that spatial separation developed within the hyperscum, between a zone at the surface of lethal physical conditions, a zone beneath the surface of stressful and probably lethal chemical conditions, and a deeper zone of more moderate conditions, which nevertheless, deteriorated after 2 - 3 months. A conceptual model describing the fate of a colony entering a hyperscum was then proposed. According to this model, a colony that arrives below a hyperscum and is not carried away by currents, becomes over-buoyant in the dark and floats into the bottom of the hyperscum. With time it migrates towards, due to its own positive buoyancy, the buoyancy of colonies rising from underneath, and the collapse of cells at the top. It survives in the dark, anaerobic environment by maintaining low levels of basal metabolism while utilizing stored reserves. Depending on weather conditions, the colony mayor may not remain within the hyperscum long enough to reach the zone of decomposition near the surface, where it would die. With the aging of the hyperscum and the accumulation of trapped decomposition products, the zone of decomposition expands. Thus, a hyperscum is essentially a site of a continuous cycle of death and dehydration at the surface and upward migration of colonies from below to replace those that died, although not all colonies entering the hyperscum necessarily reach the lethal zone. The formation of hyperscums was shown to have no major influence on the annual cycle of M. aeruginosa in Hartbeespoort Dam. The seasonality of increase and decline of the planktonic population was similar from year to year, irrespective of whether or not hyperscums formed. The phenomenon of hyperscums demonnstrated that, as Reynolds and Walsby (1975) claimed, thick cyanobacterial water-blooms do form incidentally and have no vital function in the biology of the organism. water temperature did have a major effect on the annual cycle of this species in Hartbeespoort Dam. In temperate lakes the low water temperatures in autumn and winter (<10° C) cause M. aeruginosa to lose its ability to regain buoyancy in the dark, and consequently it sinks to bottom sediments. The higher ( > l2°C) minimum winter temperature in Hartbeespoort Dam leads to the maintenance of a relatively large residual planktonic population throughout the winter. Unlike the case in temperate lakes, the long-term survival of M. aeruginosa in warm-water lakes probably does not depend on winter benthic stocks for the provision of an inoculum for the following growth season.en
dc.subjectMicrocystis aeruginosa.en
dc.subjectLake ecology--South Africa.en
dc.titleOn the ecology of hyperscum-forming Microsystis aeruginosa in a hypertrophic African lake.en


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