On the ecology of hyperscum-forming Microsystis aeruginosa in a hypertrophic African lake.
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Date
1987
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Abstract
Light 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.
Description
Thesis (Ph.D.)-University of Natal, Pietermaritzburg, 1987.
Keywords
Eutrophication--Transvaal., Microcystis aeruginosa., Cyanobacteria., Lake ecology--South Africa., Theses--Botany.