Download FULL TEXT PDF - Freshwater Biological Association

204
D. G. GEORGE
THE INFLUENCE OF GLOBAL WARMING ON FRESHWATER
PLANKTON COMMUNITIES IN BRITAIN
D. GLEN GEORGE
(Dr D. G. George, Institute of Freshwater Ecology, Windermere
Laboratory, Far Sawrey, Ambleside, Cumbria LA22 OLP, England)
Introduction
If present trends continue, most climatologists agree that the
concentration of carbon dioxide in the atmosphere will have doubled by
the year 2050. This increase in C 0 2 will have a direct effect on many
biological processes and an even more important indirect effect on the
global climate. In Britain, average temperatures may be 3-5°C higher
than they are today and there may be even more pronounced seasonal
increases in temperature. Recent models of global warming (Mitchell
1983; Gates 1985; Hansen et al. 1988) suggest that these increases in
temperature will be accompanied by more general changes in the
weather. The distribution of pressure systems over Northern Europe are
almost certain to change and could bring about very pronounced
regional shifts in the average wind speed.
Lake plankton populations are relatively well buffered against sudden
fluctuations in temperature but can react in unexpected ways to seasonal
changes in the wind speed. In recent years, it has become clear that
changes in the timing and intensity of wind mixing can have a profound
effect on the seasonal growth and succession of plankton (Reynolds
1980; Heaney & Butterwick 1985; George et al. 1990). Such effects are
likely to be most pronounced in deep thermally stratified lakes where the
stability of the water column is partly determined by the incident solar
radiation and partly by the intensity of wind mixing. In this short article I
summarize the likely response of freshwater plankton to the direct and
indirect effects of sustained global warming. The direct "physiological"
effects of increased temperature are relatively easy to predict but the
indirect effects of different mixing regimes will only be understood if we
can analyse long-term data sets from a variety of lake systems.
Direct effects of winter and summer warming on the phytoplankton
Physiological responses
Most planktonic algae are able to survive and grow within a relatively
broad range of temperatures. Hawkes (1969) examined the thermal
tolerance of different groups of algae and suggested that diatoms grow
PLANKTON & GLOBAL WARMING
205
best at temperatures below 25°C and blue-green algae at temperatures
above 30°C. There are, however, notable exceptions, such as the diatom
Acnanthes marginulata which can tolerate temperatures up to 41 °C
(Patrick 1969) and the blue-green alga Oscillatoria rubescens which was
described by Findenegg (1947) as a cold-water form.
The physiological responses of phytoplankton to temperature are now
quite well understood (Tailing 1957; Jewson 1976). Most cellular
processes are temperature dependent and their rate typically increases as
an exponential function of temperature. Fig. 1 shows the effect of
temperature on one commonly studied physiological process — the rate
of photosynthesis per unit biomass. The light-saturated rate of
photoassimilation per unit biomass (Pmax) is commonly used as a measure
of photosynthetic capacity. The curves in Fig. 1 show that most algae
photsynethesise most efficently at temperatures of around 25°C. At
higher temperatures Pmax values tend to fall quite dramatically but some
species, such as Scenenedesmus, can tolerate temperatures of 35-40°C.
In practice, the projected increases in temperature are unlikely to have
much effect on photosynthetic capacity since factors other than
temperature frequently limit this key reaction.
Population responses
Most species of planktonic algae grow well at temperatures ranging from
5 to 25°C. In most cases, the population growth increases rapidly at
temperatures between 10 and 20°C and only begins to decline at
temperatures above 25°C. Fig. 2 shows some examples of the effect of
temperature on the growth rates of algae. The growth coefficients (k) are
plotted on a logarithmic scale against a linear scale of temperature. The
lower curves are for two relatively slow-growing forms, Aphanizomenon
flos-aquae and Oscillatoria redekei. The top curve shows the unusually
rapid growth of the small thermophilic species Synechococcus. The textfigure shows that these common species of algae grow most rapidly at
temperatures well above those currently recorded in our inland lakes. A
relatively modest increase in winter and spring temperatures could,
however, give rise to an accelerated succession of species in early
summer. Increasing the rate of succession will not of necessity bring
about a greater turnover of biomass. Most of the algal species that
succeed each other in early summer are fast-growing forms but the
species that appear later in the year tend to be slow-growing. Many of
these slow-growing species, such as Microcystis and Ceratium, give rise
to nuisance water blooms so their early arrival would not be welcomed
by reservoir managers.
206
D. G. GEORGE
PLANKTON & GLOBAL WARMING
207
Community responses
During the International Biological Programme, limnologists throughout
the world attempted to measure 'primary production' in a variety of lakes
(Westlake et al., 1980). The different methods used undoubtedly
introduced a degree of uncertainty, but there were some general
geographic trends with latitude. Annual net production was not strongly
correlated with latitude, but the net annual production in lakes situated
above 59°N was typically less than 15 grams of carbon per square metre.
This trend can partly be explained by the geographical variation in
temperature and partly by the systematic change in the length of the
growing season. In a warmer world, we might therefore expect these
high latitude lakes to become more productive, but productivity
increases at lower latitudes may be limited by qualitative changes in the
plankton.
Direct effects of winter and summer warming on the zooplankton
Physiological responses
Rotifers and microcrustaceans usually account for a high proportion of
the secondary production measured in our inland lakes and reservoirs
(Morgan 1980). At one time, temperature preference was thought to be
one of the main factors controlling the seasonal occurrence of rotifers,
but the unequivocal influence of water temperature is not well
documented. In 1989, Berzins & Pejler published a paper that
summarized the temperaure preferences and tolerances of more than
200 hundred species of rotifers from waters in southern and central
Sweden. They concluded that rotifers generally have a very wide
tolerance of temperature, many common species remaining abundant at
temperatures ranging from 1 to 22°C (Fig. 3). A small proportion of
species, notably those in the genera Notholca, Synchaeta and Filinia, do
appear to be winter stenotherms but they can still tolerate temperatures
of 8 to 10°C.
The temperature tolerance of our common planktonic Crustacea has
yet to be examined systematically. Most species appear to be very
temperature tolerant and it is often difficult to separate the effects of
temperature per se from the effects of a fluctuating food supply. In
Europe, certain common species tend to appear in a band stretching
from the Mediterranean to northern Scandinavia. A few species such as
Holopedium gibberum, Cyclops scutifer and Limnocalanus macrurus
have been characterized as circumpolar but even these can survive in
the hypolimnia of deep lakes in summer.
208
D. G. GEORGE
PLANKTON & GLOBAL WARMING
209
Population responses
Temperature and food are considered to be two of the most important
factors controlling the abundance of freshwater zooplankton. Temperature generally controls growth and hatching rates, whilst the availability
of food affects the fertility of females and the survival of their offspring
(George et al. 1990). In Fig. 4 I have used a simple egg production
model to illustrate the direct effects of temperature on the potential
growth rate of Daphnia. Fig. 4 (a) shows the two temperature scenarios
used to drive the birth rate model. The curve for a 1xC0 2 atmosphere is
a sine wave fitted to current lake temperatures in the English Lake
District. The curve for a 2xC0 2 atmosphere is a sine wave modulated to
give higher winter temperatures (+ 4°C) and higher summer temperatures
(+ 2°C). Fig. 4 (b) shows the effect that these temperatures would have
on the birth rate of a notional population of Daphnia where every
individual carried one egg. It is clear from this text-figure that quite
substantial increases in winter temperature would have less effect on the
reproductive capacity of the population than the more modest increases
in summer temperature. Such a response is typical of many aquatic
invertebrates and reflects the fact that their rate of development is an
inverse linear function of temperature (see Edmondson & Winberg
1971).
Community responses
It is very difficult to identify global trends in zooplankton production
from the data available. Community productivity is intimately related to
individual physiology. Climatic factors that influence the distribution of
individual species thus indirectly influence the ratio of production to
biomass in most zooplankton communities. Some broad generalizations
are, however, possible. Production/biomass ratios tend to increase as
water temperatures increase. The most pronounced changes have been
noted in lakes that have been artificially heated by thermal discharges
(Patalas 1970) but similar trends have also been noted in natural waters
(Morgan 1980). Low production/biomass values are, however,
sometimes recorded in very warm as well as very cold waters. Low
metabolic rates per se undoubtedly limit production in cold waters but
changes in food quality are usually responsible for reduced productivity
levels in warm waters.
210
D. G. GEORGE
Indirect effects of changing weather patterns
Responses of phytoplankton communities
Current atmospheric circulation models suggest that global warming will
fundamentally alter the distribution of pressure belts and the movement
of weather systems across Northern Europe. The seasonal succession of
phytoplankton in lakes is now known to be strongly influenced by timing
as well as the strength of wind-induced mixing. Reynolds (1980) gives a
general overview of the processes involved whilst more recent
publications by the same author (e.g. Reynolds 1987) develop a suite of
models that can be used to predict the general pattern of seasonal
change. The classical view of seasonal succession is essentially
directional and implies a predetermined order in which species or subgroups dominate a community. Such a process of succession is typically
characterized by increasing species diversity and increasing production
until a characteristic "climax" community has evolved:-
where B, C and D represent the dominance of different species in the
succession. In terrestrial ecosystems such natural patterns of succession
are seldom subject to sudden natural reversals. In freshwater
phytoplankton communities the pattern of succession is frequently
interrupted and partially reversed by external perturbations:-
In most lakes, episodes of intense wind-induced mixing are usually
responsible for such sudden reversals. Year-to-year changes in species
dominance are thus intimately related to changes in the intensity and
timing of wind-induced mixing. Fig. 5 contrasts the summer
phytoplankton of Windermere in an unusually calm year and an
exceptionally windy year. In the calm year, (Fig. 5 a), the late summer
phytoplankton was dominated by the buoyant blue-green alga
Oscillatoria agardhii. This alga grows best in relatively poorly mixed
water and can be suppressed by quite short periods of intense mixing. In
the windy year, (Fig. 5 b), the Oscillatoria numbers were very low but
large numbers of small flagellates (microalgae) reappeared in late
PLANKTON & GLOBAL WARMING
211
212
D. G. GEORGE
summer when episodic mixing entrained hypolimnetic nutrients into the
epilimnion.
Responses of zooplankton communities
The weather factors that influence the succession of phytoplankton also
influence the growth and development of the zooplankton. Most species
of zooplankton feed most successfully on the small flagellates that
appear in early summer. Any change in the magnitude or timing of this
critical food "pulse" can therefore have a devastating effect on the
reproductive capacity of the zooplankton. Fig. 6 shows how the seasonal
dynamics of the cladoceran Daphnia hyalina in Esthwaite Water,
Cumbria, can be influenced by the growth and decline of the
microalgae. When a large pulse of microalgae appears in the spring (Fig.
6 a) the Daphnia lay large numbers of eggs that produce a strong
"cohort" of juveniles in early summer. When smaller numbers of
flagellates are present throughout the summer, the Daphnia lay fewer
eggs that result in a more irregular succession of cohorts. A great deal of
attention is now being paid to the matching and mismatching of
population cycles in the phytoplankton and zooplankton (Cushing 1982,
1990). Much more work is, however, needed to relate these changes to
the frequency and intensity of specific mixing episodes.
Conclusions
Most species of phytoplankton and zooplankton can tolerate
temperatures far in excess of those now being predicted for British lakes.
The general changes in atmospheric circulation expected in a warmer
world will, however, have a pronounced effect on the seasonal dynamics
of both phytoplankton and zooplankton populations. Lake plankton
populations are particularly sensitive to changes in the frequency and
intensity of wind-induced mixing. In the short-term, such changes bring
about relatively subtle shifts in species dominance. In the long-term,
however, the continued dominance of certain functional groups may
fundamentally alter the partitioning and transfer of energy in the open
water. Impact studies will thus have to be designed to cover more than
one trophic level at a variety of temporal scales. Particular attention will
have to be paid to the relative timing of physical and biological events in
lakes. Some plankton populations in Britain have already been studied for
more than fifty years. These long-term data sets provide an ideal means of
testing the match-mismatch hypotheses that are currently being advanced
to explain year-to-year variations in the plankton.
PLANKTON & GLOBAL WARMING
213
A number of methods are currently being used to construct regional
scenarios of climate in a warm, high C 0 2 world. Terrestrial ecologists can
refer directly to these predictions, but plankton ecologists need to develop
parallel scenarios of the "weather" beneath the water surface.
Unfortunately many of the key driving variables cannot yet be predicted
with any certainty. We still know very little about the likely change in the
average wind speeds let alone the seasonal distribution and frequency of
extreme winds. In this article I have paid particular attention to the
dynamics of plankton in deep, thermally stratified systems. The plankton
populations in shallow lakes will, however, also be influenced by the
flushing effect of heavy rain. Current climate change scenarios suggest
that Britain will become relatively wetter but there may be more
prolonged droughts in the eastern parts of the country.
Acknowledgements
I wish to thank Diane Hewitt for her help with data processing and Ivan
Heaney for providing unpublished data on the phytoplankton populations
of Windermere. This review is an expanded version of a report prepared
for the first phase of the NERC's "TIGER" programme.
References
Berzins, B. & Pejler, B. (1989). Rotifer occurrence in relation to
temperature. Hydrobiologia, 175, 223-232.
Cushing, D. H. (1982). Climate and Fisheries. Academic Press, London.
Cushing, D. H. (1990). Recent studies on long-term changes in the sea.
Freshwater Biology, 23, 71-84.
Edmondson, W. T. & Winberg, G. G. (1971). A Manual on Methods for
the Assessment of Secondary Productivity in Freshwaters. I.B.P.
Handbook No. 17, Blackwell, Oxford.
Findenegg, I. (1947). Untersuchungen uber die Okologie und die
Produktionsverhaltnisse des Planktons im Karnter Seengebeite.
Internationale Revue des gesamten Hydrobiologie, 43, 368-429.
Gates, W. L. (1985). The use of general circulation models in the analysis
of the ecosystem impacts of climatic change. Climatic Change, 7, 267284.
George, D. G. Hewitt, D. P., Lund, J. W. G. & Smyly, W. J. P. (1990). The
relative effects of enrichment and climate change on the long-term
dynamics of Daphnia in Esthwaite Water, Cumbria. Freshwater Biology,
23, 55-70.
Hansen, J., Fung, I., Lacis, A., Rind, D., Lebedeff, S., Ruedy, R. & Russell,
G. (1988). Global climate changes as forecast by GISS threedimensional model. Journal of Geophysical Research, 93, 9341-9364.
214
D.G.GEORGE
Hawkes, H. A. (1969). Ecological changes of applied significance from
waste heat. In Biological Aspects of Thermal Pollution, (eds Krenkel &
Parker), pp. 15-53. Vanderbilt University Press.
Heaney, S. I. & Butterwick, C. (1985). Comparative mechanisms of algal
movement in relation to phytoplankton production. In Migration:
Mechanisms and adaptive significance (ed.
M. A.
Rankin).
Contributions in Marine Science Supplement, 27, 114-134.
Jewson, D. H. (1976) The interactions of components controlling net
phytoplankton photosynthesis in a well-mixed lake (Lough Neagh,
Northern Ireland). Freshwater Biology, 6, 551-576.
Mitchell, J. F. B. (1983). The seasonal response of a general circulation
model to changes in C 0 2 and sea temperature. Quarterly Journal of the
Royal Meteorological Society, 109, 113-152.
Morgan, N. C. (1980). Secondary Production. In The Functioning of
Freshwater Ecosystems (eds E. D. Le Cren & R. H. Lowe-McConell),
pp. 247-340. Cambridge University Press.
Patalas, K. (1970). Primary and secondary production in a lake heated by
a thermal power plant. In The Environmental Challenge of the 70's (ed.
??), pp. 267-271. Proceedings of the Institute of Environmental Sciences,
16th Annual Technical Meeting, 1970. Boston, Massachusets.
Patrick R. (1969). Some effects of temperature on freshwater algae. In]
Biological Aspects of Thermal Pollution (eds Krenkel & Parker),
pp. 161-185. Vanderbilt University Press.
Reynolds, C. S. (1980). Phytoplankton assemblages and their periodicity
in stratifying lake systems. Holarctic Ecology, 3, 141-159.
Reynolds, C. S. (1984). The Ecology of Freshwater Phytoplankton.
Cambridge University Press.
Reynolds, C. S. (1987). Community organisation in the freshwater
plankton. In Organisation of Communities, Past and Present (eds J. H. R.
Gee & P. S. Giller), pp. 297-325. Blackwell Scientific Publications,
Oxford.
Straskraba, M. & Gnauck, A. (1985). Freshwater Ecosystems: Modelling
and Simulation. Developments in Environmental Modelling, No. 8,
1-309. Elsevier, Amsterdam.
Tailing, J. F. (1957). The phytoplankton population as a compound
photosynthetic system. New Phytologist, 56, 133-149.
Westlake, D. F. ef al (1980). Primary Production. In: The Functioning of
Freshwater Ecosystems, (eds E. D. Le Cren & R. H. Lowe-McConell),
pp. 141-235. Cambridge University Press.