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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. 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