The regulation of phytoplankton population dynamics in the world's largest lakes

Aquatic Ecosystem Health and Management 3 (2000) 1–21 www.elsevier.com/locate/aquech

The regulation of phytoplankton population dynamics in the world’s largest lakes C.S. Reynolds a,*, S.N. Reynolds a, I.F. Munawar b, M. Munawar b b

a NERC Institute of Freshwater Ecology, Windermere Laboratory, Ambleside LA22 0LP, UK Great Lakes Laboratory for Fisheries and Aquatic Sciences, Fisheries and Oceans Canada, P.O. Box 5050, Burlington, Canada L7R 4A6

Abstract The world’s largest lakes, really inland seas, are characterised by long retention times, and are dominated by internal physical forcing, generally low nutrient loadings and predominantly internal recycling. Most are oligotrophic. Many are severely phosphorus deficient. Certainly few ever support large crops of phytoplankton. Horizontal heterogeneity sometimes permits enhanced production in shallow bays or behind thermal bars and occasional blooms develop under conditions of near-surface stratification. An assessment of published information on the composition and seasonality of phytoplankton in the open water habitats of these lakes confirms the oligotrophic nature of the world’s great lakes. There is a predominance of diatoms at all latitudes; chrysophytes are seasonally prominent in some lakes at high latitude; other flagellates, including dinoflagellates, and species of cyanobacteria represent increasing proportions of the pelagic biomass towards the equator. There is an indication that species composition is influenced by underwater light availability and a positive correlation between Microcystis plankton and relatively higher concentrations of total phosphorus (TP . 30 mg l 21) is suggested. Picoplankton is apparently abundant during periods of relatively high insolation of the water column. Although the carrying capacity of the nutrients available is scarcely large, the production of biomass is strongly related to seasonal variability in the intensity and extent of water-column mixing and its relation to the periodicity and underwater penetration of photosynthetically active radiation. Attainment of nutrientlimited crops generally coincides with shallow mixing whereas deep circulation suppresses production. The differential effects of latitude, local climate and salinity upon this general deduction are also evaluated. The role of grazing, its contribution to nutrient recycling, and its contribution to sustaining pelagic food webs, is also considered. The paper makes some deductions about the threats placed on large-lake ecosystems by pollution, eutrophication and acidification and upon how their ecosystem health might be monitored and conserved in the future. q 2000 Elsevier Science Ltd and AEHMS. All rights reserved. Keywords: Great lakes; Phytoplankton; Population dynamics

1. Introduction The first century of scientific studies on the phytoplankton of lakes is drawing to a close. The initial * Corresponding author. Tel.: 1 44-1539-4-42468; fax: 1 441539-4-46914. E-mail address: [email protected] (C.S. Reynolds).

fascination was in discovering what lived in open water and how it was adapted to do so. This led to a great expansion of knowledge about the lives of planktonic autotrophs, of their abundance and production, of their fluctuating growth rates and physiology and of their ultrastructure and biochemistry. In recent years, great interest has been focussed on their role in pelagic food webs and how primary products are

1463-4988/00/$20.00 q 2000 Elsevier Science Ltd and AEHMS. All rights reserved. PII: S1463-498 8(99)00066-4

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transferred to the dependent heterotrophs of the open water. Techniques of investigation have also developed enormously, far beyond dipping bottles or nets in the water for specimens to examine by light microscopy, towards the sophistication of today’s satelliteborne remote sensing, flow cytometry and the battery of methods introduced through advances in molecular biology. Currently, the understanding of phytoplankton population dynamics and the processes of community assembly and organisation in the pelagic is advancing strongly but it is dominated by perspectives founded upon studies in much smaller lakes, where sampling at the appropriate spatial resolution and temporal frequencies can be accommodated more satisfactorily. The reasons for this are plainly logistic. As with plankton studies of the ocean, there is a mismatch between the scales of ship-borne operations and of planktonic population processes: effort can be invested in intensity but not, generally, in frequency. Thus, it is humbling to recognise that the dynamics of phytoplankton in the 90% of the world’s aggregate lake volume that is stored in its largest lakes (Herdendorf, 1982) are scarcely known at all. In this article, we seek to align some of the information which is available about the composition, productivity and seasonality of phytoplankton in a selection of the world’s great lakes, drawing on definitive local studies as well as previous reviews (Serruya and Pollingher, 1983; Munawar, 1987; Pollingher, 1990) and compilations (Kira, 1984), with the extrapolations of specific cell performance that it is possible to infer from modelling and experimental approaches based on much smaller lakes (Reynolds, 1986, 1989, 1990). Thus, the paper is not in any sense another review. Rather, it is an attempt to discern patterns among the reported behaviours of the plankton in large lakes and to fit these to a paradigm of phytoplankton growth and dynamics developed from studies on the phytoplankton of much smaller lakes. It seeks to develop testable hypotheses about the functional aspects of phytoplankton in large lakes, which may be investigated during the second century of its study. The paper considers the dataset which we have analysed in order to determine qualitative patterns in the seasonality, abundance and species composition in large lakes. General deductions and prognoses are set out towards the end of the paper.

2. Approaches adopted in this study Our first step was to delimit a dataset. From the morphometric data assembled by Herdendorf (1982) (see also Beeton, 1984; Herdendorf, 1990), we selected, really quite arbitrarily and on the basis of the literature we were able to locate, the twelve largest inland waters by volume (.1500 km 3); then we added the nine largest in area (.80 000 km 2) and the five of greatest depth ($450 m), which were not otherwise included. Those lakes whose volumes are conspicuously variable but which, at capacity, fulfil one of the above criteria were also included. The literaturesearch was able, in many instances, to provide information on the annual patterns of density stratification, thermal-bar formation, ice cover, the depth range of the surface mixed layer, its clarity, its basic water chemistry, its phosphorus content (either dissolved, total or both) and the reported seasonal abundance and composition of its phytoplankton. Attention was paid also to the reported structure of the zooplankton and of the fish community. Despite many blanks, we were able to construct a spread-sheet, which, in its final form, was used to sort and classify biotic features against geographical, limnological and trophic outputs. These extrapolations are what were then reviewed in the context of the physiological ecology of planktonic algae and their pelagic consumers. Finally, the deductions are worked into a series of falsifiable hypotheses which future research and training may be able to test.

3. The data set The list of the ‘world’s largest lakes’ so adopted, together with relevant geographic and morphometric information, is presented in Table 1. Nomenclature follows Herdendorf’s (1982) ‘latinised local names’. The list was appended provisionally with information gleaned from the literature and pertaining to certain physical and chemical properties of the water bodies. The main sources consulted are listed in Table 2. Note that the dataset does not make any reference to Danau Matano, Indonesia. The depth of this classical graben lake has recently been found to be in excess of 550 m (Haffner et al., 2000) which would certainly have qualified it for inclusion. If the lake is always

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Table 1 The selection of large lakes, together with latitude, longitude and elevation and morphometric details (mostly from Herdendorf, 1982, 1990; Beeton, 1984) Volume (km 3)

Kaspiyskoye More Ozero Baykal Lac Tanganyika Lake Superior Lake Malawi Lake Michigan Lake Huron Lake Victoria Great Bear Lake Ozero Issyk-kul Lake Ontario Great Slave Lake Aralskoye More Lake Erie Lake Winnipeg Ladozhskoye Ozero Lagoa dos Patos Ozero Onezhskoye Lake Turkana Lago Titicaca Lago de Nicaragua Crater Lake Danau Toba Lake Tahoe Lac Kivu Mjøsa Ozero Balkhalsh Lac Tchad Lake Eyre Dangting Hu Lac Bangweolo

78 200 22 995 18 900 12 100 6140 4920 3540 2700 2240 1740 1640 1580 1090 483 371 908 20 280 251 893 108 16 249 124 570 56 106 72 30 18 5

Area (km 2)

374 000 31 500 32 900 82 100 22 490 57 750 59 500 68 460 31 150 6240 19 100 27 200 68 000 25 660 24 390 18 140 10 140 9890 8660 8370 8150 48 1100 500 2370 365 18 200 16 600 9700 2740 4900

Depth (m) Mean

Max

209 730 574 147 273 85 59 39 72 279 86 58 16 19 15 50 2 28 29 107 13 333 226 249 240 154 5.8 4.3 3.1 6.5 1.0

1025 1741 1471 407 706 282 229 84 446 668 245 614 68 64 18 230 5 120 73 281 70 589 529 505 480 449 26.6 12 5.7 30.8 5

isothermal, as the preliminary data suggest, the ecology of its phytoplankton would make a doubly rewarding study. Before going to press, the authors were informed of a new survey of Lago General Carera (Chile/Argentina: 46830 0 S, 72800 0 E) which is over 590 m in depth (Dr D. Pugh, pers. comm.).

3.1. Seasonal stratification and mixing Attributes of the lakes relating to their reported characteristics of density stratification and hydraulic mixing are summarised in Table 3. The arrangement

Elev. (m)

Lat.

Long.

Retention (Y )

228 450 774 183 475 176 176 1134 156 1608 75 156 53 174 217 5 1 35 427 3812 32 1882 906 1899 1463 121 341 280 212 34 1140

42 N 53 N 6S 48 N 12 S 44 N 45 N 1S 66 N 43 N 44 N 62 N 45 N 42 N 53 N 61 N 31 S 62 N 4N 16 S 12 N 43 N 3N 39 N 2S 61 N 46 N 14 N 29 S 29 N 11 S

51 E 108 E 30 E 87 W 35 E 87 W 83 W 33 E 120 W 78 E 78 W 114 W 60 E 82 W 98 W 32 E 51 W 36 E 36 E 69 W 86 W 122 W 99 E 120 W 29 E 11 E 76 E 14 E 137 E 113 E 30 E

Endorheic 390 7000? 170 750 100 21 23 124 305 8 12 Endorheic 2.5 3.6 12 ? 12 13 1300 ? ? , 200 . 350 ? 6 7

of the lakes follows the classification and terminology of Lewis (1983). All but the shallowest of these lakes are subject to density stratification for most of the year. Overturn, if it occurs at all, is convectional. Tanganyika, Malawi and Kivu, all deep equatorial lakes, are classically meromictic. The maximum reported mixed depth in Toba (300 m; Mizuno, 1977) is well short of the maximum depth of the lake; thus, we classify it as meromictic. Full-column overturn in Crater and, possibly, even Tahoe may also be exceptional. At high latitudes, depth is no obstacle to convective overturn once or twice per year. In Great Bear, lake temperature rarely ever exceeds 48C; stratification is

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Table 2 Literature sources consulted in database construction Limnological background

Phytoplankton

Aralskoye Baykal

Williams and Aladin (1991); Aladin et al. (1993) Rossolimo (1957); Kolpakova et al. (1988)

Balkhalsh Bangweolo Crater Dangting Erie Eyre Great Bear Great Slave Huron Issyk-kul Kaspiyskoye Kivu Ladozhskoye Malawi Michigan Mjøsa Nicaragua Onezhskoye Ontario Patos Superior Tahoe Tanganyika Tchad Titicaca Toba Turkana Victoria Winnipeg

Ergashev (1979) Serruya and Pollingher (1983) Larson et al. (1987) Kira (1988) Gray et al. (1994). Kotwicki (1986); Williams and Kokkinn (1988) Johnson (1975, 1994) Moore (1980) Gray et al. (1994) Shaboonin (1982); Revyakin (1987) Kosarev and Yablonskaya (1994) Talling (1969); Serruya and Pollingher (1983) Raspopov (1985); Petrova and Respletina (1987) Eccles (1974); Patterson and Kachinjika (1995) Beeton (1984) Holtan (1979, 1980, 1981) Serruya and Pollingher (1983) Raspopov (1985) Gray et al. (1994) Yunes et al. (1996) Gray et al. (1994) Goldman (1988) Coulter (1988) Sikes (1972); Carmouze et al. (1983) Richerson et al. (1986) Mizuno (1977) Hopson (1982); Ka¨llquist et al. (1988) Talling (1966, 1986) Hecky et al. (1986); Brunskill et al. (1994)

Ergashev (1979); Aladin et al. (1993) Kozhov (1963); Popovskaya (2000); Verbolov et al. (1989); Shimarev et al. (1993) Abrosov (1973) Serruya and Pollingher (1983) Larson et al. (1987); McManus et al. (1992) Kira (1988) Munawar and Munawar (1981, 1986, 1996)) Blinn (1991) Johnson (1994) Duthie and Hart (1987); Pollingher (1990) Munawar and Munawar (1981, 1986, 2000) Kulumbaeva (1982); Savvaitova and Petr (1992) Kosarev and Yablonskaya (1994) Serruya and Pollingher (1983) Raspopov (1985); Petrova and Respletina (1987) Patterson and Kachinjika (1995); Allison et al. (1996) Munawar and Munawar (1986, 2000) Holtan (1978, 1979) Serruya and Pollingher (1983) Raspopov (1985) Munawar and Munawar (1981, 1986, 1996) Yunes et al. (1998) Munawar and Munawar (1981, 1986, 2000) Carney and Goldman (1988) Talling (1986) Sikes (1972); Compe`re and Iltis (1983) Serruya and Pollingher (1983) Serruya and Pollingher (1983) Hopson (1982); Liti et al. (1991) Talling (1966, 1986) Hecky et al. (1986); Brunskill et al. (1994); Patalas and Salki (1992)

always inverse. At any latitude, shallowness and expanse make lakes vulnerable to frequent winddriven holomixis: six of the lakes, all with mean depths ,13 m are supposed to be polymictic. Two others (Winnipeg, Balkhalsh) are frequently fully wind-mixed outside the months of thermal stratification. Mixing and stratification are the proximal manifestations of climatic seasonality. Lakes at high latitude experience conspicuous annual cycles of daylength and radiation income. Inverse stratification is a necessary precursor to ice cover and is associated with the short days and low winter air temperatures: all the continental lakes north of 508N have winter surface temperatures well below 48C and freeze over quite regularly. Partial ice-cover is more typical of the

Laurentian Great lakes and of the Norwegian Mjøsa which is sufficiently close to the Atlantic Ocean to experience the moderating influence of the Gulf Stream ocean currents. In much the same way, longer days and stronger solar heat-fluxes experienced at lower latitudes and during high-latitude summers. It is not usual among the published density gradients to discern the kind of sharp pycnoclines that are familiar to smalllake limnologists. Sharp gradients at the floor of the surface mixed layer are only occasionally reported, most strikingly those marking the lower boundary of the convectional layer under snow-free ice in Baykal (see Rossolimo, 1957). Elsewhere, mixing energy is propagated downwards through layers while the scale of heat transfer is only rarely sufficient to generate the

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Table 3 Thermal and mixing characters of large lakes; roman numerals denote months

Cold monomictic Great Bear Dimictic Baykal Superior Michgan Huron Ontario Great Slave Erie Winnipeg Ladozhskoye Onezhskoye Mjøsa Balkhalsh Warm monomictic Victoria Issyk-kul Turkana Titicaca Tahoe Meromictic Tanganyika Malawi Crater Toba Kivu Discontinuous warm polymictic Nicaragua Dangting

Ice cover

Thermal stratification

Mixing, depths

XI–VII a

–

Convectional, always ,48C, VII–XI b

I–V a XI–IV c I–III c I–III c I–IV c XII–VI a I–III c XI–III a II–V a I–V a XII–III c XI–IV a

VII–X; to ,20 m VII–IX; to ,25 m VII–XI; to ,25 m VII–XI; to ,25 m VI–X; to ,22 m VII–VIII; to ,30 m VI–X; to ,22 m VII, VIII, variable VI–XI; to ,25 m VI ê XI; 20 ê 30 m VII–XI; to 18 m V–X; to 18 m

Convectional, always ,48C, VI, XI,XII Convectional, always ,48C, V, X Convectional, always ,48C, IV, XII Convectional, always ,48C, IV, XII Convectional, always ,48C, V, XI Convectional, always ,48C, X, XII Can be substantially wind mixed Frequently wind-mixed Sometimes wind mixed Wind assisted convection Convection, always , 48C, V, X–XII Frequently wind-mixed

– – – – –

IX–V; variable to 40 m IV–XII; 20–30 m I–VII; 40–50 m X–VI; 40–70 m VII–VIII; .50 m

Frequently wind mixed to bottom, VI–VIII Convection, ,48C. II Convection, @ 48C, Wind assisted Convection @ 48C, Wind assisted Convection .48C, Wind assisted

– – Rare

IV–VII; 40–50 m X–III; ,40 m IV–IX; 20–70 m , 300 m all year , 70 m all year

Deepens VIII–XII, 100–250 m Deepens IV–V to .80 m Deepens to ,200 m in X

– –

Tchad Eyre Bangweolo a b c

Mixing possible throughout year, assisted by wind Mixing possible throughout year, assisted by wind

–

Continuous warm polymictic Patos

Exposed to strong S.E.winds.

– – – –

Typical shallow poymictic Nearcontinuous mixing Typical shallow polmictic Diel mixing Presumed to be typical shallow polymictic Presumed to be typical shallow polymictic

Icecover complete in most years. Complete mixing does not occur every year. Ice cover partial and absent in some years.

buoyancy which alone overcomes the inertia of residual momentum in deep water columns. Temperature gradients through the upper 100 m are usually quite gradual and the depth and thickness of seasonal thermoclines are often difficult to determine from temperature profiles alone: solute content (including gases) is generally a more reliable guide to vertical integration or to the lack of it. In this context, it is not easy to find data to

support the prevalence of Seiche activity among the world’s great lakes (Tilzer and Bossard, 1992) unless there is a developed themocline (see, for instance, Rossolimo, 1957). On the other hand, for large, irregular basins, the contribution of inertial (Coriolis’) forces in propagating momentum is undoubtedly great. It is not clear that large lakes at low latitudes are different from high-latitude lakes in these general

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properties. Being always much warmer than high-latitude lakes, however, tropical lakes are sensitive to quite small variations in air temperature. Seasonal and stochastic differences in cloud cover or wind activity (with accelerated evaporation in many cases) promote density instabilities in the water column and can lead to convective mixing through considerable depths. In this way, quite regular and pronounced seasonal changes in water-column stability occur during the calendar year. Thus, even the equatorial Lake Victoria experiences seasonal alternation between being isothermal and frequently fully mixed between June and August of most years but the lake is thermally stratified at other times (Serruya and Pollingher, 1983; Payne, 1986). Probably in all lakes at low latitude, however, the solar heat flux can lead to significant warming at the lake surface, whenever wind dissipation is sufficiently weak. At night, most of the heat gained is radiated back to the atmosphere or consumed in evaporation and the daytime heat gain is largely shed. This process of diurnal stratification and nocturnal mixing is particularly well described for Lake Titicaca (see Powell et al., 1984). Over periods of weeks to months, a recognisable epilimnion can develop, subject to the (general) difficulty of defining its variable boundaries. Net seasonal heat loss, often compounded by more frequent strong winds, reverses the processes and such thermal structure as exists may be eroded and discharged. Another type of temperature gradient associated principally with large lakes is the thermal bar. Vernal heating of the shallow inshore proceeds faster than the deeper offshore waters and, while the main body of the lake is ,48C, the warmer water is retained in inshore circulations separated from the open lake by pronounced frontal boundaries. Stoermer (1968) provided one of the earliest indications of the importance of thermal bars on the seasonal growth of phytoplankton from a study on Grand Haven in Michigan. Impacts upon diatom dynamics have since been reported from within the vicinities of thermal bar formations in Ontario (Munawar and Munawar, 1975), in Issyk-kul (Shaboonin, 1982), in Ladozhskoye and Onezhskoye (Raspopov, 1985; Petrova, 1986; Petrova and Respletina, 1987) and in Baykal (Shimarev et al., 1993; Likhoshway et al., 1996). The behaviour is expected to be general among the large northern lakes. Elsewhere, and at other times,

considerable large-scale horizontal disparity in the distribution of phytoplankton (mesoscale and reproductive patchiness) is likely to occur, simply because algae can grow faster than they can be dispersed through large basins (see the model of Joseph and Sendner, 1958). Some of the clearest examples come from the Laurentian Great Lakes (see, especially, Munawar and Munawar, 1996): algae grow faster in inshore areas, as a function of better average insolation, often, greater local inputs and availabilities of nutrients: some areas of these lakes are well-known for their enhanced productivities (Green Bay of Michigan; Saginaw Bay of Huron: Munawar and Munawar, 1996, 2000). Except where otherwise stated, we have directed our attention to the events in the open waters (the true pelagic) of these lakes. 3.2. Other characters of the database lakes Tables 4–9 list in order the lakes in the database according to latitude (Table 4), mean depth (Table 5), water clarity (as the range in reported Secchi-disc readings in open water: Table 6), and the ranges in the ratio of Secchi depth to mixed depth (zs =zm : Table 7). These are properties of the physical environment whose quantitative values have a profound significance for the rates of specific photosynthesis and biomass replication of the primary producers: deep mixing relative to light penetration is often very large (zs =zm , 0:1 for long periods) in all but the shallowest examples considered, although several of the shallow lakes are often very turbid (Dangting, Tchad, Winnipeg). The absolutely clearest waters are in Tahoe, Crater and Great Bear; the most consistently favourable photic conditions are found in Crater and Balkhalsh. In Table 8, a preliminary sub-division of the lakes in respect of the relationships involving alkalinity and free carbon dioxide, is presented. The treatment was devised largely on the basis of reported pH values. Thus, a class (1) of circumneutral lakes was identified as being always circumneutral and in which reported pH values have not exceeded 7.2–7.3. Class 2 lakes are weakly buffered to the extent that pH fluctuates quite widely between ,7 and up to pH 9, and where free carbon dioxide is depleted to very low levels at times. Class 3 lakes are those which are adequately buffered at pH values .8.2 and wherein bicarbonate

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Table 4 The distribution of representative phytoplankton categories 1–12 (see text and Table 10) in the database lakes arranged by latitude from North to South

Great Bear Great Slave Onezhskoye Ladozhskoye Mjøsa Baykal Winnipeg Superior Balkhalsh Huron Michigan Ontario Crater Issyk-kul Erie Tahoe Dangting Tchad Nicaragua Turkana Toba Victoria Kivu Tanganyika Bangweolo Malawi Titicaca Eyre Patos

Lat.

1

2

3

4

5

6

7

8

9

10

11

12

66 N 62 N 62 N 61 N 61 N 53 N 53 N 48 N 46 N 45 N 44 N 44 N 43 N 43 N 42 N 39 N 29 N 14 N 12 N 4N 3N 1S 2S 6S 11 S 12 S 16 S 29 S 31 S

X z z z z z z X z X X z z z z z z z z z z z z z z z z z z

z X X X X X X z z z z X z z X z z z z z z z z z z z z z z

z z X X X z z z X z z z X X z X z X X X z X X X z X z X z

X X z z z X z X z X X z z z z X z z z z z z z z z z z z z

z z X z z z z z z z z X z X X z z z z X z z z X z z X z z

z z z z z z z z z z z z z z z z z X z z z z z z X z z z z

z z z z z z X z z z z z z z z z z X z z z X z z X z z z z

z z z X z X z z X z z z z X z z X z z z z z z z z z X z z

. z z z z X z z X z z z X z z z z X z X X X X X z X X z z

z z z z z z z z X z z z z z z z z X z X z z X z z z z z X

z z X X X z z z z z z z z z z z z z z z z z z z z z z z z

z z z z z z z z X z z z z X z z z z z z z X X z z z X z z

is likely to be the prime carbon source for primary producers. A fourth category created for acidic lakes was not required. In Table 9, some information relating to soluble reactive phosphorus (SRP, ˆorthophosphate-P) concentrations is presented (as a maximal value in the supposition that it is biologically available) and to the reported ranges of total phosphorus (TP). The entries are arranged in approximately descending order. It is an extraordinary fact that the TP concentrations of the large lakes selected span fully four orders of magnitude, embracing values which are said, on the basis of studies on smaller lakes, to be indicative of grades from the ultraoligotrophic to the hyper-eutrophic. Using traditional criteria for discriminating among lakes (Thienemann, 1918; Naumann, 1919), most of the lakes are firmly oligotrophic. The eutrophic criterion of

deep-water anoxia is met in the tropical meromictic lakes Kivu, Malawi and Tanganyika and, significantly, also in Victoria. Hypolimnetic oxygen depletion during the stratified period, attributable to high rates of microbial metabolism, takes Victoria into the eutrophic category. On the basis of biomass yield, Patos and, historically, Erie should be considered to be eutrophic. Relatively low inputs of nitrate and rapid rates of denitrification of ammonia in these warm lakes probably contribute to significant nitrogen deficiencies.

4. Spatial patterns of phytoplankton distribution among great lakes Given the limitations on the quality and frequency

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Table 5 The distribution of representative phytoplankton categories 1–12 (see text and Table 10) in the database lakes arranged in order of mean depth (in m)

Baykal Tanganyika Crater Issyk-kul Malawi Tahoe Kivu Toba Mjøsa Superior Titicaca Ontario Michigan Great Bear Huron Great Slave Ladozhskoye Victoria Turkana Onezhskoye Erie Winnipeg Nicaragua Dangting Balkhalsh Tchad Eyre Patos Bangweolo

730 574 333 279 273 249 240 226 154 147 107 86 85 72 59 58 50 39 29 28 19 15 13 7 6 4 3 2 1

1

2

3

4

5

6

7

8

9

10

11

12

z z z z z z z z z X z z X X X z z z z z z z z z z z z z z

X z z z z z z z X z z X z z z X X z z X X X z z z z z z z

z X X X X X X z X z z z z z z z X X X X z z X z X X X z z

X z z z z X z z z X z z X X X X z z z z z z z z z z z z z

z X z X z z z z z z X X z z z z z z X X X z z z z z z z z

z z z z z z z z z z z z z z z z z z z z z z z z z X z z X

z z z z z z z z z z z z z z z z z X z z z X z z z X z z X

X z z X z z z z z z X z z z z z X z z z z z z X X z z z z

X X X z X z X X z z X z z z z z z X X z z z z z X X z z z

. z z z z z X z z z z z z z z z z z X z z z z z X X z X z

z z z z z z z z X z z z z z z z X z z X z z z z z z z z z

z z z X z z X z z z X z z z z z z X z z z z z z X z z z z

of information on the assemblages represented in the World’s large lakes, we sought a means by which to summarise and compare the character of the phytoplankton of the individual lakes. Traditionally, students of phytoplankton categorise natural assemblages by phylogenetic affinity and taxonomic subdivision. Selective evolutionary adaptations to life in major limnetic habitats, however, are manifest in common morphological and functional properties which cut across phylogenetic divisions (Reynolds, 1995). However, to adopt from the outset a set of strategic or phytosociological groups (Olrik, 1994; Reynolds, 1996) might be seen to be forcing a preconceived outcome. Instead, we have taken Hutchinson’s (1967) main (primarily taxonomic) categories of phytoplankton (below) and ascribed to these an identifying numeral. Then, from the sources of

information listed in Table 3, we scored the representation of these categories in each of the lakes as a bullet-point. This became a statement of the type of phytoplankton known to occur in each lake. By rearranging the sequence of lakes, according to the ordering devised for Tables 4–9, any qualitative patterns could then be readily observed. Twelve categories was the minimum number capable of accommodating the range of the qualitative data (Table 10). 4.1. Diatom-dominated plankton In all but one of the lakes considered, planktonic diatoms dominated the phytoplankton for at least part of the year. Open-water assemblages featuring species of Cyclotella (especially those of the Cyclotella

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Table 6 The distribution of representative phytoplankton categories 1–12 (see text and Table 10) in the database lakes arranged in order of Secchi-disc depth (in m). Insufficient information: Bangweolo, Eyre, Kivu, Toba

Tahoe Crater Great Bear Baykal Malawi Issyk-kul Superior Great Slave Tanganyika Michigan Mjøsa Balkhalsh Titicaca Erie Huron Onezhskoye Ontario Nicaragua Ladozhskoye Turkana Victoria Winnipeg Patos Tchad Dangting

24–36 # 34 # 29 5–24 13–23 13–20 10–17 4–17 12–15 9–13 4–12 0.4–12 5–10 5–9 1–8 3.6–7.5 2–6 # 5? 1.5–5 1–4.5 0.2–2.5 0.3–2 0.1–2 0.1–0.7 0.1–0.3

1

2

3

4

5

6

7

8

9

10

11

12

z z X z z z X z z X z z z z X z z z z z z z z z z

z z z X z z z X z z X z z X z X X z X z z X z z z

X X z z X X z z X z X X z z z X z X X X X z z X z

X z X X z z X X z X z z z z X z z z z z z z z z z

z z z z z X z z X z z z X X z X X z z X z z z z z

z z z z z z z z z z z z z z z z z z z z z z z X z

z z z z z z z z z z z z z z z z z z z z X X z X z

z z z X z X z z z z z X X z z z z z X z z z z z X

z X z X X z z z X z z X X z z z z z z X X z z X z

z z z z z z z z z z z X z z z z z z z X z z X X z

z z z z z z z z z z X z z z z X z z X z z z z z z

z z z z z X z z z z z X X z z z z z z z X z z z z

glomerata–Cyclotella bodanica group), Tabellaria, Aulacoseira (species of the Aulacoseira islandica– Aulacoseira subarctica group) and Urosolenia spp. are prevalent during the short growing seasons observed in the cold high-latitude examples (Great Bear, Huron, Michigan and Superior). We distinguish these by the identifier (1). In many other of the temperate lakes, Asterionella and Stephanodiscus species (especially Stephanodiscus binderanus) are generally better represented (Erie, Great Slave, Ladozhskoye, Mjøsa, Onezhskoye, Ontario and Winnipeg), which we identified as group (2). These diatoms are also in evidence in inshore or frontal (“thermal bar”) areas of Baykal (Likhoshway et al., 1996) and Michigan (Munawar and Munawar, 2000). Diatom populations tend to be greatest in deep lakes when they are thermally stratified. In Baykal, the spring diatom growth occurs while the lake is still ice-covered but, seemingly (Popovskaya, 2000), only in those years when there is a well-defined convective layer beneath the ice. According to the data of Rossolimo (1957)

this depends, in turn, on the extent of snow cover on the ice and the resultant heat-flux to the water. Among the lower latitude lakes, diatoms dominate during the cooler or windier part of the year, when mixed layers are extended to some 15–30 m. Assemblages featuring Aulacoseira granulata and, often species of Staurastrum and Closterium, dominate for periods in Kivu, Malawi, Nicaragua, Tchad and Victoria. The grouping is substantially represented during the summer in Balkhalsh, Issyk-kul Ladozhskoye, Mjøsa, Onezhskoye and Tahoe. Nitzschia spp. are the main diatom species in Crater and Tanganyika. Species of Coscinodiscus and Surirella are conspicuous in the plankton of Balkhalsh, Nicaragua and Turkana. Although not necessarily assumed to have strong mutual affinities, these diatom assemblages are referred to as group (3). 4.2. Chrysophycean plankton Hutchinson (1967) used this term in respect of the

10

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

Table 7 The distribution of representative phytoplankton categories 1–12 (see text and Table 10) in the database lakes arranged in order of reported Secchi-disc depth/mixed depth ratio (zs/zm). Insufficient information: Bangweolo, Eyre, Kivu, Toba

Dangting Victoria Winnipeg Turkana Tchad Ladozhskoye Titicaca Ontario Nicaragua Huron Tanganyika Onezhskoye Great Bear Erie Michigan Great Slave Malawi Mjøsa Superior Tahoe Issyk-kul Patos Baykal Crater Balkhalsh

0.01–0.04 0.01–0.06 0.02–0.13 0.03–0.16 0.03–0.18 0.03–0.20 0.05–0.20 0.02–0.27 Generally ,0.3? 0.02–0.32 0.05–0.35 0.13–0.38 $ 0.4 0.06–0.41 0.11–0.52 0.07–0.57 0.16–0.60 0.03–0.67 0.07–0.70 0.10–0.72 0.05–1.0 0.05–1.0 0.007–1.2 0.49–1.7 0.67–2

1

2

3

4

5

6

7

8

9

10

11

12

z z z z z z z z z X z z X z X z z z X z z z z z z

z z X z z X z X z z z X z X z X z X z z z z X z z

z X z X X X z z X z X X z z z z X X z X X z z X X

z z z z z z z z z X z z X z X X z z X X z z X z z

z z z X z z X X z z X X z X z z z z z z X z z z z

z z z z X z z z z z z z z z z z z z z z z z z z z

z X X z X z z z z z z z z z z z z z z z z z z z z

X z z z z X X z z z z z z z z z z z z z X z X z X

z X z X X z X z z z X z z z z z X z z z z z X X X

z z z X X z z z z z z z z z z z z z z z z X z z X

z z z z z X z z z z z X z z z z z X z z z z z z z

z X z z z z X z z z z z z z z z z z z z X z z z X

plankton of mountain lakes in either hemisphere where one or other or several species of Dinobryon dominated. Plankton dominated by Dinobryon spp, sometimes with species of Mallomonas and/or Uroglena have been noted in Baykal, Great Bear, Great Slave (where notably large early summer populations follow ice-melt: Pollingher, 1990), Superior and Tahoe. In addition, the group is represented in Huron and Michigan but only poorly in Erie and Ontario (Munawar and Munawar, 1986). They are accorded the identifier (4). Note that although Chrysochromulina and Ochromonas are widespread in the plankton of the temperate examples, they are treated here as nanoplankton (q.v., below).

In fact, mucilage-bound, non-motile colonial representatives of the large Chlorophyte order, the Chlorococcales (including Sphaerocystis, Kirchneriella, Botryococcus, Dictyosphaerium), as well as of the order Tetrasporales (especially Gemellicystis, Gloeocystis and Paulschulzia) occur widely throughout the series. Oocystis- or Sphaerocystis-dominated plankton is recorded in Aralskoye, Erie, Issyk-kul, Onezhskoye, Ontario, Tanganyika, Titicaca and Turkana. We identify it as Group (5). The distinctive Botryococcus-dominated plankton, prominent at times in Bangweolo and Tchad, is separately noted as Group (6). 4.4. Eutrophic chlorophyte plankton

4.3. Oligotrophic chlorococcal plankton Green algae feature in a number of distinct associations. Hutchinson (1967) proposed the heading above to apply to the Oocystis plankton he had himself observed in large clear lakes of central Asia.

A second group of Chlorococcalean algae, generally lacking mucilage, is usually taken to be more closely associated with shallow, nutrient-rich habitats—ponds, shallow lakes, slow-flowing rivers. Typical members of this group (7), which are

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

common or achieve dominance in the large lakes considered here, are Pediastrum and Scenedesmus, encountered as significant components in Bangweolo, Tchad, Victoria and Winnipeg. Colonial representatives of the Volvocales— including the genera Eudorina and Pandorina—are not recorded as dominants in any of the current examples. The impression that this is a well-defined association of small, mildly alkaline, shallow or stratified lakes receiving high insolation levels and high nutrient fluxes is not altered by the present data. 4.5. Dinoflagellate plankton Hutchinson (1967) distinguished between oligotrophic and meso/eutrophic associations of dinoflagellates which inhabit lakes large and small. The former is centred about Peridinium willei, often considered to be an oligotrophic indicator, sometimes with Ceratium hirundinella. Both are relatively eurytrophic (i.e. occurring widely in relation to the trophic condition: Ho¨ll, 1928), although Ceratium is apparently not common among low-latitude lakes. The species recorded in Lake Victoria, Ceratium brachyceros, is thought to be endemic (Pollingher, 1990). Dominance by Peridinium is noted in Baykal, Balkhalsh, Issykkul (co-dominating with Merismopedia) and Titicaca. The identifier (8) is used for dinoflagellate plankton. 4.6. Cyanobacteria-dominated plankton The Cyanobacteria are well-represented in a wide range of lacustrine habitats, where they sometimes achieve overwhelming dominance. This gives the group a collective reputation of ubiquity and rather generalised requirements whereas, in reality, individual species require quite specific conditions to be satisfied if they are to establish themselves. The first of these is the group of Nostocalean genera which are able to fix atmospheric N when such N sources as ammonium- and nitrate-N are deficient. Anabaena is a frequent dominant in Malawi, Tanganyika, Tchad, Toba, Turkana and Victoria, and is productive during calmer summers in Baykal. Anabaena spp. are also found deep in Crater Lake. Aphanizomenon forms blooms in Ladozhskoye; Cylindrospermopsis does so in Kivu. Nodularia is a N-fixing species of brackish water and which becomes

11

Table 8 The distribution of representative phytoplankton categories 1–12 (see text and Table 10) in the database lakes grouped according to categories of base status (see text) 1

2

3

4

5

6

7

8

Group 1:Circumneutral Lakes Baykal z X z X z z z X Nicaragua z z X z z z z z Toba z z z z z z z z Tahoe z z X X z z z z Kivu z z X z z z z z Mjøsa z X X z z z z z Bangweolo z z z z z X X z Group 2:Weakly buffered, subject to pH drift Balkhalsh z z X z z z z X Superior X z z X z z z z Malawi z z X z z z z z Victoria z z X z z z X z Great Bear X z z X z z z z Ontario z X z z X z z z Great Slave z X z X z z z z Erie z X z z X z z z Winnipeg z X z z z z X z Ladozhskoye z X X z z z z X Patos z z z z z z z z Onezhskoye z X X z X z z z Crater z z X z z z z z Tchad z z X z z X X z Dangting z z z z z z z X Group 3:Alkaline Lakes Tanganyika z z X z X z z z Michigan X z z X z z z z Huron X z z X z z z z Issyk-kul z z X z X z z X Turkana z z X z X z z z Titicaca z z z z X z z X Eyre z z X z z z z z

9

10 11 12

X z z z X z z z X X z z z z

z z z z z X z

z z z z X z z

X X z z X z X z z z z z z z z z z z z z z X z z X z X X z z

z z z z z z z z z X z X z z z

X z z X z z z z z z z z z z z

X z z z z z z z X X X z z z

z z z z z z z

z z z X z X z

numerous in Balkhalsh and Titicaca. Nitrogen-fixing cyanobacteria are categorised (9). Microcystis aeruginosa and its near relatives in the Chroococcales (such as Gomphospaeria naegeliana and Worochinina; together identified as group 10) can constitute a distinct element of the phytoplankton, either alone, with, or as an alternative to, dinoflagellate-dominated canopy plankton. Microcystis is a prominent component of the phytoplankton during the summer in Balkhalsh and, during the months of more stable stratification, in Kivu and Turkana. More notoriously, Microcystis may dominate overwhelmingly the surface circulations of dielly-stratified lakes of the lower latitudes, as it appears to do in

12

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

Table 9 The distribution of representative phytoplankton categories 1–12 (see text and Table 10) in the database lakes grouped according to phosphorus content of the water (SRP: maximum reported concentration of soluble reactive phosphorus; TP: range of reported total phosphorus; both in mg P l 21). Insufficient information: Nicaragua, Tchad, Bangweolo

Turkana Patos Eyre Titicaca Baykal Balkhalsh Kivu Ladozhskoye Ontario Michigan Crater Erie Victoria Onezhskoye Tanganyika Malawi Mjøsa Great Slave Winnipeg Tahoe Dangting Huron Issyk kul Superior Toba Great Bear

SRP

TP

1

2

3

4

5

6

7

8

9

10

11

12

# 786

1800–2400 # 1000 # 340 39–331

z z z z z z z z z X z z z z z z z z z z z X z X z X

z z z z X z z X X z z X z X z z X X X z z z z z z z

X z X z z X X X z z X z X X X X X z z X z z X z z z

z z z z X z z z z X z z z z z z z X z X z X z X z X

X z z X z z z z X z z X z X X z z z z z z z X z z z

z z z z z z z z z z z z z z z z z z z z z z z z z z

z z z z z z z z z z z z X z z z z z X z z z z z z z

z z z X X X z X z z z z z z z z z z z z X z X z z z

X z z X X X X z z z X z X z X X z z z z z z z z X z

X X z z z X X z z z z z z z z z z z z z z z z z z z

z z z z z z z X z z z z z X z z X z z z z z z z z z

z z z X z X X z z z z z X z z z z z z z z z X z z z

250–910 # 23 10–60

# 20 # 20 # 18 #6

#5 #3

61 # 55 13–40 # 30 10–30 9–25 # 12 5–10 4–10 1–10 4–8 3–8 2–8 #6 #5 4–5 (locally 21) 2–4 2–3 (locally 10) 0.3–0.6 # 0.1

Patos (Yunes et al., 1998), perhaps also in Tchad (Sikes, 1972) and, at times, we suspect, in Bangweolo. Merismopedia dominance is generally thought to be confined to mesotrophic but often mildly acidic lakes. Its occurrence in Issyk-kul (pH range 8.5–8.9) is not entirely consistent with this view. The solitary filamentous Oscillatoriales, chiefly represented by species of Lyngbya, Phormidium, Pseudanabaena and many formerly ascribed to the genus Oscillatoria (Planktothrix, Limnothrix, Tychonema, a.o.), are no less effective in eventually dominating the plankton of turbid, well-mixed environments. These occur typically in exposed, shallow and often enriched lakes, where species such as Planktothrix agardhii, Limnothrix redekei and Pseudanabaena limnetica are strongly selected. This group (11) is not-well represented in the current data set, except as co-dominants with diatoms in

Ladozhskoye, Mjøsa and Onezhskoye. However, what Reynolds (1996) considered its low-latitude analogue (the Spirulina–Arthrospira–Lyngbya group, 12) is conspicuous in Balkhalsh, Issyk-kul, Kivu, Titicaca and Victoria.

4.7. Cryptomonad plankton Cryptomonads are ubiquitous among freshwaters. Although commonly recorded throughout the present data set, they have been rarely noted as dominant. They have been described as ‘important’ in Mjøsa (Holtan, 1978) and they are noted as being common in the summer plankton of Ontario (Munawar and Munawar, 1986). Deep-water maxima of Cryptomonas occur in Crater Lake (Debacon and McIntyre, 1991). It is likely that the group has been underrecorded in the current dataset.

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

13

Table 10 Summary of qualitative affinities of types of phytoplankton with attributes of large lakes Positive affinities

Negative affinities

No correlation

1. Cyclotella–Rhizosolenia plankton

High latitude

Warm lakes TP .30 mg l 21 turbid lakes

Alkalinity zs =zm

2. Asterionella–Stephanodiscus plankton

Dimictic lakes

Low latitude TP , 5 mg l 21 high alkalinity

Clarity zs =zm

High latitude

P clarity alkalinity latitude zs =zm

Low latitude

P alkalinity

Shallow lakes (,20 m) low alkalinity

P clarity latitude zs =zm

Turbid lakes (,5 m) frequent mixing?

P alkalinity latitude

3. A.granulata (Nitzschia, Surirella) plankton 4. Dinobryon/Uroglena plankton

Max. zs =zm . 0:3 clarity . 8 m

5. Sphaerocystis/Oocystis plankton 6. Botryococcus plankton

Shallow polymictic lakes

7. Pediastrum plankton

Max zs =zm , 0:2

8. Dinoflagellate plankton

min zs =zm . 0:2

9. Nostocalean plankton

P clarity alkalinity latitude zs =zm

10. Microcystis plankton

TP . 30 mg l21

11. Planktothrix plankton

High latitude

High latitude

Clarity alkalinity zs =zm

12. Spirulina/Lyngbya

High latitude

4.8. Nanoplankton

(as under clear ice) to provide the best opportunities to the potentially fast-growing, high-productivity organisms of the nanoplankton. Poor representation in the records from Tchad and Nicaragua is not unexpected but elsewhere, under-recording is probably to blame.

Nanoplankton, defined by Sieburth et al. (1978) to include planktonic algae in the size range 2–20 mm, is not specifically delimited in many of the datasets, but it is clear from the recorded presence of the smaller algal genera (Chlorella, Ankistrodesmus, Koliella, Chlamydomonas, Rhodomonas, Chrysochromulina, Ochromonas, Bicoeca, Chromulina, a.o.) that the category is probably well-represented in the lakes considered here. It features in all the North American lakes, in Mjøsa, Kivu and Tanganyika. So far as it is possible to judge, the most productive periods for nanoplankton are in newly stratified conditions, when mixed depth shrinks to a few meters or less

4.9. Picoplankton Chroococcoid cyanobacteria, such as Synechococcus and Synechocystis spp., and tiny chlorophytes, like Chloromonas and the small-celled Chlorella minutissima (individuals in the size range, 0.2– 2 mm: Sieburth et al., 1978), constitute the picoplankton. Specific descriptions of the picoplanktonic

14

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

association have been given for Ontario (Caron et al., 1985; Munawar and Munawar, 1986; Pick and Caron, 1987), Superior (Munawar and Fahnenstiel, 1982; Fahnenstiel et al., 1986; Munawar et al., 1987) and Baykal ‘in low productivity years’ (Popovskaya, 2000). Bearing in mind the widespread distribution of picoplankton among large, clear, often oligotrophic lakes (Pick, 1991) and seas (Stockner and Antia, 1986), it seems to be only a matter of time before the prevalence of picoplankton in many more of the world’s great lakes is established.

5. Correlations among phytoplankton distributions and limnological properties of large lakes With the exception of the cryptomonad, nanoplanktonic and picoplanktonic categories, the distribution of the groups of phytoplankton recognised among the lakes of the dataset is summarised in Table 10. It is interesting that this qualitative approach produces so relatively few consistencies. It is surely interesting that latitude was the best predictor of phytoplankton representation, especially in delimiting the ranges of (say) Aulacoseira plankton from those of Cyclotella or (again say) those of Dinobryon from those of Spirulina. No direct effect could be proposed:

the phenomenon is mediated by water temperature, day length and light relations, perhaps even the availability of carbon dioxide. The pH/alkalinity categories produced no compelling correlations. Elsewhere, the distributions support some of the prejudices carried from smaller lakes. The Cyclotella group (1), the chrysophyte assemblage (4) and the Sphaerocystis group (5) generally occur among more oligotrophic lakes when light is relatively abundant, while the relative tolerance of diatom- (2, 3) and Planktothrix-dominated (11) plankton of the lowaverage insolation of deep mixed layers is well-established (Reynolds 1986, 1989, 1995). Some alternation in relation to mixing intensity and relative light availability should be expected to influence the success of recruitment during the year and, in turn, changes in species composition. When near-surface stratification raises the lightlimited biomass capacity, the constraint moves sooner or later to the flux of assimilable resources. The experience in small lakes is that fast-growing species (nanoplankton and small microplankton) expand but that, sooner or later, larger, slower-growing species (of dinoflagellate and colonial cyanobacteria) may replace them, provided that some resources continue to be available. In this context, the ability of Microcystis to dominate in the warmer, low-latitude lakes at

Fig. 1. Matrices for the calculation of phytoplankton carrying capacity of lakes in terms of light energy and nutrient resources. (a) Matrix to show the distribution of contours of maximum supportable phytoplankton chlorophyll content in terms of mixed water-column depth (hm, in m) and the combined coefficient of vertical light attenuation due to pure water (e W) and any colour and particulate material (e P); (b) maximum chlorophyll yield for the phosphorus available. From relationships discussed in Reynolds (1992).

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

15

Table 11 Annual distribution and scale of biomass peaks (in mg l 21 fresh mass). Insufficient information: Balkhalsh, Bangweolo, Dangting, Eyre, Nicaragua, Toba Cold monomictic lakes Great Bear Dimictic lakes Superior Mjøsa Baykal Michgan Huron Erie(WestBasin) Ontario Ladozhskoye Onezhskoye Great Slave Winnipeg Warm monomictic lakes Issyk-kul Victoria Turkana Tahoe Titicaca Meromictic lakes Tanganyika Malawi Crater Kivu Polymictic lakes Patos Tchad

Diacmic

VI (,0.06); IX (#0.09)

Monacmic Monacmic Diacmic Diacmic Diacmic Diacmic Diacmic Diacmic Diacmic ? Polyacmic?

VIII–X (0.4–0.6) VII–VIII (#2.5) IV–V (0.1–8.0); VIII–IX (#1) VI (#0.9); VIII–IX (#0.5) VI (,1.2); VII (,0.8) IV (10–12); VIII (,8) III–IV (2–3); VIII–IX (#8) V (0.2–1.0); VIII–IX (#2) V(#1), VIII (#2) VI (#1) “Late summer” peak #10

Diacmic Monacmic Monacmic ^ Monacmic ^ Monacmic

V, VIII V–VI (#5) subsidiary peaks VIII–IX, XII) XI–XII (#5) minimum, V–VII VI–IX (0.4) V–VI minimum X–XI

^ Monacmic ^ Monacmic ^ Monacmic ^ Monacmic

Maximum (,0.9) during period of deep mixing (VIII–X) Maximum (,0.3) VI–IX Maximum (,0.2) V–VI Maximum (,2.0) VI–IX

^ Monacmic ^ Monacmic

“Late summer” maximum (#9) Maximum (#0.2) V–X

the times of maximum stability, especially in those of higher (.30 mg l 21) TP content, accords with the consensus view from studies on smaller lakes (Pearson et al., 1990).

6. Biomass supportive capacities of large lakes The database gives some indication of the maximal biomass of open-water phytoplankton standing crops (variously as chlorophyll concentration, biovolume, dry or fresh mass) in many of the lakes, as well as a perspective of the seasonal variability of its abundance. Table 11 presents a summary of the information we have abstracted. Biomass is expressed on a common scale of fresh mass, assuming a density of 1000 kg m 23 and adopting the conversion factors derived in Reynolds (1984). Thus, 1 mg chlorophyll a is equivalent to 50 mg carbon is equivalent to

0.22 mm 3 of living protoplasm with a mass of 0.22 mg. It can be seen that, in the majority of instances, phytoplankton biomass is normally very low in the well-mixed open waters of the world’s great lakes. Comparing Table 11 with Table 3 it is also apparent that the peaks are attained when the water column is stratified (including under ice in the case of lakes with diacmic cycles, as in Fig. 2b; thus, in Superior and Mjøsa, where winter ice cover is relatively brief and less extensive, there is almost no spring bloom). In the low-latitude lakes, the annual fluctuations in biomass are related to the cycle of mixed layer deepening and truncation. This behaviour is generally understood from studies on the biomass-carrying capacities of much smaller lakes. Supportive capacity is generally defined by basic limnological properties of the environment, including its temperature (u ), density structure (especially as it affects mixed depth, zm), light

16

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

Fig. 2. Stylised phytoplankton-chlorophyll carrying-capacity curves in respect to the annual fluctuations of light income, chl(I p), and nutrient, chl(K), in (a) a large monmictic temperate lake (such as Superior), (b) a large dimictic temperate lake (Baykal) and (c) a tropical meromictic lake (Tanganyika). The actual biomass supported has to be within the envelopes simultaneously enclosed by both capacities.

attenuation (e l ), hydraulic renewal (tw) and external nutrient loads (L). From these basic data, some further properties of the underwater environment can be derived. Integrated insolation (I p), aggregated photoP periodicity ( tp) and the concentrations of available nutrient ([K ]) may be re-calculated in terms of the plankton chlorophyll that might be supported. The relevant equations were assembled by Reynolds (1992) and are, incidentally, written into the PACGAP software ( qUnited Kingdom Environment Agency). Assessment of the changing supportive capacities of each resource reveals the sensitivity of the biological respondents to seasonal variations in irradiance and nutrient income, and in the way that this capacity is

diluted over a mixed layer. Fig. 1a is a matrix for relating maximum phytoplankton biomass for a given mixed layer depth and light extinction. Fig. 1b is the regression of chlorophyll concentration yield against the concentration of available P. The hypothetical plots in Fig. 2 compare nutrient- and energy-capacities lakes through time: they provide a very simple conceptual model as to how phytoplankton biomass is regulated in deep lakes: light is the overwhelming constraint for very long periods; density stratification provides a much-enhanced light environment in the near-surface layer, the supportive capacity of which quickly switches to the nutrient resource. The extent to which that capacity is filled is largely a function of the time available for the phytoplankton present to grow and increase before the opportunity is lost. It is worth observing that deep mixing of hitherto stratified water also affects the resource–supply function as greater circulation entrains from greater depth water with a higher nutrient content. In Tanganyika, for instance, the onset of mixing simultaneously raise the resource capacity and depresses the energy capacity. For a time biomass production is greatly stimulated (to achieve the annual biomass peak) until the light-determined capacity is exerted. On restratification, the improving light conditions soon overtake the nutrient capacity once again but not before the biomass has had a chance to respond to the second opportunity (Talling, 1986).

7. Trophic linkages Attention was given to the possible importance of grazing and the transport of materials through planktonic linkages. At least qualitative data with respect to the zooplankton are available for most of the lakes considered although the extent to which the rotifers and ciliates are treated is quite variable. Good information is available on the ciliates of Ladozhskoye, Onezhskoye and the Laurentian lakes. The planktonic rotifers are described in these studies and also for Baykal, Tahoe and Victoria. The crustacea are sometimes listed with biomasses or, if not, as a species list only. Table 12 lists characteristic and conspicuous members of the crustacean zooplankton, in what we believe approximates to a

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

17

Table 12 Characteristic zooplankton and fish communities in Great Lakes. Insufficient information: Crater, Mjøsa, Patos

Great Bear Great Slave Onezhskoye Ladozhskoye Baykal Winnipeg Superior Balkhalsh Huron Michigan Ontario Issyk-kul Erie Tahoe Dangting Tchad Nicaragua Turkana Toba Victoria Kivu Tanganyika Bangweolo Malawi Titicaca Eyre

Crustaceans

Predominant fish taxa

Diaptomus, Limnocalanus Limnocalanus, Diaptomus Limnocalanus, Eudiaptomus Limnocalanus, Eudiaptomus Epischura, Macrohectopus, etc. Diaptomids, Ceriodaphnia Diaptomus,Limnocalanus Arctodiaptomus, Daphnia Diaptomus, Bosmina, Holopedium Diaptomus, Limnocalanus Eurytemora, Diaptomus, Limnocalanus Arctodiaptomus Bosmina,Cyclopoids Leptodiaptomus, Daphnia Epischura, Diaptomus, Bosmina

Salvelinus, Coregonus

Diaphanosoma, Daphnia, Tropodiaptomus Mesocyclops, Diaptomus Mesocyclops, Thermocyclops Cyclops Daphnia, Chydorus, Diaptomus Copepods; Cladocera in VI/VII Cyclops, Diaptomus Mesocyclops, Diaphanosoma Bockella, Microcyclops Moina

ranking in importance. As with the phytoplankton, the distribution shows some affinity with latitude and the listing of lakes follows that sequence. Limnocalanus is one genus common at high latitudes which becomes less so towards the equator. Cyclopoids seem more important at low latitudes. Only Victoria and Eyre are not dominated by copepods. In most examples, the dominant forms are calanoids, while cladocerans such as Daphnia and Bosmina are rather rarer. This is consistent with the essentially oligotrophic nature of the lakes and the sparsity of algal foods: mostly, the phytoplankton is far too dilute to sustain obligate filter-feeders like Daphnia. The critical range is between 0.1 and 0.4 mg C l 21 (Reynolds, 1984: or ,1.5 mg fresh-weight l 21). It is interesting that the seasonal expansion of cladocera noted in Kivu

Coregonus, Osmerus, Lucioperca Coregonus, Osmerus, Perca Comephros, Procottus, Asprocottus Stizostedion, Coregonus, Perca Oncorhynchus, Salmo Perca, Schizothorax Oncorhynchus, Salmo, Alosa Alosa, Cyprinus, Onchorhynchus, Perca Oncorhynchus, Salmo, Alosa, Coregonus Leuciscus, Schizothorax Stizostedion, Perca, Osmerus Oncorhynchus, Salmo Coila, Cyprinids Schilbe, Citharinus, Labeo Silurids, Cichlids Alestes, Lates, Hydrocynus Tilapia, Aplocheilus, Lebistes Lates, Tilapia, Haplchromis, Alestes Cyprinids, Cichlids, Clariids Stolothrissa, Limnthrissa, Laprichthys Tilapia Varicorhinus, Labeo, Osparidium Engraulicypris, Diplotaxodon Orestias, Trichomycterus, Salmo Neasilurus, Craterocephalus

(Serruya and Pollingher, 1983) responds to the seasonal increase in food stimulated by changes in stratification. Some of the descriptions list the species of rotifers (the genera Keratella, Kellicotia and Polyarthra are very cosmopolitan in distribution; Notholca is common through the Laurentian lakes; Synchaeta is prominent in Baykal). Allan et al. (1994) provide lists detailing the planktonic ciliates. Their role (inter alia) in closing the microbial loop between phytoplankton carbon fixation and excretion, bacteria and their nanoflagellate consumers, on the one hand, and crustacean zooplankton, on the other, gives circumstantial support for its operation in these lakes. A selective feeding of calanoid genera of zooplankton permits the co-existence of smaller, ungrazed organisms,

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C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

including all the components of the microbial loop, whereas intense, non-selective filter feeding removes them. Our database records the main genera of pelagic fish present in the lakes. The original intention was to detect the existence of trophic linkages relevant to the structuring of the planktonic communities. The summary in Table 12 shows the high incidence of salmonid and coregonid populations at higher latitudes but the functional complexities in individual tropical lakes, discussed at length by Lowe-McConnell (1975), Ribbink (1994) and others, put generalisations beyond the scope of this article. The extent to which natural and anthropogenically influenced fluctuations in the growth and recruitment of primarily planktivorous and ultimately piscivorous fish populations affect the mass maintained at lower trophic levels in temperate lakes continues to be vigourously debated. We suspect that such relationships are yet more obscure at low latitudes. Further research into the trophic networks of great lakes remains a top priority.

8. General deductions The general impression to be gained from this brief overview is that the phytoplankton of large lakes, except the very shallow examples, is characteristically sparse and usually quite oligotrophic in character. This may have been broadly anticipated to be attributable to a certain poverty of plant nutrients. Certainly, the hydraulic loads and the concentrations of nutrients dissolved therein determine that retention times are protracted and external loading rates are trivial. In this sense, we suppose that great lakes are not just large small lakes but, rather, that they function more like the open sea. Their internal exchanges are likely to be dominated by internal mechanisms but such recycles must occur almost wholly within the mixed water column: among the lakes selected on the criteria of volume or depth (Table 1), the bottom is so remote from most of the water column that sediment–water exchanges probably do not figure in nutrient budgets either. Microbial processes and feedbacks in the top 100–200 m are largely responsible for maintaining even the relatively low fertility of these lakes. Unimpeded mixing of the upper layers of very large lakes involves a much greater depth of

water than is frequently the case in small lakes and so contributes to a more efficient turnover of resources within the water. A similar conclusion was reached by Guildford et al. (1994), whose comparative studies of the phytoplankton through a series of Canadian lakes of increasing size showed that phytoplankton in large lakes turn out to be less nutrient-deficient than those of small lakes. However, also like the open seas and oceans, there are long periods of deep mixing through which production is severely constrained by the poverty of available light. We suppose there to be insufficient biomass-specific autotrophy to come up even to the limits of the nutrient resources available. Primary production and expansion of the biomass of primary producers is confined to periods of restricted mixing: these are periods of net heat gain and weakened dissipation in low-latitude lakes or after very long periods of heat gain in temperate lakes and, indeed, of heat loss leading to ice cover in the high latitudes. These growth opportunities are met by compensatory loss of resources so, in general, one biomass constraint quickly replaces the other and the oligotrophic character is not overcome. Oceanographers attach great significance to ‘new production’, being that assembled from ‘new’ (as opposed to internally recycled) limiting nutrient. The upwelling areas of the seas, where relatively nutrient-rich deep-water circulations are forced to the surface, have minor analogues among very large lakes, most famously in Baykal and Tanganyika (Tilzer and Bossard, 1992); indeed, renewal of deep waters is an important influence on the productivity in most large lakes. As it is, open pelagic systems are characterised by a scarcity of new nutrient which internal re-use conserves as far as possible. With respect to the attributes of the phytoplankton of great lakes, organisms benefit from being resistant to settling, either by being very small and wellentrained or by being large and motile (Legendre and Le Fe`vre, 1989). With scarce resources, to escape direct consumption (either by being much smaller or much larger than the preferred size of the main consumers) is also a valuable pre-adaptation. In relatively well mixed conditions imposing moderate to severe light limitation, the most appropriate adaptations are those of a good light-harvesting antenna and an adaptive capability to increase the cell-specific

C.S. Reynolds et al. / Aquatic Ecosystem Health and Management 3 (2000) 1–21

photosynthetic capacity, by raising the levels of chlorophyll and accessory pigments. Depending upon the frequency of alternation between energy- and resource-limitation, the opportunities afforded to phytoplankton by the structural organisation of the truly pelagic system are alternately weighted towards a composition featuring diatoms and Oscillatoria-like Cyanobacteria (mixed conditions) and to one eventually assembled round large dinoflagellates, colonial chrysophytes or cyanobacteria.

Acknowledgements We are grateful to the sponsors of the Symposium on the Great Lakes of the World for the challenge to make this modest compilation of data on the phytoplankton. It would not have been possible without access to the resources of the Library of the Freshwater Biological Association. Most of the literature searching was undertaken by S.N.R., during a placement supported by the Cumbria Training and Enterprise Council. Grateful appreciation is expressed to both bodies.

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