Freshwater Biology (2000) 45, 105–109
Plankton population dynamics: food web interactions and abiotic constraints KARL O. ROTHHAUPT Limnologisches Institut, Universita¨t Konstanz, D-78457 Konstanz, Germany
SUMMARY 1. In this introduction, I try to follow some developments in plankton ecology, how they have led to current research topics, and how the contributions in this issue of Freshwater Biology are related to these fields of research. 2. Due to several favourable features, such as small size, short generation time and a relatively homogeneous habitat, planktonic organisms remain ideal subjects for theoretical and experimental population ecology. 3. Important current research topics involve: (1) the control of plankton communities by external abiotic factors; (2) bottom-up (limitation by resources) and top-down (control by predators) effects in the food web; (3) the importance of dormant resting stages and benthic – pelagic coupling in plankton dynamics; (4) costs and benefits of the mixotrophic strategy, i.e. the ability to combine a phototrophic and a phagotrophic mode of nutrition. Keywords: abiotic factors, community organization, food web, mixotrophic protists, model, plankton, population ecology, predation, resource limitation
Introduction The papers in this issue of Freshwater Biology deal with classic issues of general population ecology and community ecology. They treat topics such as control by the physical and chemical environment, resource use and top-down control in the food web and life history strategies including diapause and benthic stages. All have in common the use of plankton as model organisms and as a model community. Due to their small size, short generation time, often high abundance and relatively homogeneous distribution, plankton organisms facilitate field studies and experimental studies at various scales, ranging from microcosms in the laboratory to mesocosms in lakes. Above this, plankton is of central importance in the pelagic food web of lakes and oceans and, for that reason, planktology has been a core discipline in limnology and biological oceanography since Victor Hensen’s pioneering studies in the late 19th century (Sommer, 1996; Smetacek,
Correspondence: Karl O. Rothhaupt. E-mail:
[email protected] © 2000 Blackwell Science Ltd
1999). Because of the many similarities between freshwater and marine plankton communities, this issue of Freshwater Biology also includes some marine studies. Owing to the phase boundaries to the lithosphere and the atmosphere, it is obvious to regard lakes, and the biotic communities they harbour, as more or less isolated entities. It was probably on account of this feature that Forbes (1887) wrote his famous essay ‘The Lake as a Microcosm’. Forbes was greatly influenced by Darwinian biology and he envisaged the biotic community of the lake as consisting of interacting individuals and populations, with the ‘balance of nature’ (a commonly accepted notion by natural historians in the 19th century) arising from Darwinian struggle. Although this ‘balance of nature’ is not a commonly held view today, it is the Darwinian focus on adaptations of individuals and mechanisms acting on populations and communities which is the common theme of the contributions in this volume. It is the classical domain of mathematical and experimental population biology and this approach has been successfully adopted in plankton ecology (Sommer, 1989). 105
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In population and community ecology, mathematical models can be helpful to engender testable hypotheses which stimulate field studies and experimental work. The paper by Scheffer & Rinaldi (2000) demonstrates very nicely how relatively simple models can be used to obtain testable predictions of patterns in food webs. The contribution by Malchow (2000) considers the emergence of spatio-temporal patterns in models of plankton dynamics and Mehner (2000) uses a simulation approach to explore the influence of spring water warming on a fish– zooplankton interaction. Today, it is commonly accepted that, within the physical constraints of, for example, mixing, stratification and light limitation (Reynolds, 1997), plankton communities are structured by the simultaneous impact of bottom-up (limitation by resources) and topdown (control by predators) effects. For the classic primary producer – grazer food chain, this combination of physical control and trophic effects in both directions found its expression in the PEG model of plankton succession (Sommer et al., 1986), which explains the seasonal sequence of plankton species in lakes by taking the underlying mechanisms explicitly into account. George (2000) explores the influence of the physical environment on plankton dynamics by looking at the impact of the weather on the long-term dynamics of zooplankton species. Bottom-up aspects are in the focus of the contribution by Jeppesen et al. (2000), who compare trophic structure and species richness along a phosphorus gradient in Danish lakes. The understanding of the influence of resource supply, a typical bottom-up effect, on the taxonomic composition of the plankton (at first the phytoplankton) was decisively advanced by the Tilman (1977) chemostat competition experiments with the diatoms Asterionella formosa Hassall and Cyclotella meneghiniana Ku¨tzing and his development of the ‘mechanistic resource competition theory’ (Tilman, 1982). The nonsubstitutable nature of mineral nutrients for phytoplankton (‘essential nutrients’ in Tilman’s terminology) led to the conclusion that supply ratios of nutrients (e.g. Si:P or N:P), not the absolute concentrations, determine the taxonomic outcome of competition. This approach was adopted by others and led to the identification of taxonomic and sizerelated trends among planktonic algae, depending on the nutrient regime (summarized by Sommer, 1989).
Light as a limiting resource for phytoplankton differs from mineral nutrients because it forms a gradient in the water column. However, theoretical and experimental progress has recently been made in incorporating light into the competition theory of phytoplankton (Huisman et al., 1999). Mechanistic resource competition theory (Tilman, 1982) has usually assumed that, under equilibrium conditions, as many species can coexist as there are different limiting resources. The non-match of only a few limiting factors (i.e. light, N, P, Si, some trace nutrients) and the observed high numbers of cooccurring phytoplankton species (usually several dozens) is an apparent contradiction, which Hutchinson (1961) termed the ‘paradox of the plankton’. It was Hutchinson’s idea that the paradox may be resolved by non-equilibrium conditions. The ‘intermediate disturbance hypothesis’ (Connell, 1978), originally developed with tropical rainforests and coral reefs in mind, was successfully applied to explain phytoplankton diversity in laboratory microcosms (Gaedeke & Sommer, 1986), lake enclosures (Flo¨der & Sommer, 1999) and a field study of lakes (Sommer, 1993). In accordance with this hypothesis, diversity has been found to be maximal when external disturbance events, such as weather-induced mixing in lakes, revert or interrupt the sequence of competition at time scales of about two to three generation times of the relevant organisms. A recent simulation study suggests that diversityenhancing non-equilibrium conditions may also arise from ‘self generated disturbances’ due to complex dynamics in the phytoplankton community (Huisman & Weissing, 1999). Hence, the assumption existing hitherto, that in the absence of external disturbances the number of limiting resources corresponds to the number of coexisting species, may not always hold true. The paper by Scheuring et al. (2000) presents an alternative theoretical attempt to explain the coexistence of several phytoplankton species without external disturbances, by considering the effects of fine-scale hydrodynamic patterns. Whereas mineral nutrients and light are evidently essential (non-substitutable) resources for the phytoplankton, it is difficult to identify non-substitutable resources for the zooplankton. Different food items (e.g. different food algae) usually have ‘package character’ and constitute substitutable resources. Hence, resource competition of the zooplankton cannot be © 2000 Blackwell Science Ltd, Freshwater Biology, 45, 105 –109
Plankton population dynamics 107 treated and predicted in the same (successful) way as resource competition of the phytoplankton. Rothhaupt (1988) was able to apply the Tilman (1982) mechanistic resource competition theory to laboratory experiments with two the rotifers Brachionus rubens Ehrenberg and Brachionus calyciflorus Pallas; although this was more or less an ‘academic exercise’ with little relevance and applicability to the natural situation. The identification of non-substitutable (essential) food constituents for the zooplankton may help to improve our understanding of resource competition of the zooplankton. The contributions by Boersma & Stelzer (2000) and von Elert & Stampfl (2000) examine certain highly unsaturated fatty acids as possible essential food constituents for zooplankton. Besides the population-oriented view, there is a second, biogeochemically oriented, view of ecology which considers processes like cycling of matter or production and categories like trophic levels or biomass, usually paying little attention to variations in constituent species and their underlying dynamics. A recent stoichiometric attempt seeks to blend both positions, the population approach and the biogeochemical approach, again with a strong impetus from plankton ecology (Sterner, Elser & Hessen, 1992). Ecological stoichiometry emanated from the observation that the elemental contents (e.g. C:P or N:P ratios) of planktonic primary producers depend on the state of limitation and vary widely, even within species, whereas the elemental contents of planktonic consumers vary little within single species, but show typical patterns between taxa. This has bearings on food quality (i.e. the stoichiometric suitability of the food) for consumers, resource competition between consumers, but also on recycling patterns of mineral nutrients by consumers and, consequently, possible shifts in N- and P-limitation of whole plankton communities (Elser et al., 1988). The contribution by Hessen & Alstad (2000) considers the requirement of Daphnia for calcium in its food as a possible stoichiometric food quality criterion. Dormant (benthic) resting stages can be decisive elements in life histories and in the population biology of plankton organisms. While this is obviously the case for inhabitants of temporary waters, it can also apply to inhabitants of permanent lakes, as has been shown for phytoplankton (Hansson, 1996), zooplankton (De Stasio, 1990) and protozoans © 2000 Blackwell Science Ltd, Freshwater Biology, 45, 105 – 109
(Mu¨ller & Wu¨nsch, 1999). A recent study suggested the competitive advantage of algae with the capability for recruiting from the benthos (Hansson, 1996). Hairston, Hansen & Schaffner (2000) explore the effect of diapause emergence on the seasonal dynamics of a zooplankton assemblage and Garstecki et al. (in press) present a study on the benthic–pelagic exchange of heterotrophic protists in a shallow estuary. About 15–20 years ago, the traditional view of the role of bacteria in plankton communities had to be modified (Azam et al., 1983). New techniques revealed that heterotrophic bacteria in the plankton were much more abundant and productive than previously thought. Moreover, it became clear that bacteria are often not remineralizers of mineral nutrients but, rather compete with phytoplankton for the uptake of dissolved mineral nutrients (Rothhaupt & Gu¨de, 1992). When the phagotrophic capacities of some phototrophs, already described by microscopists in the early 20th century, were re-discovered (Bird & Kalff, 1986), it eventually became clear that this may be an efficient strategy of ‘eating one’s competitor’ (Thingstad et al., 1996). Indeed, mixotrophs, i.e. organisms that are able to combine a phototrophic and a phagotrophic mode of nutrition, often dominate oligotrophic systems. Due to their capability to utilize alternative carbon- and mineralnutrient sources, they are able to co-exist with obligately phototrophic and phagotrophic competitors (Rothhaupt, 1996). The contribution by Jones (2000) gives an overview of mixotrophy in planktonic protists and the study by Dolan & Pe´rez (2000) explores the costs and benefits of mixotrophy in marine oligotrich ciliates. The papers in this special issue of Freshwater Biology illustrate that plankton continues to be an ideal model to study the classic issues of population and community ecology. This applies to the traditional grazing food chain, but also to the microbial food web, which is largely based on bacterial production. As new molecular techniques increasingly permit the investigation of the taxonomic composition of microbial communities (Pernthaler et al., 1997), we will increasingly be able to study the mechanisms affecting the organization of the microbial community and how it interacts with the grazing food chain (Ju¨rgens, 1995; Ju¨rgens, Arndt & Rothhaupt 1994).
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Acknowledgments This special issue of Freshwater Biology is the result of a workshop, held in Konstanz in November, 1998, that was financed by the European Science Foundation (ESF) Programme in Population Biology. Additional financial support was given by the Special Collaborative Programme (SFB 248) ‘Cycling of matter in Lake Constance’.
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