Symposium 2: The Theory of Ecology
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1 Symposium 2: The Theory of Ecology The recent ESA meeting in Milwaukee focused on linking research and education, but ecological theory was a pervasive sub-theme. Lord Robert May inaugurated this sub-theme in his opening plenary lecture, Ecological science and tomorrow s world. He eloquently and humorously demonstrated that theory has repeatedly provided a necessary framework to tackle ecological problems and challenges. The room was packed perhaps more to hear May than because of his subject and his was an effective introduction to the prominence of theory in ecological research and policy. Closely following May s presentation, Sam Scheiner and Mike Willig gathered seven ecologists from across the discipline to present this symposium on a general theory of ecology. The audience was large, energetic, and ready for discussion and debate. What is a scientific theory? Many of us learned that a theory is a system of ideas or statements explaining something, esp. one based on general principles independent of the things to be explained; a hypothesis that has been confirmed or established by observation or experiment and is accepted as accounting for known facts (Brown [Oxford English Dictionary] 1993:3274). Among biologists, this definition has its best example in the theory of evolution by means of natural selection (Darwin 1859). Scheiner and Willig take a different view of theory. In his introduction, Scheiner considered it a misapprehension to think of theory as a unified explanation for observed phenomena. Rather, theory consists of a nested hierarchical framework connecting broad principles to specific models. A general theory is comprised of a scientific domain and fundamental principles. Constituent theories and specific models round out the hierarchy. In ecology, the scientific domain is spatial and temporal patterns of distribution and abundance. Eight fundamental principles attend this domain: organisms are distributed heterogeneously in space and time all organisms interact with their biotic and abiotic environments the distribution of organisms and their interactions are susceptible to contingency environmental conditions are heterogeneous in space and time resources are finite and heterogeneous in space and time January
2 birth and death rates result from interactions with abiotic, biotic environments ecological properties of populations are the consequence of evolution individual variation predominates Scheiner s definition of a theory was controversial. What predictions arise from this general theory? Should a theory make predictions? What new understanding is gained from the eight underlying principles? Does the general theory have utility apart from its constituent theories? Scheiner and Willig assert that the role of theory is to make assumptions and basic principles explicit and to provide a framework for component constituent theories and models, but not to provide explanations, predictions, or to link cause and effect. Within this context, the six ensuing presentations were diverse. Two addressed long-held constituent theories (niche theory, succession disturbance theory); two focused on specific models (predator prey; species diversity), and two ambitiously proposed new constituent theories (one for Ecosystems and one for Global Change). A Theory of Ecosystems Ecology By addressing energy and matter exchanged among individuals, populations, communities and the environment, ecosystem ecology embraces all levels of ecological organization. Indy Burke and Bill Lauenroth presented a new, constituent theory of Ecosystems Ecology based in part on the separate theories of ecosystems energetics and organismal stoichiometry championed by Reiners (1986). The domain of their theory is the exchange of matter and energy; they add disturbance and evolution to Reiners ideas to develop a comprehensive understanding of spatial and temporal patterns of Net Ecosystem Production, or NEP. This fundamental attribute drives trophic dynamics, elemental cycling, and the distribution of key chemical and physical conditions. Burke and Laurenroth propose that NEP responds to and controls patterns of oxidation, temperature, ultraviolet radiation, and the distribution of elements. Ultimately, it constrains the evolution of metabolic pathways, and these constraints further affect rates of NEP in a tight feedback. Changes in NEP occur because controls over autotrophic and heterotrophic components differ. In Fig. 1, conditions favoring autotrophy (increases in water, light and nutrients), will cause NEP to increase (the top, dashed trajectory). This trajectory characterizes much of the earth s history, during which atmospheric oxygen has accumulated, carbon dioxide has declined, and global temperatures have also declined. Conversely, when oxygen and temperature increase, NEP becomes negative (Fig. 1, lower, solid trajectory). Disturbances to the spatial and temporal distribution of NEP will alter fundamental ecosystem characteristics both regionally and globally. This theory predicts that ecosystems exhibiting long turnover times will be resistant to disturbance. In contrast, ecosystems and components with short turnover times will exhibit resilience. By incorporating evolutionary dynamics, Burke and Lauenroth extend their theory to predict that ecosystems subjected to perturbations that encompass the evolutionary history of the dominant organisms will show resistance or resilience; ecosystems subjected to perturbations outside the dominant organisms evolutionary histories will respond through instability, alternative states, or regime shifts. 110 Bulletin of the Ecological Society of America
3 The Burke-Lauenroth Theory of Ecosystem Ecology posits that net ecosystem production both responds to and controls all features of environment; that NEP is closely linked with the evolution of metabolic pathways; and that turnover of organic matter and evolutionary history of organisms dictate ecosystem responses to disturbance at all scales. Fig. 1. Net Ecosystem Production (NEP) represents the balance between autotrophy (stimulated by water, light, and nutrients) and heterotrophy, which increases with oxygen concentrations and temperature. As conditions favoring autotrophy increase, NEP will increase (the top, dashed trajectory). As conditions favoring heterotrophy increase, NEP will decline (the bottom, solid trajectory). This figure has been modified slightly from Burke and Lauenroth, A Theory of Ecosystem Ecology. Perspectives on Global Change Theory Global changes present unique challenges to ecologists because most of our research is carried out at small scales, on a limited number of organisms, and over short enough periods of time so that responses to change can be approximated as linear and monotonic. Peters, Bestelmeyer, and Knapp drove this point home in their presentation, using the dust bowl of the 1930s as an example. Although local effects of drought were well documented, the continental-wide scale of the Dust Bowl was completely unexpected. Underlying this surprise were broader scale processes such as wind that connected distant sites and that were not studied or considered. We know that effects of global change on ecosystem dynamics are increasing and that these changes are often nonlinear. Their trajectories are changing (dust storms are increasing in frequency, for example) and their effects operate across broad spatial and temporal scales. Peters et al. presented a convincing argument that incorporating multi-scale connectivity is essential in order to make predictions about global change. Fine-scale changes often translate into regional or continental shifts, and broader-scale drivers can completely overwhelm fine-scale variation. A theoretical framework that links changes in drivers with ecosystem-level responses across range of spatial and temporal scales is needed. It should integrate five key perspectives: (1) retro-spection based (for example) on legacy data; (2) a fine-scale view of ecological processes; (3) extensions to broader scales; (4) anticipating future changes in ecological drivers; and (5) connectivity across scales and habitats. Both the need and the value of this theory are clear: we must improve our understanding of the effects of global change along with our ability to predict these effects. The remaining four presentations in this symposium covered more familiar ground long-standing, January
4 well-developed constituent theories and families of models. Disturbance and Successional Theory Pickett, Meiners, and Cadenasso elegantly refashioned succession theory in the Scheiner-Willig context, in combination with the disturbance theory long associated with successional sequences. The domain of this theory is any change in composition or structure of species collections at a defined site within some time frame. From the times of Cowles, Clements and Gleason, the common ecological phenomenon of change in (plant) community composition or architecture has been documented, described, and debated. In their reworking, Pickett et al. forgo older assumptions of progress, directionality, a fixed end point, and community integration to present a clear causal repertoire (Fig. 2). The specific mechanisms identified and their combinations provide grist for the individual models that complete Scheiner s and Willig s hierarchy. Fig. 2. The constituent theory of succession as represented hierarchically by its general domain (the process), causes, and specific mechanisms. These mechanisms and their combinations form the basis of the models required to complete Scheiner and Willig s hierarchy. I. Process II. General Causes III. Specific Mechanisms Change in Plant Community Composition or Architecture Differential Site Availability Differential Species Availability Coarse scale disturbance Coarse scale resource gradients Dispersal rain Propagule pool Differential Species Performance Resource availability Ecophysiology Life history Stress Competition Allelopathy Consumers Pickett et al. presented two mature, interconnected theories that focus on disturbance and individual interactions. Successional trajectories are contingent on many factors (length of environmental gradient available, adaptive capacities of species in pool, disturbance type, size, frequency; resource base, colonization order, landscale context) and involve trade-offs between processes that may operate over different temporal or spatial scales. In combination, these refashioned theories provide now familiar hypotheses or predictions about life-history strategies, species richness patterns, and patch dynamics, to name a few. This represents one of ecology s oldest and best-developed constituent theory and provides both the predictions and general understanding that many of us seek from theory. The other venerable constituent theory in the Symposium was that of the niche a stalwart in ecology textbooks that has been under scrutiny since Hubbell proposed his Neutral Theory. In light of recent debates (occupying several ESA sessions), it was instructive to listen to Jon Chase (Ecological niches: moving from old school to modern synthesis ) cover a succinct history of the niche, bring us up to 112 Bulletin of the Ecological Society of America
5 date with niche theory, and present ideas for integrating niche and neutral models. The concept of the niche is fundamental to ecology, and it has had a long history of theoretical and empirical consideration. Hutchinson s famous definition as an n-dimensional hypervolume may well be the best conceptualization of a niche, but its empirical translation has proved challenging. Connell s studies of Balanus glandula and Chthamalus stellatus are the most comprehensive descriptions of niches achieved, but ecologists don t do this sort of research any longer. Studies of the niche have progressed from the realization that we do not need to measure all niche axes (MacArthur s warblers), through May s awful mistake (what happens when we ignore the important axes, though?), and added the statistical rigor that examination of null models contributed. A qualitative advance in niche theory accompanied incorporation of explicit mechanisms, Tilman s R* theory, for example; subsequently, the theory has incorporated predators, disturbance, heterogeneity, and diverse temporal and spatial scales. What has Neutral Theory added to this long maturation? Neutral Theory claims to account more fully for species diversity patterns than Niche Theory can, but makes the mistake of equating the number of coexisting species (allowed in Niche Theory) with the number of limiting resources. With this constraint relaxed, it is easier to see how the two competing theories can be integrated, and this integration is underway by Chase and others (Adler et al. 2007). Chase considers determinism to underlie the effects of different factors on species, while stochasticity influences colonization and extinction. Further maturation of niche theory seems imminent. The most specific tier in Scheiner and Willig s hierarchy is that of individual models; these have been the focus of much theoretical ecology. Bob Holt s fast-paced presentation (The theory of natural enemy victim interactions) provided a whirlwind tour of enemy victim models. Holt maintains that consumer-resource relationships represent a fundamental unit of community ecology. Here, resources are represented by any living population harmed by consumption, and a daunting volume of theory (models) has developed to describe classical predator prey interactions, plant herbivore interactions, predator-parasitoid-host dynamics, and mutualisms that, under certain circumstances, turn bad. These models rest on the following underlying precepts: (1) no species can rely on self-consumption and persist; (2) asymmetry exists between benefits and costs; (3) energy gained must be greater than energy consumed. Beyond these unifying principles, there appears little integration among the increasing forest of models. Theoretical and mathematical ecologists have extended the well-loved and well-worn Lotka- Volterra model, seeking explanations or predictions for stability, persistence, oscillations, limit cycles, lagged oscillations, and unstable dynamics. Holt deftly navigated these extensions: additions of density or ratio dependence, explicit modeling of functional and numerical responses, additions of stage- and age-structure, the complexities of spatial heterogeneity, and the recognition that internal states (energy reserves, elemental stoichiometry) may influence the enemy victim interaction. Models extend beyond two species to consider apparent competition and indirect food web effects. When these extensive ecological models are combined with an explosion of models for disease dynamics, host parasite interactions, and host parasite parasitoid interactions, it is easy to agree with Holt assertion that no unified, constituent theory for enemy victim interactions exists. His conclusion, that future attempts toward a unified theory of enemy victim interactions will need to deal with all of these issues in a January
6 systematic manner, identifies a clear challenge in the advance of enemy victim theory. It is hard to leave the general subject of ecological theory without considering diversity gradients. Fox, Scheiner, and Willing (Theory of diversity gradients: What you think you know is wrong) covered this aspect, focusing on ecological rather than geographic gradients. At least 17 different models address the association between species richness and resources or environmental stressors. All of them rely on a few fundamental propositions: (1) a gradient in a limiting resource exists, (2) the number of individuals present is a direct function of these resources, and (3) the number of species present is a direct function of the number of individuals present. Additional assumptions include (1) the variance in a limiting environmental factor increases with its mean, and (2) nonmonotonic relationships reflect trade-offs. In order to demonstrate why many of these models go wrong, Fox et al. focused on one. Wright s Energy Model: s = a (Eρ/m) z where s = number of species; E = available energy; ρ = number of individuals/ unit of energy; and a, m, and z are constants. Fox s key point was that Wright s model failed because of mistaken hidden assumptions, and because scale matters. In fact, the challenges to developing predictive models of species diversity are substantial when species are not similar, they interact, individuals within a species or population are not energetically equivalent, and steady-state conditions do not apply. Considerations of scale, which are implicit when translating numbers of individuals into numbers of species, or local patterns into landscape patterns, are critical. What we learned from listening to Fox et al. explain and discount one model for species diversity gradients is that combining existing models to support a constituent theory will not be easy. This brief synopsis belies the richness in each talk, and the 25 minutes allocated to each speaker was also often inadequate. Scheiner and Willig are editing a book that includes these talks plus several others; it will give all of us a chance to consider each constituent theory and its associated models in more detail, along with the overall value of the Theory of Ecology that results. Does this general theory help us understand anything we didn t understand before? Does it provide new approaches to challenges, or better predictions for ecological change? Or does it rather provide us a fairly concise statement of the current status of our ecological understanding of the natural world? The presentations in Scheiner and Willig s symposium indicate that the book will be interesting, regardless of the answers to these questions. Literature cited Adler, P. B., J. Hille Ris Lambers, and J. M. Levine A niche for neutrality. Ecology Letters 10: Brown, L., editor The new shorter Oxford English dictionary. Clarendon Press, Oxford, UK. Darwin, C On the origin of species by means of natural selection. John Murray, London, UK. Saran Twombly Division of Environmental Biology, National Science Foundation Any opinions, findings, conclusions, or recommendations expressed are those of the author and do not reflect the views of the National Science Foundation. 114 Bulletin of the Ecological Society of America
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