Daniel F. Doak

The Keystone-Species Concept in Ecology and ConservationManagement and policy must explicitly consider the complexity of interactions in natural systems

1Will the extinction of a single species in a community cause the loss of many others? Can we identify a set of species that are so important in determining the ecological functioning of a community that they warrant special conservation efforts? The answer to these questions hinges on the existence of a limited number of species whose loss would precipitate many further extinctions; these species have often been labeled keystone species. The term keystone species has enjoyed an enduring popularity in the ecological literature since its introduction by Robert T. Paine in 1969: Paine (1969) was cited in more than 92 publications from 1970 to 1989; an earlier paper (Paine 1966), which introduced the phenomenon of keystone species in intertidal systems but did not use the term, was cited more than 850 times during the same period. As used by Paine and other ecologists, there are two hallmarks of keystone species. First, their presence is crucial in maintaining the organization and diversity of their ecological communities. Second, it is implicit that these species are exceptional, relative to the rest of the community, in their importance.

Filling key gaps in population and community ecology

We propose research to fill key gaps in the areas of population and community ecology, based on a National Science Foundation workshop identifying funding priorities for the next 5-10 years. Our vision for the near future of ecology focuses on three core areas: predicting the strength and context-dependence of species interactions across multiple scales; identifying the importance of feedbacks from individual interactions to ecosystem dynam- ics; and linking pattern with process to understand species coexistence. We outline a combination of theory devel- opment and explicit, realistic tests of hypotheses needed to advance population and community ecology.

Physical stress and diversity-productivity relationships: the role of positive interactions.

If environmental stress provides conditions under which positive relationships between plant species richness and productivity become apparent, then species that seem functionally redundant under constant conditions may add to community functioning under variable conditions. Using naturally co-occurring mosses and liverworts, we constructed bryophyte communities to test relationships between species diversity (1, 2, 4, 8, 16, 24, or 32 species) and productivity under constant conditions and when exposed to experimental drought. We found no relationship between species richness and biomass under constant conditions. However, when communities were exposed to experimental drought, biomass increased with species richness. Responses of individual species demonstrated that facilitative interactions rather than sampling effects or niche complementarity best explained results—survivorship increased for almost all species, and those species least resistant to drought in monoculture had the greatest increase in biomass. Positive interactions may be an important but previously underemphasized mechanism linking high diversity to high productivity under stressful environmental conditions.

LONGEVITY CAN BUFFER PLANT AND ANIMAL POPULATIONS AGAINST CHANGING CLIMATIC VARIABILITY

Both means and year-to-year variances of climate variables such as temperature and precipitation are predicted to change. However, the potential impact of changing climatic variability on the fate of populations has been largely unexamined. We analyzed multiyear demographic data for 36 plant and animal species with a broad range of life histories and types of environment to ask how sensitive their long-term stochastic population growth rates are likely to be to changes in the means and standard deviations of vital rates (survival, reproduction, growth) in response to changing climate. We quantified responsiveness using elasticities of the long-term population growth rate predicted by stochastic projection matrix models. Short-lived species (insects and annual plants and algae) are predicted to be more strongly (and negatively) affected by increasing vital rate variability relative to longer-lived species (perennial plants, birds, ungulates). Taxonomic affiliation has little power to explain sensitivity to increasing variability once longevity has been taken into account. Our results highlight the potential vulnerability of short-lived species to an increasingly variable climate, but also suggest that problems associated with short-lived undesirable species (agricultural pests, disease vectors, invasive weedy plants) may be exacerbated in regions where climate variability decreases.

LIFE STAGE SIMULATION ANALYSIS: ESTIMATING VITAL-RATE EFFECTS ON POPULATION GROWTH FOR CONSERVATION

We developed a simulation method, known as life-stage simulation analysis (LSA) to measure potential effects of uncertainty and variation in vital rates on population growth (λ) for purposes of species conservation planning. Under LSA, we specify plausible or hypothesized levels of uncertainty, variation, and covariation in vital rates for a given population. We use these data under resampling simulations to establish random combinations of vital rates for a large number of matrix replicates and finally summarize results from the matrix replicates to estimate potential effects of each vital rate on λ in a probability-based context. Estimates of potential effects are based on a variety of summary statistics, such as frequency of replicates having the same vital rate of highest elasticity, difference in elasticity values calculated under simulated conditions vs. elasticities calculated using mean invariant vital rates, percentage of replicates having positive population growth, and variation in λ explained ...

Demographic compensation and tipping points in climate-induced range shifts

To persist, species are expected to shift their geographical ranges polewards or to higher elevations as the Earth’s climate warms. However, although many species’ ranges have shifted in historical times, many others have not, or have shifted only at the high-latitude or high-elevation limits, leading to range expansions rather than contractions. Given these idiosyncratic responses to climate warming, and their varied implications for species’ vulnerability to climate change, a critical task is to understand why some species have not shifted their ranges, particularly at the equatorial or low-elevation limits, and whether such resilience will last as warming continues. Here we show that compensatory changes in demographic rates are buffering southern populations of two North American tundra plants against the negative effects of a warming climate, slowing their northward range shifts, but that this buffering is unlikely to continue indefinitely. Southern populations of both species showed lower survival and recruitment but higher growth of individual plants, possibly owing to longer, warmer growing seasons. Because of these and other compensatory changes, the population growth rates of southern populations are not at present lower than those of northern ones. However, continued warming may yet prove detrimental, as most demographic rates that improved in moderately warmer years declined in the warmest years, with the potential to drive future population declines. Our results emphasize the need for long-term, range-wide measurement of all population processes to detect demographic compensation and to identify nonlinear responses that may lead to sudden range shifts as climatic tipping points are exceeded.

KILLER APPETITES: ASSESSING THE ROLE OF PREDATORS IN ECOLOGICAL COMMUNITIES

Large body size, carnivory, and endothermic costs lead to exceptionally high caloric demands in many mammalian predators. The potential impact on prey resources may be marked but is difficult to demonstrate because of the mobility, sparseness, and cryptic nature of these animals. In this study, we developed a method based on comparative bioenergetics and demographic modeling to evaluate predator effects and then used this approach to assess the potential impact of killer whales on sea otter and Steller sea lion populations in the Aleutian Islands. Daily caloric requirements of killer whales determined from allometric regressions for field metabolic rate show that an adult killer whale requires 51-59 kcal·kg 21 ·d 21 (2.5-2.9 W/kg). Caloric values of prey items determined by bomb calorimetry ranged from 41 630 kcal for an adult female sea otter to sequentially higher values for male otters, sea lion pups, and adult Steller sea lions. Integrating these results with demographic changes in marine mammal populations show that fewer than 40 killer whales could have caused the recent Steller sea lion decline in the Aleutian archipelago; a pod of five individuals could account for the decline in sea otters and the continued suppression of sea lions. The collapse of the historical prey base of killer whales due to human whaling may have contributed to a sequential dietary switch from high to low caloric value prey, thereby initiating these declines. This study demonstrates that a combined physiological-demographic approach increases our ability to critically evaluate the potential impact of a predator on community structure and enables us to define underlying mechanisms

Spatial scale mediates the influence of habitat fragmentation on dispersal success: Implications for conservation

Abstract Increasingly, conservationists are seeking insights from ecological theory to choose strategies of habitat management that will best maintain threatened species. Often, these questions revolve around ways of mitigating the dangers posed by habitat fragmentation. Problems involving the scale of both animal movement and spatial heterogeneity inexorably arise when assessing the effects of fragmentation. We present results from a simple spatial model that simulates the dispersal of animals in a landscape of stochastically clustered habitat fragments. Varying the number of clusters and the spatial scale at which clustering occurs illustrates that heterogeneity has different and conflicting effects on animal movement when it occurs at different scales. Indeed, the scale of clustering is the most important feature in determining disperser performance in our model. Seeking to compare our modeling results with actual data, we review empirical studies of fragmented populations and habitats. Surprisingly, we conclude that very few studies have addressed the mechanisms by which fragmentation will influence population dynamics or, in particular, the ways in which spatial scale mediate these effects. We conclude that the explicit consideration of scale is essential in discussions of habitat fragmentation and of optimal conservation strategies.

UNDERSTANDING AND PREDICTING ECOLOGICAL DYNAMICS: ARE MAJOR SURPRISES INEVITABLE

Ecological surprises, substantial and unanticipated changes in the abundance of one or more species that result from previously unsuspected processes, are a common outcome of both experiments and observations in community and population ecology. Here, we give examples of such surprises along with the results of a survey of well-established field ecologists, most of whom have encountered one or more surprises over the course of their careers. Truly surprising results are common enough to require their consideration in any reasonable effort to characterize nature and manage natural resources. We classify surprises as dynamic-, pattern-, or intervention-based, and we speculate on the common processes that cause ecological systems to so often surprise us. A long-standing and still growing concern in the ecological literature is how best to make predictions of future population and community dynamics. Although most work on this subject involves statistical aspects of data analysis and modeling, the frequency and nature of ecological surprises imply that uncertainty cannot be easily tamed through improved analytical procedures, and that prudent management of both exploited and conserved communities will require precautionary and adaptive management approaches.

Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism.

Understanding cooperation is a central challenge in biology, because natural selection should favor “free-loaders” that reap benefits without reciprocating. For interspecific cooperation (mutualism), most approaches to this paradox focus on costs and benefits of individual partners and the strategies mutualists use to associate with beneficial partners. However, natural selection acts on lifetime fitness, and most mutualists, particularly longer-lived species interacting with shorter-lived partners (e.g., corals and zooxanthellae, tropical trees and mycorrhizae) interact with multiple partner species throughout ontogeny. Determining how multiple partnerships might interactively affect lifetime fitness is a crucial unexplored link in understanding the evolution and maintenance of cooperation. The tropical tree Acacia drepanolobium associates with four symbiotic ant species whose short-term individual effects range from mutualistic to parasitic. Using a long-term dataset, we show that tree fitness is enhanced by partnering sequentially with sets of different ant symbionts over the ontogeny of a tree. These sets include a “sterilization parasite” that prevents reproduction and another that reduces tree survivorship. Trees associating with partner sets that include these “parasites” enhance lifetime fitness by trading off survivorship and fecundity at different life stages. Our results demonstrate the importance of evaluating mutualism within a community context and suggest that lifespan inequalities among mutualists may help cooperation persist in the face of exploitation.