Oswald J. Schmitz

Status and Ecological Effects of the World’s Largest Carnivores

Background The largest terrestrial species in the order Carnivora are wide-ranging and rare because of their positions at the top of food webs. They are some of the world’s most admired mammals and, ironically, some of the most imperiled. Most have experienced substantial population declines and range contractions throughout the world during the past two centuries. Because of the high metabolic demands that come with endothermy and large body size, these carnivores often require large prey and expansive habitats. These food requirements and wide-ranging behavior often bring them into conflict with humans and livestock. This, in addition to human intolerance, renders them vulnerable to extinction. Large carnivores face enormous threats that have caused massive declines in their populations and geographic ranges, including habitat loss and degradation,persecution, utilization, and depletion of prey. We highlight how these threats can affect theconservation status and ecological roles of this planet’s 31 largest carnivores. Ecologically important carnivores. Seven species of large carnivores with documented ecological effects involving (A) “tri-trophic cascades” from large carnivores to prey to plants, (B) “mesopredator cascades” from large carnivores to mesopredators to prey of mesopredators, and (C) both tri-trophic and mesopredator cascades. [Photo credits: sea otter (N. Smith), puma (W. Ripple), lion (K. Abley), leopard (A. Dey), Eurasianlynx (B. Elmhagen), dingo (A. McNab), gray wolf (D. Mclaughlin)] Advances Based on empirical studies, trophic cascades have been documented for 7 of the 31 largest mammalian carnivores (not including pinnipeds). For each of these species (see figure), human actions have both caused declines and contributed to recovery, providing “natural experiments” for quantifying their effects on food-web and community structure. Large carnivores deliver economic and ecosystem services via direct and indirect pathways that help maintain mammal, avian, invertebrate,and herpetofauna abundance or richness. Further, they affect other ecosystem processes and conditions, such as scavenger subsidies, disease dynamics, carbon storage, stream morphology, and crop production. The maintenance or recovery of ecologically effective densities of large carnivores is an important tool for maintaining the structure and function of diverse ecosystems. Outlook Current ecological knowledge indicates that large carnivores are necessary for the maintenanceof biodiversity and ecosystem function. Human actions cannot fully replace the role of large carnivores. Additionally, the future of increasing human resource demands and changing climate will affect biodiversity and ecosystem resiliency. These facts, combined with the importance of resiliente cosystems, indicate that large carnivores and their habitats should be maintained and restored wherever possible. Preventing the extinction of these species and the loss of their irreplaceable ecological function and importance will require novel, bold, and deliberate actions. We propose a Global Large Carnivore Initiative to coordinate local, national, and international research, conservation, and policy. Preserving Predators Large-bodied animals play essential roles in ecosystem structuring and stability through both indirect and direct trophic effects. In recent times, humans have disrupted this trophic structure through both habitat destruction and active extirpation of large predators, resulting in large declines in numbers and vast contractions in their geographic ranges. Ripple et al. (10.1126/science.1241484; see the Perspective by Roberts) review the status, threats, and ecological importance of the 31 largest mammalian carnivores globally. These species are responsible for a suite of direct and indirect stabilizing effects in ecosystems. Current levels of decline are likely to result in ecologically ineffective population densities and can lead to ecosystem instability. The preservation of large carnivores can be challenging because of their need for large ranges and their potential for human conflict. However, the authors demonstrate that the preservation of large carnivores is ecologically important and that the need for conservation action is immediate, given the severity of the threats they face. Large carnivores face serious threats and are experiencing massive declines in their populations and geographic ranges around the world. We highlight how these threats have affected the conservation status and ecological functioning of the 31 largest mammalian carnivores on Earth. Consistent with theory, empirical studies increasingly show that large carnivores have substantial effects on the structure and function of diverse ecosystems. Significant cascading trophic interactions, mediated by their prey or sympatric mesopredators, arise when some of these carnivores are extirpated from or repatriated to ecosystems. Unexpected effects of trophic cascades on various taxa and processes include changes to bird, mammal, invertebrate, and herpetofauna abundance or richness; subsidies to scavengers; altered disease dynamics; carbon sequestration; modified stream morphology; and crop damage. Promoting tolerance and coexistence with large carnivores is a crucial societal challenge that will ultimately determine the fate of Earth’s largest carnivores and all that depends upon them, including humans.

Trophic Cascades in Terrestrial Systems: A Review of the Effects of Carnivore Removals on Plants

We present a quantitative synthesis of trophic cascades in terrestrial systems using data from 41 studies, reporting 60 independent tests. The studies covered a wide range of taxa in various terrestrial systems with varying degrees of species diversity. We quantified the average magnitude of direct effects of carnivores on herbivore prey and indirect effects of carnivores on plants. We examined how the effect magnitudes varied with type of carnivores in the study system, food web diversity, and experimental protocol. A metaanalysis of the data revealed that trophic cascades were common among the studies. Exceptions to this general trend did arise. In some cases, trophic cascades were expected not to occur, and they did not. In other cases, the direct effects of carnivores on herbivores were stronger than the indirect effects of carnivores on plants, indicating that top‐down effects attenuated. Top‐down effects usually attenuated whenever plants contained antiherbivore defenses or when herbivore species diversity was high. Conclusions about the strength of top‐down effects of carnivores varied with the type of carnivore and with the plant‐response variable measured. Vertebrate carnivores generally had stronger effects than invertebrate carnivores. Carnivores, in general, had stronger effects when the response was measured as plant damage rather than as plant biomass or plant reproductive output. We caution, therefore, that conclusions about the strength of top‐down effects could be an artifact of the plant‐response variable measured. We also found that mesocosm experiments generally had weaker effect magnitudes than open‐plot field experiments or observational experiments. Trophic cascades in terrestrial systems, although not a universal phenomenon, are a consistent response throughout the published studies reviewed here. Our analysis thus suggests that they occur more frequently in terrestrial systems than currently believed. Moreover, the mechanisms and strengths of top‐down effects of carnivores are equivalent to those found in other types of systems (e.g., aquatic environments).

BEHAVIORALLY MEDIATED TROPHIC CASCADES: EFFECTS OF PREDATION RISK ON FOOD WEB INTERACTIONS

Trophic cascades are regarded as important signals for top-down control of food web dynamics. Although there is clear evidence supporting the existence of trophic cascades, the mechanisms driving this important dynamic are less clear. Trophic cascades could arise through direct population-level effects, in which predators prey on herbivores, thereby decreasing the abundance of herbivores that impact plant trophic levels. Trophic cascades could also arise through indirect behavioral-level effects, in which herbivore prey shift their foraging behavior in response to predation risk. Such behavioral shifts can result in reduced feeding time and increased starvation risk, again lowering the impact of her- bivores on plants. We evaluated the relative importance of these two mechanisms, using field experiments in an old-field system composed of herbaceous plants, grasshopper her- bivores, and spider predators. We created two treatments, Risk spiders that had their che- licerae glued, and Predation spiders that remained unmanipulated. We then systematically evaluated the impacts of these predator manipulations at behavioral, population, and food web scales in experimental mesocosms. At the behavioral level, grasshoppers did not dis- tinguish between Risk spiders and Predation spiders. Grasshoppers exhibited significant shifts in feeding-time budget in the presence of spiders vs. when alone. At the grasshopper population level, Risk spider and Predation spider treatments caused the same level of grasshopper mortality, which was significantly higher than mortality in a control without spiders, indicating that the predation effects were compensatory to risk effects. At the food web level, Risk spider and Predation spider treatments decreased the impact grasshoppers had on grass biomass, supporting the existence of a trophic cascade. Moreover, Risk spider and Predation spider treatments produced statistically similar effects, again indicating that predation effects on trophic dynamics were compensatory to risk effects. We conclude that indirect effects resulting from antipredator behavior can produce trophic-level effects that are similar in form and strength to those generated by direct predation events.

Effects of Predator Hunting Mode on Grassland Ecosystem Function

The way predators control their prey populations is determined by the interplay between predator hunting mode and prey antipredator behavior. It is uncertain, however, how the effects of such interplay control ecosystem function. A 3-year experiment in grassland mesocosms revealed that actively hunting spiders reduced plant species diversity and enhanced aboveground net primary production and nitrogen mineralization rate, whereas sit-and-wait ambush spiders had opposite effects. These effects arise from the different responses to the two different predators by their grasshopper prey—the dominant herbivore species that controls plant species composition and accordingly ecosystem functioning. Predator hunting mode is thus a key functional trait that can help to explain variation in the nature of top-down control of ecosystems.

Biodiversity and the productivity and stability of ecosystems

Attempts to unveil the relationships between the taxonomic diversity, productivity and stability of ecosystems continue to generate inconclusive, contradictory and controversial conclusions. New insights from recent studies support the hypothesis that species diversity enhances productivity and stability in some ecosystems, but not in others. Appreciation is growing for the ways that particular ecosystem features, such as environmental variability and nutrient stress, can influence biotic interactions. Alternatives to the diversity-stability hypothesis have been proposed, and experimental approaches are starting to evolve to test these hypotheses and to elucidate the mechanisms underlying the functional role of species diversity.

PREDATOR DIVERSITY AND TROPHIC INTERACTIONS

The recognition that predators play important roles in ecosystems has prompted research to resolve how combinations of predator species influence ecosystem functions. Interactions among predator species and their prey can lead to a host of linear and nonlinear effects. Understanding the conditions causing these effects is critical for assigning predator species to functional groups in ways that lead to predictive theory of predator diversity effects on trophic interactions. To this end, I provide a synthesis of experiments examining multiple-predator-species effects on mortality of single shared prey. I show how experimental design and experimental venue can determine the conclusion about the importance of predator diversity on trophic interactions. In addition, I link natural history insights on predator species habitat and hunting behavior with linear and nonlinear multiple-predator effects to derive a new concept of predator diversity effects on trophic interactions. This concept holds that the nature of predator diversity effects is contingent upon predator species hunting mode plus predator and prey species habitat domain (defined as the spatial extent to which a microhabitat is used by a species). This concept allows the classification of multiple-predator effects into four broad functional categories: substitutable, nonlinear due to predator species interference, nonlinear due to intraguild predation, and nonlinear due to predator species synergism. Experimental evidence so far provides ample and comparatively equal support for substitutable, interference, and intraguild effects, and equivocal support for nonlinear synergisms. The paper closes by discussing ways to further a research program aimed at using the building blocks presented here to understand predator functional diversity and trophic interactions in complex ecological systems.

Direct and Indirect Effects of Predation and Predation Risk in Old-Field Interaction Webs

Indirect effects emerge when a change in the abundance of one species indirectly affects another by changing the abundances of intermediate species—called density‐mediated indirect effects—or they arise when one species modifies how two other species interact—called trait‐mediated indirect effects. I report on field experiments that evaluated how grass and herb biomass in old‐field interaction webs was influenced indirectly by a spider carnivore through its interactions with a generalist and a grass‐specialist grasshopper species. I manipulated interaction pathways between the spider and the plants using different combinations of the grasshopper species. I changed the modality of predator‐prey interactions to isolate density‐mediated from trait‐mediated effects using natural spiders (predation spiders) or spiders that were prevented from subduing prey by mouthpart manipulation (risk spiders). I found that indirect effects were stronger in speciose, reticulate food webs than in linear food chains owing to a trait‐mediated effect, a diet shift by herbivores in response to predation risk. Spiders alone did not have significant effects on grasshopper densities in the field experiments, removing any possibility of density‐mediated indirect effects. The study illustrates that ecologists should not underestimate the importance of behavioral ecology in determining community‐level interactions.

REVISITING THE CLASSICS: CONSIDERING NONCONSUMPTIVE EFFECTS IN TEXTBOOK EXAMPLES OF PREDATOR-PREY INTERACTIONS

Predator effects on prey dynamics are conventionally studied by measuring changes in prey abundance attributed to consumption by predators. We revisit four classic examples of predator-prey systems often cited in textbooks and incorporate subsequent studies of nonconsumptive effects of predators (NCE), defined as changes in prey traits (e.g., behavior, growth, development) measured on an ecological time scale. Our review revealed that NCE were integral to explaining lynx-hare population dynamics in boreal forests, cascading effects of top predators in Wisconsin lakes, and cascading effects of killer whales and sea otters on kelp forests in nearshore marine habitats. The relative roles of consumption and NCE of wolves on moose and consequent indirect effects on plant communities of Isle Royale depended on climate oscillations. Nonconsumptive effects have not been explicitly tested to explain the link between planktonic alewives and the size structure of the zooplankton, nor have they been invoked to attribute keystone predator status in intertidal communities or elsewhere. We argue that both consumption and intimidation contribute to the total effects of keystone predators, and that characteristics of keystone consumers may differ from those of predators having predominantly NCE. Nonconsumptive effects are often considered as an afterthought to explain observations inconsistent with consumption-based theory. Consequently, NCE with the same sign as consumptive effects may be overlooked, even though they can affect the magnitude, rate, or scale of a prey response to predation and can have important management or conservation implications. Nonconsumptive effects may underlie other classic paradigms in ecology, such as delayed density dependence and predator-mediated prey coexistence. Revisiting classic studies enriches our understanding of predator-prey dynamics and provides compelling rationale for ramping up efforts to consider how NCE affect traditional predator-prey models based on consumption, and to compare the relative magnitude of consumptive and NCE of predators.

CONNECTING THEORETICAL AND EMPIRICAL STUDIES OF TRAIT‐MEDIATED INTERACTIONS

Trait-mediated interactions (TMIs), in which trophic and competitive inter- actions depend on individual traits as well as on overall population densities, have inspired large amounts of research, but theoretical and empirical studies have not been well con- nected. To help mitigate this problem, we review and synthesize the theoretical literature on TMIs and, in particular, on trait-mediated indirect interactions, TMIIs, in which the presence of one species mediates the interaction between a second and third species. (1) In models, TMIs tend to stabilize simple communities; adding further biological detail often reduces stability in models, but populations may persist even if their dynamics become mathematically unstable. (2) Short- and long-term changes in population density caused by TMIs depend even more on details, such as the curvature of functional responses and trade-offs, which have rarely been measured. (3) The effects of TMIs in multipredator communities depend in a straightforward way on the specificity of prey defenses. (4) Tritrophic and more complex communities are theoretically difficult; few general conclu- sions have emerged. Theory needs new kinds of experiments as a guide. The most critical needs are experiments that measure curvatures of trade-offs and responses, and experiments that (combined with theory) allow us to scale from short- to long-term responses of com- munities. Anecdotal evidence from long-term and large-scale studies suggests that TMIs may affect community dynamics at practical management scales; community models in- corporating TMIs are necessary and require closer collaborations between theory and ex-

EFFECTS OF TOP PREDATOR SPECIES ON DIRECT AND INDIRECT INTERACTIONS IN A FOOD WEB

Current theory on trophic interactions in food webs assumes that ecologically similar species can be treated collectively as a single functional unit such as a guild or trophic level. This theory implies that all species within that unit transmit identical direct and indirect effects throughout the community. We evaluated this assumption by conducting experiments to compare the direct and indirect effects of three top-predator species, be- longing to the same hunting spider guild, on the same species of grasshopper and on old- field grasses and herbs. Observations under field conditions revealed that each spider species exhibited different hunting behavior (i.e., sit-and-wait, sit-and-pursue, and active hunting) and occupied different locations within the vegetation canopy. These differences resulted in different direct effects on grasshopper prey. Grasshoppers demonstrated significant be- havioral (diet) shifts in the presence of sit-and-wait and sit-and-pursue species but not when faced with actively hunting species. Grasshopper density was significantly reduced by spider species that occupied lower parts of the vegetation canopy (sit-and-pursue and actively hunting species), but it was not significantly reduced by the sit-and-wait spider species that occupied the upper parts of the canopy. These direct effects manifested themselves differ- ently in the plant trophic level. The sit-and-wait spider caused indirect effects on plants by changing grasshopper foraging behavior (a trait-mediated effect). The sit-and-pursue spider caused indirect effects by reducing grasshopper density (density-mediated effects); the effects of changes in grasshopper behavior were thus not reflected in the plant trophic level. The actively hunting spiders had strictly density-mediated indirect effects on plants. The study offers mechanistic insight into how predator species within the same guild can have very different trophic effects in food webs. Thus classical modeling approaches that treat all predator species as a single functional unit may not adequately capture biologically relevant details that influence community dynamics.