Aaron J. Wirsing

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.

Predicting ecological consequences of marine top predator declines

Recent studies document unprecedented declines in marine top predators that can initiate trophic cascades. Predicting the wider ecological consequences of these declines requires understanding how predators influence communities by inflicting mortality on prey and inducing behavioral modifications (risk effects). Both mechanisms are important in marine communities, and a sole focus on the effects of predator-inflicted mortality might severely underestimate the importance of predators. We outline direct and indirect consequences of marine predator declines and propose an integrated predictive framework that includes risk effects, which appear to be strongest for long-lived prey species and when resources are abundant. We conclude that marine predators should be managed for the maintenance of both density- and risk-driven ecological processes, and not demographic persistence alone.

Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics

1. Risk effects of predators can profoundly affect community dynamics, but the nature of these effects is context dependent. 2. Although context dependence has hindered the development of a general framework for predicting the nature and extent of risk effects, recent studies suggest that such a framework is attainable if the factors that shape anti-predator behaviour, and its effectiveness, in natural communities are well understood. 3. One of these factors, the interaction of prey escape tactics and landscape features, has been largely overlooked. 4. We tested whether this interaction gives rise to interspecific variation in habitat-use patterns of sympatric large marine vertebrates at risk of tiger shark (Galeocerdo cuvier Peron and LeSueur, 1822) predation. Specifically, we tested the a priori hypothesis that pied cormorants (Phalacrocorax varius Gmelin, 1789) would modify their use of shallow seagrass habitats in a manner opposite to that of previously studied dolphins (Tursiops aduncus Ehrenberg, 1833), dugongs (Dugong dugon Müller, 1776), and green turtles (Chelonia mydas Linnaeus, 1758) because, unlike these species, the effectiveness of cormorant escape behaviour does not vary spatially. 5. As predicted, cormorants used interior and edge portions of banks proportional to the abundance of their potential prey when sharks were absent but shifted to interior portions of banks to minimize encounters with tiger sharks as predation risk increased. Other shark prey, however, shift to edge microhabitats when shark densities increase to take advantage of easier escape despite higher encounter rates with sharks. 6. The interaction of landscape features and escape ability likely is important in diverse communities. 7. When escape probabilities are high in habitats with high predator density, risk effects of predators can reverse the direction of commonly assumed indirect effects of top predators. 8. The interaction between landscape features and prey escape tactics can result in a single predator species having differential effects on their sympatric prey that could cascade through ecosystems and should be incorporated into a general framework for context dependence of risk effects.

Can environmental heterogeneity explain individual foraging variation in wild bottlenose dolphins (Tursiops sp.)

Because behavioral variation within and among populations may result from ecological, social, genetic and phenotypic differences, identifying the mechanism(s) responsible is challenging. Observational studies typically examine social learning by excluding ecological and genetic factors, but this approach is insufficient for many complex behaviors associated with substantial environmental variation. Indian Ocean bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia show individual differences in foraging tactics, including possible tool use with marine sponges and social learning may be responsible for this diversity. However, the contributions of ecological factors to the development of these foraging tactics were not previously investigated. Here, we determined the relationship between ecological variables and foraging tactics and assessed whether differences in habitat use could explain individual differences in foraging tactics. We monitored 14 survey zones to identify how foraging tactics were spatially distributed and matched behavioral data to the ecological variables within each zone. Three of four foraging tactics were significantly correlated with ecological characteristics such as seagrass biomass, water depth, presence of marine sponges and season. Further, individual differences in habitat use were associated with some tactics. However, several tactics overlapped spatially and previous findings suggest demographic and social factors also contribute to the individual variation in this population. This study illustrates the importance of environmental heterogeneity in shaping foraging diversity and shows that investigating social learning by ruling out alternative mechanisms may often be too simplistic, highlighting the need for methods incorporating the relative contributions of multiple factors.

Patterns of Top-Down Control in a Seagrass Ecosystem: Could a Roving Apex Predator Induce a Behaviour-Mediated Trophic Cascade?

1. The loss of large-bodied herbivores and/or top predators has been associated with large-scale changes in ecosystems around the world, but there remain important questions regarding the contexts in which such changes are most likely and the mechanisms through which they occur, particularly in marine ecosystems. 2. We used long-term exclusion cages to examine the effects of large grazers (sea cows, Dugong dugon; sea turtles Chelonia mydas) on seagrass community structure, biomass and nutrient dynamics. Experiments were conducted in habitats with high risk of predation (interior of shallow banks) and lower risk (edges of banks) to elucidate whether nonconsumptive (risk) effects of tiger sharks (Galeocerdo cuvier), a roving predator, structure herbivore impacts on seagrasses. 3. In lower-risk habitats, excluding large herbivores resulted in increased leaf length for Cymodocea angustata and Halodule uninervis. C. angustata shoot densities nearly tripled when released from herbivory, while H. uninervis nearly disappeared from exclusion cages over the course of the study. 4. We found no support for the hypothesis that grazing increases seagrass nutrient content. Instead, phosphorus content was higher in seagrasses within exclosures. This pattern is consistent with decreased light availability in the denser C. angustata canopies that formed in exclosures, and may indicate that competition for light led to the decrease in H. uninervis. 5. Impacts of large grazers were consistent with a behaviour-mediated trophic cascade (BMTC) initiated by tiger sharks and mediated by risk-sensitive foraging by large grazers. 6, Our results suggest that large-bodied grazers likely played important roles in seagrass ecosystem dynamics historically and that roving predators are capable of initiating a BMTC. Conservation efforts in coastal ecosystems must account for such interactions or risk unintended consequences.

The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem

The worldwide decline of large-bodied marine taxa has made it difficult to draw conclusions about the relative importance of top-down control, and the mechanisms through which it might operate, in coastal marine ecosystems. Since 1997, the Shark Bay Ecosystem Research Project has used the relatively pristine seagrass community of Shark Bay, Australia, to investigate the potential for tiger sharks, the apex predator in the ecosystem, to have an impact on their large-bodied prey through non-consumptive (‘risk’) effects. Here, we synthesise nearly 15 years of data to demonstrate that tiger sharks have widespread risk effects on both large-bodied herbivores and mesopredators in Shark Bay and explore the possibility that these impacts may cascade to lower trophic levels. Although much work remains to be done, our studies suggest that losses of top predators in subtropical estuaries may have greater consequences than generally appreciated and that efforts to conserve and restore their populations should be a priority. Furthermore, future management strategies and studies must explicitly consider the potential for predators to influence behaviour of even large-bodied marine taxa.

Fear factor: do dugongs (Dugong dugon) trade food for safety from tiger sharks (Galeocerdo cuvier)?

Predators can influence plants indirectly by altering spatial patterns of herbivory, so studies assessing the relationship between perceived predation risk and habitat use by herbivores may improve our understanding of community organization. In marine systems, the effects of predation danger on space use by large herbivores have received little attention, despite the possibility that predator-mediated alterations in patterns of grazing by these animals influence benthic community structure. We evaluated the relationship between habitat use by foraging dugongs (Dugong dugon) and the threat of tiger shark predation in an Australian embayment (Shark Bay) between 1997 and 2004. Dugong densities were quantified in shallow (putatively dangerous) and deep (putatively safe) habitats (seven survey zones allocated to each habitat), and predation hazard was indexed using catch rates of tiger sharks (Galeocerdo cuvier); seagrass volume provided a measure of food biomass within each zone. Overall, dugongs selected shallow habitats, where their food is concentrated. Foragers used shallow and deep habitats in proportion to food availability (input matching) when large tiger sharks were scarce and overused deep habitats when sharks were common. Furthermore, strong synchrony existed between daily measures of shark abundance and the extent to which deep habitats were overused. Thus, dugongs appear to adaptively manage their risk of death by allocating time to safe but impoverished foraging patches in proportion to the likelihood of encountering predators in profitable but more dangerous areas. This apparent food-safety trade-off has important implications for seagrass community structure in Shark Bay, as it may result in marked temporal variability in grazing pressure.

Spatial responses to predators vary with prey escape mode

Prey often avoid their predators but may, under certain conditions, remain in or even shift to space where predators are relatively abundant when threatened. Here, we review studies of habitat choices by multiple, sympatric prey species at risk from a shared predator to show that the defensive decision to avoid or select predator-rich space is contingent on prey escape behaviour. We suggest that prey species with escape tactics offering little chance of survival following an encounter should seek predator scarcity, whereas those with tactics whose post-encounter effectiveness is spatially correlated with predator abundance should be most likely to match the distribution of their predators. Furthermore, we argue that the nature of the defensive spatial response of a prey species with a particular escape tactic also depends on the hunting approach used by its predator and the setting of the predator–prey interaction (i.e. landscape features). Accordingly, an integrated approach that accounts for prey escape behaviour and the context provided by predator hunting mode and landscape features should lead to a better understanding of antipredator spatial shifts and improve our ability to anticipate the consequences of changes in predator numbers for prey distributions and ecosystem dynamics. We conclude by encouraging further exploration of contingency in antipredator behaviour and the possibility that generalist predators might indirectly influence prey resources and community properties via diverse pathways that are mediated by spatial shifts of prey species with different escape tactics.

Saving the World's Terrestrial Megafauna

From the late Pleistocene to the Holocene, and now the so called Anthropocene, humans have been driving an ongoing series of species declines and extinctions (Dirzo et al. 2014). Large-bodied mammals are typically at a higher risk of extinction than smaller ones (Cardillo et al. 2005). However, in some circumstances terrestrial megafauna populations have been able to recover some of their lost numbers due to strong conservation and political commitment, and human cultural changes (Chapron et al. 2014). Indeed many would be in considerably worse predicaments in the absence of conservation action (Hoffmann et al. 2015). Nevertheless, most mammalian megafauna face dramatic range contractions and population declines. In fact, 59% of the world’s largest carnivores (≥ 15 kg, n = 27) and 60% of the world’s largest herbivores (≥ 100 kg, n = 74) are classified as threatened with extinction on the International Union for the Conservation of Nature (IUCN) Red List (supplemental table S1 and S2). This situation is particularly dire in sub-Saharan Africa and Southeast Asia, home to the greatest diversity of extant megafauna (figure 1). Species at risk of extinction include some of the world’s most iconic animals—such as gorillas, rhinos, and big cats (figure 2 top row)—and, unfortunately, they are vanishing just as science is discovering their essential ecological roles (Estes et al. 2011). Here, our objectives are to raise awareness of how these megafauna are imperiled (species in supplemental table S1 and S2) and to stimulate broad interest in developing specific recommendations and concerted action to conserve them.

A comparison of shark and wolf research reveals similar behavioral responses by prey

Marine and terrestrial ecologists rarely exchange information, yet comparing research from both sides of the land–sea boundary holds great potential for improving our understanding of ecological processes. For example, by comparing the interaction between tiger sharks (Galeocerdo cuvier) and dugongs (Dugong dugon) to that between gray wolves (Canis lupus) and elk (Cervus elaphus), we show that top predators in marine and terrestrial ecosystems trigger three similar types of anti-predator behavior: (1) encounter avoidance, (2) escape facilitation, and (3) increased vigilance. By implication, the ecological roles of top predators in both ecosystems may be more similar than previously thought, and studies that fail to account for multiple modes of anti-predator behavior are likely to underestimate these roles and the consequences of eliminating predators from ecosystems. We encourage more communication between marine and terrestrial ecologists, in the interest of generating further insights into ecosystem dy...