Rise Of The Predator BlackJacks
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Monkeys exploded in abundance on the predator-free islands, denuding islands of vegetation and causing complete reproductive failure in birds by eating their eggs Terborgh et al.
Across sub-Saharan Africa, another primate mesopredator, the olive baboon Papio anubis , has dramatically increased in abundance in areas where lion and leopard populations have been decimated Brashares et al.
Excessive predation by baboons is exacerbating declines in ungulate populations, and increasingly brazen troops of crop-raiding baboons force families to take children out of school to help guard fields Brashares et al.
A preliminary literature survey shows that the release of baboons has resulted in widespread conflict with humans and their livestock, pets, and crops.
In the Atlantic Ocean, overharvesting of sharks led to population explosions of the cownose ray Rhinoptera bonasus , which in turn reduced bay scallop Argopecten irradians populations to such low levels that a century-old scallop fishery was recently forced to close figure 2 ; Myers et al.
Yearly abundance estimates from surveys of great sharks top level , elasmobranch shark, ray, and skate mesopredators middle level , and bivalve prey, the bay scallop bottom level.
Adapted from Myers and colleagues and reprinted with permission from the American Association for the Advancement of Science.
Abundance estimates were obtained from a variety of surveys conducted in the Atlantic Ocean from to See Myers and colleagues for survey details and scientific names.
The dotted arrow between the top and middle trophic levels represents a loss of mesopredator control following shark declines; the solid arrow between the middle and bottom trophic levels represents increased control of bay scallops by the cownose ray mesopredator following release.
Conservation efforts geared toward controlling exotic species can also be greatly hindered by mesopredator release. The potential for mesopredator release to complicate conservation efforts is particularly well illustrated in the case of islands that are infested by both rats and cats.
Modeling efforts Courchamp et al. If control efforts unintentionally catalyze the release of an exotic mesopredator, even the best-intentioned conservation efforts may backfire and place ecosystems in greater jeopardy Bergstrom et al.
Mesopredator outbreaks are commonly observed in fragmented habitats, an association that can be credited to three factors.
First, apex predators tend to require more area than mesopredators and are therefore more likely to disappear when habitat is lost.
Second, large predators are likely to encounter high levels of conflict with humans where fragmentation occurs, leading to higher levels of persecution.
In scenarios in which this improved resource availability is primarily responsible for mesopredator outbreaks, the presence of large predators is even more critical because such top-down regulation is the only constraint on mesopredator abundance.
When both top-down and bottom-up constraints on mesopredators'population growth are relaxed, as they most commonly are in fragmented landscapes, the setting is ideal for the explosive growth of mesopredator populations.
A fundamental challenge in demonstrating mesopredator release is ruling out alternative explanations for mesopredator overabundance, such as the habitat changes that often cooccur with the loss of apex predators.
Uncertainty surrounding the causal mechanisms that underlie mesopredator outbreaks muddies prescriptions for management.
Unfortunately, studies of mesopredator release often fail to demonstrate causal links between apex predator declines and mesopredator outbreaks.
Gehrt and Prange also demonstrated that raccoons did not avoid coyotes in their Illinois study site. Litvaitis and Villafuerte similarly argued that the negative correlation between numbers of Egyptian mongoose Herpestes ichneumon and Iberian lynx Lynx pardinus in Spain resulted from differential habitat use rather than topdown control by lynx, but a subsequent path analysis supports the hypothesis that lynx do indeed control mongoose numbers Palomares et al.
In recognition of this paucity of hard evidence for mesopredator release, several recent studies have used radiotelemetry to convincingly demonstrate apex predator control of mesopredators.
Additionally, researchers conducted several experiments in which apex predator numbers were manipulated in replicated treatments and the responses by mesopredators and prey were documented e.
These studies show that mesopredator release can occur rapidly and dramatically when apex predators are removed, but an experimental approach is rarely possible at large scales and with large carnivores.
However, modeling approaches can be used to parse the relative contributions of bottom-up habitat and resources and top-down apex predator forces.
This approach has been employed nicely in a large-scale study examining the relative influence of apex predators wolves and lynx and land-use changes on red fox populations in Sweden Elmhagen and Rushton Thus far, we have painted a rather bleak picture of ecosystems decimated by mesopredator outbreaks induced by large predator extirpations.
However, predator management is characterized by complex ecological, economic, and social trade-offs. While large predators present many ecological benefits, they can also pose a serious threat to species of conservation concern.
For instance, cougars Puma concolor contributed to the near extinction of endangered Sierra bighorn sheep in the s Ovis canadensis sierrae ; Wehausen Any proposal to protect or reintroduce apex predators must acknowledge the full range of trade-offs involved in predator management.
Ideally, an evaluation of the full expense of mesopredator release would compare the costs of tolerating apex predators with the expense of managing mesopredator outbreaks in their absence.
Although previous assessments of predator control programs provide some insight into such expenses, they also illustrate the difficulty in deriving the true economic cost of tolerating versus managing any given predator.
These results indicate that such predator control programs probably do not make economic sense, because the benefits to the sheep industry and society as a whole are very likely lower than the costs to taxpayers.
Rigorous cost-benefit analyses that take into account the ecosystem services of apex predators, as well as the costs associated with tolerating those predators, are sorely lacking.
In the few cases in which data exist to compare economic losses from apex predators and the mesopredators they suppress, mesopredators appear to be equally damaging, if not more so.
In their comprehensive review of carnivore management and human food production, Baker and colleagues reported annual monetary losses due to invasive red foxes in Australia as nearly 3.
Baker and colleagues also reported that losses of juvenile cattle to golden jackals Canis aureus ; 2. The economic impacts of mesopredators should be expected to exceed those of apex predators in any scenario in which mesopredators contribute to the same or to new conflict with humans, but mesopredators occur at higher densities than apex predators and exhibit greater resiliency to control efforts.
Another reason the relative costs of top predator restoration versus mesopredator overabundance are not readily apparent is that economic impacts of mesopredator release often differ among stakeholders.
For example, persecution of dholes in Bhutan was intended to protect livestock but led to greater numbers of wild boar Sus scrofa and to resultant crop devastation that in some cases caused abandonment of agricultural fields Wangchuk Similarly, in North America, antelope hunters and sheep ranchers may appreciate the drop in coyote numbers that has accompanied the return of wolves to the intermountain west, whereas elk hunters and cattle ranchers may resent the resurgence of wolf depredation.
Interestingly, the majority of financial compensation programs to mitigate human-wildlife conflict in North America are aimed at crop farmers to offset the costs of damage caused by deer Odocoileus spp.
This consequence of historic wolf control is not often acknowledged by opponents of predator reintroduction, or even by the farmers themselves.
The relative financial losses caused by apex predators versus those caused by mesopredators and the ungulates they suppress often vary across time because of the delayed nature of release, thus making cost-benefit analyses more complex.
In cases where it may appear fiscally advantageous to extirpate apex predators and contend with mesopredator outbreaks, it is important to recognize that such disturbances can reduce the resiliency of ecosystems and lead to financial losses in the future.
In the North Atlantic Ocean, for example, overfishing led to the collapse of a valuable cod fishery, but the cod collapse relaxed top-down control of shrimp and crab populations that are even more economically profitable than cod Frank et al.
Efforts to preserve or restore apex predators may be costly, but these financial costs may well be offset by the benefits of reduced mesopredator abundance and greater ecosystem resilience.
Careful accounting of the full costs and benefits of apex predators and mesopredators will help clarify the impacts of predator management actions on ecosystems, economies, and societies.
Apex predators may be instrumental in preventing outbreaks of mesopredators and the consequent ecological, financial, and social problems, but significant roadblocks impede large carnivore conservation.
Much of their habitat is gone. They sometimes kill people. They often kill animals that people like, such as pets, livestock, and ungulates.
Direct lethal control of mesopredators by humans thus appears to be an attractive alternative to apex predator conservation.
By controlling mesopredator populations ourselves, could we avoid the costs of mesopredator overabundance, while also avoiding the costs of living with lions, wolves, tigers, bears, and sharks?
Several factors indicate that such management can be problematic. Overabundant mesopredators are often resilient to control programs because they are characterized by high densities, high rates of recruitment, and high rates of dispersal Palomares et al.
Lethal control can thus be likened to mowing a lawn, in that persecution induces vigorous growth in the mesopredator population.
Critics have argued that such control efforts must be intensive and most likely expensive to be effective, and that management options that address the disturbances underlying mesopredator overabundance would be more effective Goodrich and Buskirk Why are apex predators more effective than humans at controlling mesopredators?
Emerging studies of behavior-mediated interactions indicate that it is exceptionally difficult to replicate the full ecosystem effects of apex predation Peckarsky et al.
In a review of intraguild predation, Palomares and Caro noted that interactions between predators result not only in direct killing but also in avoidance behavior and defensive group formation.
Fear of predation can therefore have an even stronger impact on food webs than the killing itself Brown and Kotler The reintroduction of wolves to the Greater Yellowstone Ecosystem is a particularly compelling example of such behaviorally mediated interactions.
Reintroduced wolves reduced elk populations through direct killing, but the extent of the wolves' influence in the ecosystem was greatly increased because of the fear-induced shift in elk behavior.
Elk began to avoid the riparian areas they had favored in the absence of wolves and moved to safer areas.
As a result, the vegetation recovered along stream banks, sparking the recovery of beaver Castor canadensis populations Ripple and Beschta Likewise, a recent experiment in the coral reefs of the Bahamas showed that large groupers Epinephelus striatus benefit small reef fish by changing the behavior of smaller groupers Cephalopholis spp.
The smaller, fish-eating groupers spent less time foraging and more time hiding in the presence of the larger, invertebrate-eating groupers; reef fish abundance was thus higher in the presence of large groupers solely as a result of the behavioral response of smaller groupers.
These examples suggest that replicating the full suite of influences that apex predators exert on mesopredators is likely to be exceptionally challenging, if not impossible.
Since large carnivores are difficult to conserve, and humans are likely to be poor ecological replacements, perhaps mesopredators themselves could fill the role of apex predator.
This scenario commonly occurs when an apex predator is fully eradicated and the mesopredator directly below the former apex predator in the trophic hierarchy becomes a replacement figure 1.
Indeed, in a few cases, mesopredator behavior has shifted to more closely resemble the behavior of the former apex predator. For example, coyotes can form larger packs and hunt larger game in the absence of wolves Gese and Grothe If mesopredators can replace the role of apex predators, it is tempting to conclude that their ascendancy is not so problematic after all, from an ecological perspective.
However, this line of reasoning is dangerous for two reasons. When we become accustomed to successive stages of environmental degradation, an intact ecosystem can easily transform into a weedy landscape that harbors few desirable native species.
Second, mesopredator populations that increase following the removal of apex predators tend to have fundamentally different relationships with people and ecosystems.
While large carnivores generally avoid human-dominated regions, mesopredators can reach high densities in developed areas, increasing the likelihood of disease outbreaks and other conflicts between humans and wildlife.
Additionally, large predators tend to have a more restricted and carnivorous diet than mesopredators. Omnivorous mesopredators that consume agricultural plants can reach particularly high densities in modified environments, as baboons and wild boars have.
Furthermore, mesopredators should be more efficient than top predators at exploiting a shared resource, or they would not be able to successfully compete for the resource while being persecuted by the larger species Holt and Polis , Vance-Chalcraft et al.
Thus, mesopredators have the potential to exploit prey resources more thoroughly than top predators do.
The ascendancy of the coyote in North America is an excellent example of the pitfalls mentioned above. The fact that coyotes are now considered top predators throughout much of the United States illustrates the problem of shifting baselines and the promotion of mesopredators to apex status.
While coyotes may suppress some mesopredators, they display several classic mesopredator traits themselves: They have an omnivorous, opportunistic diet; tolerate close contact with humans; and flourish despite intense persecution.
Because of these traits, coyotes will never fully replace the role of the top predators that once controlled their numbers.
The dominance of coyotes across several habitats and the high cost of efforts to control them illustrate that the serial promotion of mesopredators to apex status may be a less effective means of maintaining ecosystem integrity than learning to live with true apex predators and protecting their habitat.
The question remains, however: How do we learn to live with the original apex predators? Coexistence with predators requires humans to be willing and able to modify their own behavior.
For example, in suburban areas of the United States, proper trash management and prohibition of wildlife feeding whether predators or prey reduces the likelihood of conflict with scavenging predators such as bears and coyotes Beckmann and Berger In rural areas around the world, compensating livestock owners for losses to predation is a commonly used tactic to encourage tolerance of predators.
However, these programs can be subject to fraud and provide no incentive for ranchers to take steps that reduce conflict, such as using guard animals or improving pens Baker et al.
A promising alternative program, community-run insurance, has been pioneered in Bhutan to improve coexistence among livestock owners and snow leopards Wang and Macdonald Through self-policing, this program has reduced fraud, and it uses discounted premiums and bonuses as incentives to improve animal husbandry practices Snow Leopard Trust A combination of tactics such as educational programs in urban and suburban areas, programs to reduce financial losses in rural areas, and improved habitat management will all be necessary to successfully coexist with large predators in human-modified landscapes.
To illustrate changes in the distributions of apex predators and mesopredators over time, we examined historic from the 18th and 19th centuries and current range maps for 36 species of terrestrial mammalian carnivores that occur in North America table 1.
Seven of these species can be considered apex predators—the three bear species, two large cats cougar and jaguar , the largest canid wolf , and the largest mustelid wolverine, Gulo gulo.
Although coyotes and some other carnivores now function as apex predators in many areas, for the analyses presented here, we categorized species on the basis of their historic rather than their current ecological roles.
We excluded the red wolf Canis rufus from our analysis because of the uncertainty regarding its historical distribution and taxonomic status.
Shapefiles for most range maps were the same as those used by Laliberte and Ripple in their analysis of carnivore and ungulate range contractions.
Because of the various inaccuracies associated with mapping changes in geographic ranges Laliberte and Ripple , we use these maps to examine broadscale patterns of change and caution readers against using the maps to infer fine-scale patterns.
We conducted our analyses using ArcGIS 9. Distributional changes of extant terrestrial mammalian carnivores in North America.
Historically, two to five apex predators occurred in any given location throughout North America, but today they are completely absent from most of the east-central United States and have declined in all areas except British Columbia and Alaska figure 3a—3c.
In fact, some parts of the northern prairies once harbored five apex predator species, but now there are none. In contrast, mesopredator species richness has increased in areas scattered throughout North America figure 3f.
Distributional changes of mammalian carnivores in North America. The 7 apex predator species and 26 mesopredator species used to create the maps are listed in table 1.
Historic maps for three small tropical cats [jaguarundi, ocelot, and margay] were unavailable and these species were excluded from our analyses.
Changes in species richness for apex predators c and mesopredators f were calculated by subtracting current ranges a, d from historic ranges b, e.
Historic g and current h numbers of mesopredators per apex predator were calculated by dividing historic d and current e mesopredator richness by historic a and current b apex predator richness.
Areas of complete apex predator extirpation are shown in gray b, h. Historic ranges were digitized from maps based on field sightings from the 18th and 19th centuries see Laliberte and Ripple [] for details.
We smoothed the range boundaries using a 5-kilometer mean moving-window analysis to account for uncertainty in the historic distributions. Taken together, the number of mesopredators per apex predator in North America today is far higher and more spatially variable than it used to be.
Today, there are as many as 17 mesopredators per top predator in some areas figure 3h. This dramatic change in North America's predator landscape is very likely mirrored around the world, with consequences that we are just beginning to fully understand Roemer et al.
Because the loss of apex predators may or may not cause mesopredator numbers to increase, the ability to better predict mesopredator responses to the reintroduction or removal of apex predators would greatly enhance the effectiveness of conservation and management efforts.
The occurrence of intraguild predation in food webs is the norm rather than the exception Arim and Marquet , and the unique dynamics that result from the interplay between competition and predation have sparked a rich body of theory over the past decade e.
On the basis of these theories, Brashares and colleages identified two ecosystem characteristics that should strongly influence the probability and severity of mesopredator release: ecosystem productivity and species diversity.
The impact of ecosystem productivity on relationships among predators has been well explored in theoretical studies of intraguild predation e.
In low-productivity systems, theory predicts that apex predators should often become extinct even in the absence of human influence, and mesopredators should then be regulated by the limited supply of food rather than by predation Holt and Polis In high-productivity systems, on the other hand, apex predators should have enough resources to effectively dominate and suppress the mesopredators.
These predictions have been supported by several empirical studies. Similarly, Elmhagen and Rushton found that wolves and lynx were more effective at suppressing red fox numbers in the more productive regions of Sweden over a year period.
Because regions with high productivity are often converted to agriculture, one of the most effective ways to reduce the risk of mesopredator outbreaks should be to increase the suitability of agricultural areas for large carnivores e.
While high productivity should make mesopredator release more likely if the apex predator is removed, high species diversity should have the opposite effect Brashares et al.
Removal of one apex predator from a system with many apex predators, many mesopredators, and many prey species should not have a strong effect compared with removal from a system dominated by a few species.
The dramatic changes due to predator loss that have been observed on relatively depauperate islands support this idea Terborgh et al.
Maintaining the overall diversity of an ecosystem should therefore act to buffer against severe mesopredator outbreaks. Global declines in populations of birds, fish, reptiles, rodents, and ungulates have catalyzed concerns about mesopredator release.
In fact, the primary goal of mesopredator release studies is usually the detection of these cascading effects e. In order to predict the cascading effects of apex predator removal or reintroduction on prey species, the strength and structure of the interactions among apex predators, mesopredators, and prey species must be identified.
Interactions among apex predators, mesopredators, and prey species fall into two basic structural categories: linear and triangular figure 4.
The key distinction between linear and triangular interactions is shared predation: The apex predators and mesopredators rely primarily on a shared prey item in a triangular interaction, whereas the apex predator relies on different prey in a linear interaction.
In figure 4 , the coyote-fox-bird interaction is linear: Coyotes rarely prey on birds, so there is no direct connection between these species.
In contrast, the cat-rat-bird interaction is triangular, because cats prey heavily on both rats and birds. Example of a a linear mesopredator interaction coyote-fox-bird and b a triangular mesopredator interaction cat-rat-bird.
Dotted lines in a represent the expanded food web that the linear interaction is part of. In b , X , Y , and Z represent the strengths of the interactions between species.
Because a linear interaction is basically a classic trilevel trophic cascade, predicting the effect of apex predator removal on prey appears to be straightforward: A decline in the apex predator should cause an increase in the mesopredator and a decrease in the prey.
However, placing the linear interaction within the context of the greater food web reveals much more complexity. In figure 4a , the coyote-fox-bird interaction is expanded to include other prey items eaten by coyotes and foxes.
Coyotes rely primarily on lagomorphs and rodents as prey, and foxes also eat these species. Thus, the food web contains two triangular interactions coyote-fox-rodent, coyote-fox-lagomorph in addition to the linear coyote-fox-bird focal interaction.
In a controlled experiment in Texas, removal of coyotes resulted in much higher mesopredator abundance bobcats, Lynx rufus ; skunks; gray foxes, Urocyon cinereoargenteus ; and badgers, Taxidea taxus , but the increase in mesopredators did not lead to the decreased rodent numbers that classic trophic cascade theory would predict Henke and Bryant In fact, Ord's kangaroo rat Dipodomys ordii populations increased and competitively excluded other rodents, leading to higher rodent density in areas from which coyotes were removed.
This result suggests that coyotes were more effective predators of kangaroo rats than were the mesopredators that replaced them.
Because these mesopredators tend to target other prey species such as birds, insects, and reptiles, it is possible that cascading mesopredator effects would have been detected if other prey had been monitored.
This example illustrates that the effects of apex predators and mesopredators will be best understood when placed within the larger food web Holt and Huxel All other things being equal, shared predation a triangular interaction should reduce the cascading effects of mesopredator release.
This is because the apex predator limits prey directly in a triangular interaction, and the mesopredator must therefore replace and exceed predation by the apex predator for the cascading effects of apex predator removal to become apparent.
Because mesopredators tend to be more efficient than apex predators, they may often be able to achieve these higher predation rates Vance-Chalcraft et al.
If an apex predator instead obtains its food primarily from other prey as in the case of a linear interaction , then even small increases in predation by the mesopredator following removal of the apex could be sufficient to enable detection of cascading effects.
In addition to the structure of the relationships between predators, the strengths of these relationships can aid specific predictions about the influence of apex predators on other trophic levels.
In the case of a triangular interaction, the strengths of the three paths that make up the triangle dictate the consequences of losing an apex predator.
Consider the cat-rat-bird triangular interaction in figure 4b , where X is the strength of cat control of birds, Y is the strength of cat control of rats, and Z is the strength of rat control of birds.
Assume the current populations are stable i. That is, for the bird population to increase after cats are removed, the direct suppression of birds by cats X must be greater than the combined effect of the release of rats Y and the suppression of birds by rats Z.
This model can be expanded to include bottom-up forces such as productivity, and these predictions can be tested in real systems using path analysis cf.
Elmhagen and Rushton Wildlife managers seeking to restore ecosystems would do well to determine the nature and strength of links between apex predators, mesopredators, and prey before attempting costly eradication or reintroduction programs.
The loss of apex predators as a result of persecution and habitat conversion has created outbreaks of mesopredator populations throughout the world.
The ecological release of mesopredators has negatively affected our oceans, rivers, forests, and grasslands, placing added strains on prey species that in many cases are already struggling.
As songbird populations precipitously decline and other prey populations collapse as a result of, in part, elevated predation rates, the full ecological, social, and economic implications of mesopredator release are beginning to emerge.
Restoration of apex predators to areas where they have been extirpated could do much to stem the tide of undesirable consequences of mesopredator release.
However, the daunting task of apex predator conservation will require substantial habitat restoration, greater public acceptance of large carnivores, and compromises among the people most directly affected by these predators.
Careful application of trophic theory and strategies to balance the trade-offs inherent to the management of apex and mesopredators are urgently needed; reversing and preventing mesopredator release is becoming increasingly difficult and costly as the world's top predators continue to edge toward obliteration.
We thank James A. Estes and John Terborgh for inviting J. We are grateful to the reviewers for their constructive input on earlier drafts.
Julia K. Baum, Paul Elsen, and Charles Yackulic provided valuable assistance. Amarasekare P. Coexistence of intraguild predators and prey in resourcerich environments.
Ecology 89 : — Google Scholar. Arim M Marquet PA. Intraguild predation: A widespread interaction related to species biology.
Ecology Letters 7 : — Terrestrial carnivores and human food production: Impact and management. Mammal Review 38 : — Barton BT. Cascading effects of predator removal on the ecology of sea turtle nesting beaches.
Master's thesis. University of Central Florida , Orlando. Google Preview. Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico.
Beckmann JP Berger J. Rapid ecological and behavioural changes in carnivores: The responses of black bears Ursus americanus to altered food.
Journal of Zoology : — Berger KM. Carnivore-livestock conflicts: Effects of subsidized predator control and economic correlates on the sheep industry.
Conservation Biology 20 : — Does interference competition with wolves limit the distribution and abundance of coyotes? Journal of Animal Ecology 76 : — Indirect effects and traditional trophic cascades: A test involving wolves, coyotes, and pronghorn.
Indirect effects of invasive species removal devastate World Heritage island. Journal of Applied Ecology 46 : 73 — Testing intraguild predation theory in a field system: Does numerical dominance shift along a gradient of productivity?
Ecology Letters 6 : — Brady J. Coyote advocates demand end to aerial gunning. National Public Radio. Ecological and conservation implications of mesopredator release.
Trophic Cascades. Island Press. Foraging and the ecology of fear. Foraging: Behavior and Ecology. University of Chicago Press.
Predator release of the gastropod Cyphoma gibbosum increases predation on gorgonian corals. Oecologia : — Buskirk SW.
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AVPR I RiseFor example, in suburban areas of the United States, proper trash management and prohibition of wildlife feeding whether predators or prey reduces the likelihood of conflict with scavenging predators such as bears and coyotes Beckmann and Berger In rural areas around the world, compensating livestock owners for losses to predation is a commonly used tactic to encourage tolerance of predators.
However, these programs can be subject to fraud and provide no incentive for ranchers to take steps that reduce conflict, such as using guard animals or improving pens Baker et al.
A promising alternative program, community-run insurance, has been pioneered in Bhutan to improve coexistence among livestock owners and snow leopards Wang and Macdonald Through self-policing, this program has reduced fraud, and it uses discounted premiums and bonuses as incentives to improve animal husbandry practices Snow Leopard Trust A combination of tactics such as educational programs in urban and suburban areas, programs to reduce financial losses in rural areas, and improved habitat management will all be necessary to successfully coexist with large predators in human-modified landscapes.
To illustrate changes in the distributions of apex predators and mesopredators over time, we examined historic from the 18th and 19th centuries and current range maps for 36 species of terrestrial mammalian carnivores that occur in North America table 1.
Seven of these species can be considered apex predators—the three bear species, two large cats cougar and jaguar , the largest canid wolf , and the largest mustelid wolverine, Gulo gulo.
Although coyotes and some other carnivores now function as apex predators in many areas, for the analyses presented here, we categorized species on the basis of their historic rather than their current ecological roles.
We excluded the red wolf Canis rufus from our analysis because of the uncertainty regarding its historical distribution and taxonomic status.
Shapefiles for most range maps were the same as those used by Laliberte and Ripple in their analysis of carnivore and ungulate range contractions.
Because of the various inaccuracies associated with mapping changes in geographic ranges Laliberte and Ripple , we use these maps to examine broadscale patterns of change and caution readers against using the maps to infer fine-scale patterns.
We conducted our analyses using ArcGIS 9. Distributional changes of extant terrestrial mammalian carnivores in North America. Historically, two to five apex predators occurred in any given location throughout North America, but today they are completely absent from most of the east-central United States and have declined in all areas except British Columbia and Alaska figure 3a—3c.
In fact, some parts of the northern prairies once harbored five apex predator species, but now there are none.
In contrast, mesopredator species richness has increased in areas scattered throughout North America figure 3f.
Distributional changes of mammalian carnivores in North America. The 7 apex predator species and 26 mesopredator species used to create the maps are listed in table 1.
Historic maps for three small tropical cats [jaguarundi, ocelot, and margay] were unavailable and these species were excluded from our analyses. Changes in species richness for apex predators c and mesopredators f were calculated by subtracting current ranges a, d from historic ranges b, e.
Historic g and current h numbers of mesopredators per apex predator were calculated by dividing historic d and current e mesopredator richness by historic a and current b apex predator richness.
Areas of complete apex predator extirpation are shown in gray b, h. Historic ranges were digitized from maps based on field sightings from the 18th and 19th centuries see Laliberte and Ripple [] for details.
We smoothed the range boundaries using a 5-kilometer mean moving-window analysis to account for uncertainty in the historic distributions.
Taken together, the number of mesopredators per apex predator in North America today is far higher and more spatially variable than it used to be.
Today, there are as many as 17 mesopredators per top predator in some areas figure 3h. This dramatic change in North America's predator landscape is very likely mirrored around the world, with consequences that we are just beginning to fully understand Roemer et al.
Because the loss of apex predators may or may not cause mesopredator numbers to increase, the ability to better predict mesopredator responses to the reintroduction or removal of apex predators would greatly enhance the effectiveness of conservation and management efforts.
The occurrence of intraguild predation in food webs is the norm rather than the exception Arim and Marquet , and the unique dynamics that result from the interplay between competition and predation have sparked a rich body of theory over the past decade e.
On the basis of these theories, Brashares and colleages identified two ecosystem characteristics that should strongly influence the probability and severity of mesopredator release: ecosystem productivity and species diversity.
The impact of ecosystem productivity on relationships among predators has been well explored in theoretical studies of intraguild predation e.
In low-productivity systems, theory predicts that apex predators should often become extinct even in the absence of human influence, and mesopredators should then be regulated by the limited supply of food rather than by predation Holt and Polis In high-productivity systems, on the other hand, apex predators should have enough resources to effectively dominate and suppress the mesopredators.
These predictions have been supported by several empirical studies. Similarly, Elmhagen and Rushton found that wolves and lynx were more effective at suppressing red fox numbers in the more productive regions of Sweden over a year period.
Because regions with high productivity are often converted to agriculture, one of the most effective ways to reduce the risk of mesopredator outbreaks should be to increase the suitability of agricultural areas for large carnivores e.
While high productivity should make mesopredator release more likely if the apex predator is removed, high species diversity should have the opposite effect Brashares et al.
Removal of one apex predator from a system with many apex predators, many mesopredators, and many prey species should not have a strong effect compared with removal from a system dominated by a few species.
The dramatic changes due to predator loss that have been observed on relatively depauperate islands support this idea Terborgh et al.
Maintaining the overall diversity of an ecosystem should therefore act to buffer against severe mesopredator outbreaks.
Global declines in populations of birds, fish, reptiles, rodents, and ungulates have catalyzed concerns about mesopredator release. In fact, the primary goal of mesopredator release studies is usually the detection of these cascading effects e.
In order to predict the cascading effects of apex predator removal or reintroduction on prey species, the strength and structure of the interactions among apex predators, mesopredators, and prey species must be identified.
Interactions among apex predators, mesopredators, and prey species fall into two basic structural categories: linear and triangular figure 4.
The key distinction between linear and triangular interactions is shared predation: The apex predators and mesopredators rely primarily on a shared prey item in a triangular interaction, whereas the apex predator relies on different prey in a linear interaction.
In figure 4 , the coyote-fox-bird interaction is linear: Coyotes rarely prey on birds, so there is no direct connection between these species.
In contrast, the cat-rat-bird interaction is triangular, because cats prey heavily on both rats and birds.
Example of a a linear mesopredator interaction coyote-fox-bird and b a triangular mesopredator interaction cat-rat-bird. Dotted lines in a represent the expanded food web that the linear interaction is part of.
In b , X , Y , and Z represent the strengths of the interactions between species. Because a linear interaction is basically a classic trilevel trophic cascade, predicting the effect of apex predator removal on prey appears to be straightforward: A decline in the apex predator should cause an increase in the mesopredator and a decrease in the prey.
However, placing the linear interaction within the context of the greater food web reveals much more complexity.
In figure 4a , the coyote-fox-bird interaction is expanded to include other prey items eaten by coyotes and foxes. Coyotes rely primarily on lagomorphs and rodents as prey, and foxes also eat these species.
Thus, the food web contains two triangular interactions coyote-fox-rodent, coyote-fox-lagomorph in addition to the linear coyote-fox-bird focal interaction.
In a controlled experiment in Texas, removal of coyotes resulted in much higher mesopredator abundance bobcats, Lynx rufus ; skunks; gray foxes, Urocyon cinereoargenteus ; and badgers, Taxidea taxus , but the increase in mesopredators did not lead to the decreased rodent numbers that classic trophic cascade theory would predict Henke and Bryant In fact, Ord's kangaroo rat Dipodomys ordii populations increased and competitively excluded other rodents, leading to higher rodent density in areas from which coyotes were removed.
This result suggests that coyotes were more effective predators of kangaroo rats than were the mesopredators that replaced them.
Because these mesopredators tend to target other prey species such as birds, insects, and reptiles, it is possible that cascading mesopredator effects would have been detected if other prey had been monitored.
This example illustrates that the effects of apex predators and mesopredators will be best understood when placed within the larger food web Holt and Huxel All other things being equal, shared predation a triangular interaction should reduce the cascading effects of mesopredator release.
This is because the apex predator limits prey directly in a triangular interaction, and the mesopredator must therefore replace and exceed predation by the apex predator for the cascading effects of apex predator removal to become apparent.
Because mesopredators tend to be more efficient than apex predators, they may often be able to achieve these higher predation rates Vance-Chalcraft et al.
If an apex predator instead obtains its food primarily from other prey as in the case of a linear interaction , then even small increases in predation by the mesopredator following removal of the apex could be sufficient to enable detection of cascading effects.
In addition to the structure of the relationships between predators, the strengths of these relationships can aid specific predictions about the influence of apex predators on other trophic levels.
In the case of a triangular interaction, the strengths of the three paths that make up the triangle dictate the consequences of losing an apex predator.
Consider the cat-rat-bird triangular interaction in figure 4b , where X is the strength of cat control of birds, Y is the strength of cat control of rats, and Z is the strength of rat control of birds.
Assume the current populations are stable i. That is, for the bird population to increase after cats are removed, the direct suppression of birds by cats X must be greater than the combined effect of the release of rats Y and the suppression of birds by rats Z.
This model can be expanded to include bottom-up forces such as productivity, and these predictions can be tested in real systems using path analysis cf.
Elmhagen and Rushton Wildlife managers seeking to restore ecosystems would do well to determine the nature and strength of links between apex predators, mesopredators, and prey before attempting costly eradication or reintroduction programs.
The loss of apex predators as a result of persecution and habitat conversion has created outbreaks of mesopredator populations throughout the world.
The ecological release of mesopredators has negatively affected our oceans, rivers, forests, and grasslands, placing added strains on prey species that in many cases are already struggling.
As songbird populations precipitously decline and other prey populations collapse as a result of, in part, elevated predation rates, the full ecological, social, and economic implications of mesopredator release are beginning to emerge.
Restoration of apex predators to areas where they have been extirpated could do much to stem the tide of undesirable consequences of mesopredator release.
However, the daunting task of apex predator conservation will require substantial habitat restoration, greater public acceptance of large carnivores, and compromises among the people most directly affected by these predators.
Careful application of trophic theory and strategies to balance the trade-offs inherent to the management of apex and mesopredators are urgently needed; reversing and preventing mesopredator release is becoming increasingly difficult and costly as the world's top predators continue to edge toward obliteration.
We thank James A. Estes and John Terborgh for inviting J. We are grateful to the reviewers for their constructive input on earlier drafts.
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