Invited Paper HOW DO PREY PERSIST?

WILLIAM J. MATTER,1 School of Natural Resources, University of Arizona, Tucson, AZ 85721, USA R. WILLIAM MANNAN, School of Natural Resources, University of Arizona, Tucson, AZ 85721, USA

Abstract: Understanding predatorprey relations is critical for management and conservation of species. Common descriptions of predatorprey dynamics often imply that low population density of prey, prey switching by predators, and high fecundity or productivity of prey are important in allowing prey species to coexist with predators. Studies of the effects of introduced predators on prey species do not support the idea that low prey density, switching by predators, and fecundity of prey are vital to coexistence of predator and prey. More likely, prey have a suite of morphological and behavior adaptations, including uses of specific habitat features, that render some individuals far less vulnerable to predation and allow predators and prey to coexist. Management activities designed to maintain desired prey species should include maintaining or enhancing features of habitat that reduce prey vulnerability.

JOURNAL OF WILDLIFE MANAGEMENT 69(4):13151320; 2005

Key words: coexistence, extinction, habitat, introduced species, predation, predatorprey relations, prey switching, refugia.

Predation is a major ecological force influencing population dynamics, species distributions, and community structure (Kerfoot and Sih 1987:viii). The most obvious, direct effect of predation is the killing of prey, but a variety of indirect effects of predators on behavior and life histories of prey, and on dynamics at other trophic levels, have been recognized (Kerfoot and Sih 1987, Crawley 1992, Werner and Anholt 1996). Understanding predatorprey relations is critical for management and conservation of species and species complexes, and it relies in part on understanding the ecological and evolutionary processes at work. We suggest that, at times, there is confusion about the link between evolutionarily selected features of prey and the persistence of prey species over ecological time. We reached this conclusion largely from common descriptions of how prey species are able to coexist with predators that have obvious adaptations to find, pursue, capture, and consume prey. We agree that morphological and behavioral features of prey animals (e.g., coloration, burrowing, nocturnal activity pattern, escape behavior, speed) reduce the likelihood of predation; however, we disagree with the notion that prey populations ultimately are protected from predator-caused extinction by the following: (1) low population density (i.e., as predators remove individual prey, prey become increasingly rare, the rate of encounter decreases, and this leads to diminishing returns to predators, who eventually die or give up the search and leave the area); (2) prey switching by predators
1

E-mail: wmatter@ag.arizona.edu

(i.e., predators switch to alternate prey so hunting pressure on the original prey is lessened); and (3) high fecundity or productivity (i.e., the reproductive output of prey exceeds the consumptive capacity of predators). These ideas are rarely presented in such a straightforward manner; rather, they often are implied in verbal and mathematical expressions of predatorprey interactions in ecology textbooks (e.g., Ricklefs 1990, Krebs 1994, Smith 1996). Consider the following passage (Begon et al. 1996:374): Predators increase in abundance when there are large numbers of prey. But this leads to an increased predation pressure on the prey, and thus to a decrease in prey abundance. This then leads to a food shortage for predators and a decrease in predator abundance, which leads to a relaxation of predation pressure and an increase in prey abundance, which leads to an increase in predator abundance, and so on []. Such descriptions of population dynamics treat predators and prey like molecules, where encounter rates of predator and prey are almost solely a product of their abundances (Gotelli 1998:126-127). The implication of this view is that when prey reach low densities, relative rarity protects remaining individuals from loss to predators. Begon et al. (1996:337) explain the roles of rarity and switching to predatorprey relations: The preferences of many consumers are fixed [] But many others switch their preference, such that food items are eaten disproportionately often when they are common and are disproportionately ignored when they are rare. This implies that not only is prey rarity important in

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protecting prey from local extirpation but also that this protection is accentuated if alternate prey are available. Ricklefs (2001:357) describes a similar result from switching: [S]witching to alternative sources of food when prey are scarce may reduce pressure on prey. In Ricklefs view, rarity of one prey species triggers switching to alternative prey, and once switching occurs, reduced hunting pressure on the original prey protects the population from continued losses, especially if predators develop a search image for alternate prey (Ricklefs 1990:422, Begon et al. 1996:338). The role of reproductive output of prey in reducing chances of extirpation may be overemphasized when ecologists focus on simple predatorprey models (e.g., Lotka-Volterra models) that rely almost exclusively on the abundance and population growth rates of predator and prey. For example, Ricklefs (2001:354) draws from Lotka-Volterra models that, If the reproductive rate of the prey (r) were to increase, [...] the prey population would be able to bear the burden of a larger predator population [...]. This implies that reproductive rate is somehow key to reducing the negative effects of predation enough, we presume, to block extirpation of prey by predators. Below, we explore how these concepts are inconsistent with empirical data and an evolutionary view of how prey persist despite predation. We first review studies of the effects of 2 introduced predators on prey species. We assume that changes to prey populations soon after modern introductions of nonnative predators were probably similar to changes that occurred when a predator species first crossed geographic barriers in the past. Potential outcomes of any predator introduction include the extinction of some prey species and the persistence of others. We focus on how some prey species persisted whereas others did not, rather than on the impact of predators on the distribution or abundance of prey. We found that studies of naturally occurring predatorprey complexes were of less help in understanding why some prey persisted and others did not because predatorprey complexes today consist only of species able to coexist; naturally occurring predators rarely cause extinctions of coevolved prey.

after World War II. By the 1960s, all birds were eliminated from the southern 1/3 of the island, and by 1996 only 3 of 12 native forest bird species persisted in the wild (Rodda et al. 1997). Of 12 native lizards, 6 were extirpated, and 3 were localized and rare (Rodda et al. 1997). Although concurrent introductions of lizards and mammals to Guam complicate assessment of the causes for extinction of some native species, predation by brown tree snakes almost certainly is responsible for the extirpation of most bird species, 2 of 3 native species of bats, and several species of lizards (Rodda and Fritts 1992, Rodda et al. 1997). Some species, although eaten by brown tree snakes, have survived despite the spread of snakes.

Nile Perch
Nile perch (Lates niloticus) were introduced to Lake Victoria in east-central Africa in the 1950s and exploded in abundance by the early 1980s (Goldschmidt et al. 1993). Within a decade, about 200 endemic species of haplochromine cichlid fishes were extirpated, and the abundance and distribution of many other fish species were reduced. Some fish species that inhabited littoral areas, especially areas with rocky substrate, were impacted less (Seehausen et al. 1997), and some native species even increased in abundance (Seehausen et al. 1997). Predation by Nile perch is not the only recent change in the lake ecosystem, but there is general agreement that predation is the primary cause of extinction for many, if not most, cichlids outside of littoral areas (Goldschmidt et al. 1993, Seehausen et al. 1997).

ARE PREY PROTECTED BY THEIR RARITY?

The following reasoning is commonly used to account for the persistence of prey: (1) predators encounter and consume prey frequently when prey are abundant, (2) survival and recruitment of predators is high in this food-rich setting, (3) numbers of prey decline as a consequence of predation, (4) predators encounter fewer prey because prey are less abundant, (5) before the prey species is eliminated, predators die or leave the area, and (6) numbers of prey are able to recover because of low predatory pressure. This logic, however, is not consistent with empirical data on the impact of Nile perch and brown tree snakes. Over 200 fish species in Lake Victoria and many species of birds and lizards on Guam must have become increasingly rare as

CASE STUDIES Brown Tree Snakes

Brown tree snakes (Boiga irregularis) probably were transported accidentally to the island of Guam in the western Pacific Ocean sometime

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they approached extinction, but they were not protected from extirpation by their rarity. Alternatively, some native species in Lake Victoria and on Guam persisted despite being subject to predation by introduced species, but no researchers have suggested that the rarity of these native survivors has been key to their persistence. Many other extinctions of prey caused by introduced predators (Atkinson 1989, Diamond 1989, Lever 1994) indicate that rarity is not effective protection from predators. One could argue that these case studies focus on predators and prey that did not share an evolutionary history. However, study of the impact of introduced predators illustrates a weakness of the prey-rarity argument; rarity is not an adaptation. If protection of prey from predation rests primarily on low density, persistence of prey relies primarily on chance. This idea presumes that rarity of prey is the primary mechanism that reduces the chance of encounter and capture by predators sufficiently to block eventual capture of all prey. If rarity was adequate protection, there would not have been strong selection for obvious adaptive features (e.g., coloration, burrowing, activity patterns, escape behavior, speed) known to thwart predators. Biologists studying the impact of brown tree snakes and Nile perch have begun to identify why some native species persist despite predation by introduced predators (Rodda et al. 1997, Seehausen et al. 1997). Survivors have combinations of features (e.g., association with cover or other protective environmental conditions, body size, escape behavior and speed, timing of daily activity) that make individuals in certain environmental settings far less vulnerable to predation. Surviving species probably had these features for reasons unrelated to predation, or certainly unrelated to predation by Nile perch or brown tree snakes, so they might be considered pre-adaptations or exaptations (Gould and Vrba 1982). Currently, these features make it possible for certain prey to persist despite the actions of novel predators. Similarly, we expect prey that coevolved with particular predators have a variety of antipredator features (i.e., combinations of behavior, morphology, and habitat use) that are essential for persistence of prey. In sites with many refuges or ideal escape terrain, prey may be relatively abundant, yet most individuals may have low vulnerability to predation. We conclude that rarity of prey does not contribute significantly to persistence of prey in the face of predation.

ARE PREY PROTECTED BY PREDATORS SWITCHING TO ALTERNATE PREY?

Predators are thought to foster persistence of prey by switching to alternate prey species (Ricklefs 1990:422, Begon et al. 1996:338). Specifically, as abundance of a particular prey species declines, often due to predation, predators encounter fewer individuals, so they switch to alternate, more abundant prey. This switch, along with development of a search image for alternate prey, reduces predatory pressure and risk of extinction for the original prey species. We examined this claim with data from Lake Victoria and Guam. Brown tree snakes certainly switched among a variety of alternate prey (e.g., birds, lizards, mammals), and Nile perch preyed on over 200 species of fish, but switching was not sufficient to protect an extraordinary number of species from extinction. In fact, predator abundance was sustained by switching to numerous alternative prey. Switching, like rarity, is equivalent to relying on chance as the mechanism that protects prey from extinction. That is, the presence of alternate prey, in combination with the relative rarity of the original prey, must reduce the chance of encounter and capture by predators sufficiently to block eventual capture of all individuals of the original prey. Most, if not all, modern extinctions of prey by introduced predators occurred despite the presence of alternate prey (e.g., Diamond 1989, Rodda and Fritts 1992, Lever 1994), indicating that switching was not effective protection from predation. In natural settings with more than one prey species, predators often may be more likely to remove the most vulnerable individuals (e.g., individuals in poor nutritional state or without protective shelter) of a preferred prey species (Begon et al. 1996:327-328). If this is true, eventually, most remaining individuals will be relatively invulnerable primarily because they have access to refuges or escape terrain or because they are less susceptible to predation because of their age or nutritional state. Predators will have lower rates of capture and be forced to switch to alternate prey that are more available (i.e., vulnerable). Viewed in this way, predator switching is not a mechanism resulting in persistence of prey species, rather, switching is imposed on predators by the relative invulnerability of prey remaining after capture of the most vulnerable individuals. If all individuals in a population are vulnerable to predators, predators eventually will capture them all (as in Lake Victoria and on Guam), especially

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if large numbers of predators are sustained by the availability of alternate prey (Murdoch and Bence 1987, Rodda and Fritts 1992). Similarly, Buehler and Keith (1982) speculated that snowshoe hare (Lepus americanus) were subject to more consistent, high levels of predation in the southern part of their range where the abundance of predators was sustained by opportunities to switch among a variety of prey species in comparison to the northern part of the range with fewer alternative prey. We conclude that the presence of alternative prey likely contributes to the maintenance of predatory pressure, not its diminution.

ARE PREY PROTECTED BY THEIR REPRODUCTIVE OUTPUT?

Undoubtedly, the reproductive potential of species is honed by natural selection; reproductive strategies (e.g., along the r-K continuum) are part of evolved life histories. But, we believe that it is an overstatement to claim that the reproductive output of prey is one of the primary adaptations for persistence in the face of predation. We use a simple thought experiment to illustrate. Imagine an island that has 2 species of flightless, ground-nesting birds, where 1 species lays 3 eggs per clutch, once each year, and the other lays 6 eggs per clutch, twice each year. This difference in reproductive output will not significantly alter the ability of domestic cats or an introduced species of snake to drive both prey species to extinction if all individuals produced are vulnerable to predation at some point in their lives. To persist, in this example, a bird species must have a combination of behavior, habitat, and morphology that protects some individuals in all life stages from predators (e.g., if some adult birds, eggs, and nestlings are difficult for snakes to detect or if selected habitat occurs in areas avoided by snakes). A species with these features would persist even if it had the lowest fecundity among all potential prey. Relying on fecundity as an antipredator mechanism is tantamount to relying on chance (i.e., production of many young must increase the chance that some will not be eaten). Studies of species extirpated by introduced predators (e.g., brown tree snakes and Nile perch) show that all individual prey produced, no matter the number, are doomed if they do not have adaptations and habitat conditions that prevent predation of some individuals. There is no evidence that species extirpated by brown tree snakes and Nile perch tended to be

the least fecund or that survivors tended to be the most fecund. We are not arguing that fecundity and reproductive strategies are unimportant to prey survival; they have been selected strongly, as made clear in r/K-selection theory (Ricklefs 1990:577, Smith 1996:448450). However, high reproductive potential likely is not selected primarily as an antipredator feature. Rather, high reproductive potential likely has been selected because of unpredictable availability of resources or stochastic forces of mortality suffered even by adapted individuals (Ricklefs 1990:577, Smith 1996:448450). Biologists may mistake the strategy of swamping, where most young of a population are produced at about the same time, as an example of prey being protected by their reproductive output. However, the adaptive significance of swamping rests more on synchrony of birth or hatching of young (Taylor 1984:7980) than on the number of young produced by each individual. Swamping can be an effective strategy for a prey population, regardless of the fecundity of individuals, as long as most young are produced in a brief time period (i.e., a brief period of vulnerability), and this flush of young allows some individuals to grow to invulnerable life stages or to move to areas with protective cover (Ims 1990). For example, some deer and some mayflies exhibit synchronous birth or hatching of young, even though a female deer has 12 young and a female mayfly has hundreds. Some minimum number of reproducing adults may be required for swamping to be effective, just as herding or schooling probably require a minimum number of animals to be effective antipredator tactics; however, existence of a minimum population size is not evidence that per capita reproductive output is key to persistence of a prey species.

EVOLUTION OF PREDATOR AND PREY

The possible outcomes for a single prey species after introduction of a novel predator include: (1) Extinction of preythe geographic range of the new predator encompasses the range of a prey, and no individuals have features that reduce their vulnerability to predation sufficiently to result in coexistence. Without alternate prey, the predator also may be extirpated. (2) Restriction of range of preythe geographic range of the new predator partially overlaps the range of a prey that lacks antipredator features; the predator eliminates prey from the area of overlap but not in areas outside of the predators range. (3)

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Preadaptation, selection, coexistence, and coevolution of predator and preysome individuals of a prey species already have features that render these prey less vulnerable to the new predator. Individual prey without these features are killed quickly (i.e., selection against individuals without antipredator features). Generally, only prey species with such preadaptations (Gould and Vrba 1982) will be able to coexist with a novel predator long enough to undergo the coevolutionary arms race or escalation (Vermeij 1994) that results from further fine-tuned adaptation of predators and prey to each other. The first 2 scenarios are common following modern introductions of nonnative predators including many mammals, snakes, and a variety of fish and invertebrates (Courtney and Stauffer 1984, Atkinson 1989, Diamond 1989, Lever 1994, Simberloff 1995) and do not result in coexistence. The third scenario results in coexistence of predator and prey because prey species have a combination of behavior, morphology, and physiology that, together with specific habitat conditions, precluded extinction by rendering some individuals far less vulnerable to predation. We do not mean that predation has no probabilistic features. For example, the capture of a particular prey organism by a predator may involve several probabilistic events or conditions, and every individual prey has some chance of being killed by a predator. But the inability of predators to capture all individuals of a population of prey is largely the consequence of specific adaptations that greatly reduce the likelihood of predation of individuals that are in prime condition and occupy sites where these adaptations are most effective.

CONCLUSIONS AND MANAGEMENT IMPLICATIONS

Ecologists have documented many predatormediated extinctions of prey in cases where a predator was newly introduced (as on Guam and in Lake Victoria), or where coevolved species were placed in environments that lacked a habitat feature required for escape and avoidance adaptations of prey to be effective (Murdoch and Bence 1987). However, a striking feature of many natural animal communities is that some predators and prey have coexisted for long periods (i.e., thousands to tens-of-thousands of years) when both were in the core of their ranges. Any description of the evolutionary relationship between predator and prey must account for such prolonged coexistence.

After modern introductions of nonnative predators, some prey persisted despite being killed by introduced predators. Examination of why some species persisted should help in understanding coevolved, predatorprey relationships and the consequences of species introductions in the future. We see little support for the idea that when prey become relatively rare, their vulnerability to predators is reduced significantly by virtue of rarity per se. Also, if all individual prey are vulnerable to predators, the prey species will not persist regardless of opportunities for prey switching. Alternatively, if some individual prey are relatively invulnerable to predators, the prey species will persist even if there are no alternate prey. Finally, the role of reproductive output in protecting prey from extinction is more subtle and indirect than often assumed. If reproductive potential is high but all individuals produced are vulnerable to predation (e.g., because of a lack of protective cover), the prey species will likely be eliminated. However, if prey have adaptations to find and defend areas needed for hiding or escape but suffer reduced reproductive potential (e.g., because primary productivity is low in areas with the best cover), the prey species probably will persist, even if only in low numbers. Further research is likely to reveal that prey persist in nature because of a variety of morphological and behavioral adaptations, including specific uses of habitat, not as a result of rarity or fecundity of prey or the presence of alternate prey. If this is true, management activities intended to influence predatorprey relations are restricted to modifying habitat conditions because little can be done (at least in the short term) to affect behavioral or morphological adaptations. Therefore, activities designed to maintain desired prey species should include maintaining or enhancing features of habitat that reduce prey vulnerability. In situations where habitat features play a significant role in allowing prey to coexist with predators, controlling the number of predators as a technique for maintaining a prey species, if necessary at all, should be viewed only as an interim strategy until required habitat conditions are present.

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