Alien predators and amphibian declines: review of two decades of science and the transition to conservation

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1 Diversity and Distributions (2003) 9, SPECIAL ISSUE: AMPHIBIAN DECLINES Blackwell Publishing, Ltd Alien predators and amphibian declines: review of two decades of science and the transition to conservation LEE B. KATS* and RYAN P. FERRER Natural Science Division, Pepperdine University, Pacific Coast Highway, Malibu, CA 90263, U.S.A. Abstract. Over the last two decades, numerous studies have shown that alien predators contributed to amphibian population declines. Both experimental studies and correlative field surveys implicated alien species of fish, bullfrogs and crayfish as major contributors to amphibian population decline, and in some instances local extinction. Additional studies have demonstrated that alien predators also caused long-term changes in aquatic communities. Recent studies have examined the feasibility of removing alien predators, and provide some evidence that amphibian populations can recover. Applying information gained from past studies to the recovery of amphibian populations will be the challenge of future studies. International, national and local policies that regulate alien predators should be based largely on the body of scientific evidence already in the literature. Scientists need to be more involved with policy-makers to most effectively change laws that regulate alien predators. Key words. Amphibian decline, biological invasions, conservation, declining amphibian populations, alien predators. INTRODUCTION While many suggested causes of global amphibian declines are controversial, others have become widely accepted as contributors. Debates continue as to the role of disease and climate change as contributors to amphibian population declines, while other potential causes of population declines such as habitat loss and the spread of alien species have become generally accepted as detrimental to amphibians (Kiesecker, 2003). Fifteen years ago, the negative impact of alien predators on amphibians was still considered a theory in need of testing (Hayes & Jennings, 1986). Since then, numerous studies have implicated alien species in amphibian population declines (Tables 1 and 2). Aliens harm amphibians by competing with native species (Kiesecker, 2003), carrying disease (Kiesecker et al., 2001a; * Corresponding author Blaustein & Kiesecker, 2002), hybridizing (Riley et al., in press) or preying on amphibians. This review examines recent studies that implicated aliens as predators on amphibians, and explores the implications of the continued spread of aliens in the decline of amphibians. SOURCES OF ALIEN PREDATORS Alien species introduced from one continent to another (e.g. Stein et al., 2000), often have negative impacts on amphibians (Tables 1 and 2). Translocation of species within a continent generally has similar ecological implications. In both situations, native species lack evolutionary history with aliens, and lack of adaptations leads to population declines. Many amphibian species apparently lack prior evolutionary experience even with species functionally similar to most alien predators (Diamond & Case, 1986); consequently, amphibians are particularly vulnerable to alien predators Blackwell Publishing Ltd. 99

2 100 L. B. Kats and R. P. Ferrer Table 1 Examples of field surveys showing negative correlations between alien predators and native amphibian populations Native amphibian Alien predator Reference Hyla regilla Oncorhynchus sp. Matthews et al. (2001) Rana muscosa Salmo sp. Bradford (1989) Oncorhynchus sp. Knapp & Matthews (2000) Oncorhynchus sp. Knapp et al. (2001) Oncorhynchus sp. Bradford et al. (1993) Oncorhynchus sp. Bradford et al. (1998) Salvelinus fontinalis Salmo trutta Rana aurora Rana catesbeiana Moyle (1973) Rana catesbeiana Jennings and Hayes (1985) Rana catesbeiana Adams (1999) Rana boylii Rana catesbeiana Moyle (1973) Rana blairi Rana catesbeiana Hammerson (1982) Rana pipiens Rana catesbeiana Hammerson (1982) Litoria spenceri Oncorhynchus mykiss Gillespie (2001) Salmo trutta Litoria phyllochroa Oncorhynchus mykiss Gillespie (2001) Salmo trutta Ambystoma macrodactylum Oncorhynchus sp. Tyler et al. (1998a) Oncorhynchus sp. Funk & Dunlap (1999) Salvelinus fontinalis Taricha torosa Gambusia affinis Gamradt & Kats (1996) Procambarus clarkii Procambarus clarkii Gamradt et al. (1997) Alien predators have affected almost exclusively amphibians with complex life cycles (adult and larval stages). Amphibian eggs and aquatic larvae are particularly vulnerable to alien aquatic predators (although alien rats reportedly caused the extinction of species of New Zealand frogs, Towns & Daugherty, 1994). Alien predators are spread to new locations both intentionally and accidentally. Fish are the most widespread alien predator on amphibians (Stebbins & Cohen, 1995) and in many cases have been placed into habitats to provide game for sport fishermen (Cory, 1963; Knapp, 1996; Stein et al., 2000). For example, salmonids have been introduced throughout the world, including North America, Australia, New Zealand, Europe and Central America (Bradford et al., 1993; Brönmark & Edenhamn, 1994; Townsend, 1996; Pough et al., 1998). Mosquitofish (Gambusia) are one of the most widespread genera of vertebrates because of their effectiveness in controlling mosquito populations. Unfortunately, they eat more than mosquitoes (Miura et al., 1979; Bence, 1988) and their diet includes amphibian larvae (Webb & Joss, 1997; Goodsell & Kats, 1999). Every fish introduction for biological control that has been studied thoroughly has had negative effects on non-target species (Simberloff & Stiling, 1996). Bullfrogs (Rana catesbeiana) also have been intentionally distributed to new habitats as a human food item (Moyle, 1973; Jennings & Hayes, 1985). While bullfrogs are thought frequently to be competitors with other amphibians (Kupferberg, 1997; Kiesecker et al., 2001b), adults are generalist predators and also feed on native amphibians (Zweifel, 1955; Beringer & Johnson, 1995; Kiesecker & Blaustein, 1997). Once bullfrogs colonize a habitat they are difficult to remove, and their effects on aquatic systems are long-lasting (Bury & Luckenbach, 1976; Todd, 2001; New South Wales National Parks and Wildlife Service, 2002).

3 Table 2 Examples of the effects of alien predators on native amphibans in experimental studies Native amphibian Alien Predator Effect on native amphibian Reference Rana aurora Rana catesbeiana Reduced activity/increased refuge use/ Kiesecker & Blaustein (1997) Decreased survivorship Rana catesbeiana Reduced metamorph size and rate/survivorship/ Kiesecker & Blaustein (1998) Habitat use alteration R. catesbeiana and M. dolomieui Reduced metamorph size and rate/survivorship/ Habitat use alteration R. catesbeiana Reduced feeding activity Kiesecker et al. (2001) Gambusia affinis Tail injury/reduced metamorph size/ Lawler et al. (1999) Decreased activity Rana catesbeiana Decreased survivorship/reduced metamorph size G. affinis and R. catesbeiana Reduced metamorphosis rate Rana temporaria Pacifastacus leniusculus Tail injury Nyström et al. (2001) Oncorhynchus mykiss Reduced metamorph size and rate P. leniusculus and O. mykiss Reduced metamorph size and rate/ Decreased survivorship Hyla regilla Gambusia affinis Decreased larval survivorship Goodsell & Kats (1999) Litoria spenceri Oncorhynchus mykiss Decreased larval survivorship Gillespie (2001) Salmo trutta Decreased larval survivorship Litoria phyllochroa Oncorhynchus mykiss Decreased larval survivorship Gillespie (2001) Salmo trutta Decreased larval survivorship Bufo sp. Pacifastacus leniusculus Decreased larval survivorship Axelsson et al. (1997) Ambystoma macrodactylum Carassius auratus Decreased survivorship Monello & Wright (2001) Oncorhynchus sp. Decreased larval survivorship/ Tyler et al. (1998b) Habitat use alteration/decrease in size Ambystoma gracile Oncorhynchus sp. Decreased larval survivorship/ Tyler et al. (1998b) Habitat use alteration/decrease in size and weight Taricha torosa Procambarus clarkii Decreased egg and larval survivorship Gamradt & Kats (1996) Gambusia affinis Decreased larval survivorship Procambarus clarkii Tail injury/decreased breeding activity Gamradt et al. (1997) Impact of alien predators on amphibians 101

4 102 L. B. Kats and R. P. Ferrer Populations of alien predators also establish through accidental introductions or when people release unwanted animals into the wild. Accidental introductions would include primarily the unintended dispersal of organisms that had been stocked as game or as biocontrol agents (Kolar & Lodge, 2000). Game fish intended for lakes or ponds are presumably spread easily to other habitats during floods (e.g. Bradford, 1989). Crayfish, widespread alien predators on amphibians, are found frequently in lakes and ponds either because they are stocked intentionally as fish food or accompany stocked fish (Lodge et al., 2000). In the Santa Monica Mountains of southern California, crayfish (Procambarus clarkii) are found in relatively isolated streams where the source of crayfish colonization is often not clear (Gamradt & Kats, 1996). However, in some streams it seems likely that crayfish washed out of nearby ponds during floods. Their original source is probably an angler s bait bucket. The dumping of bait buckets is the most important vector for the introduction of alien crayfish (Ludwig & Leitch, 1996; Lodge et al., 2000). Mosquitofish also spread via similar mechanisms after being introduced for biocontrol purposes (Gamradt & Kats, 1996). While these small fish are placed typically into ephemeral pools to control mosquito larvae, floods probably sweep these fish into nearby streams, rivers or lakes. Some alien predator populations become established when organisms are released into the wild because they are no longer wanted as pets or are no longer needed in captivity. For example, goldfish (Carassius auratus) have become established in some habitats and while generally not thought of as predatory, at least one study has indicated that goldfish will eat amphibians (Monello & Wright, 2001). Clawed frogs (Xenopus spp.) are used widely in biological experiments. Populations of these animals have probably been established when people released clawed frogs that were no longer needed for their intended purpose. TYPES OF STUDIES Two types of studies have demonstrated negative effects of alien predators on amphibians. Many studies report a negative correlation in the field between the presence of alien predators and the absence of amphibians (Table 1). Experimental studies demonstrate that either amphibians do poorly (slowed growth, smaller size) in the presence of aliens or are eliminated in short-term studies because of high mortality (Table 2). The large number of convincing studies in both categories has contributed to the widely accepted knowledge that alien predators are contributing to amphibian decline. Correlative studies are based typically on field surveys, where habitats that currently have alien predators are compared to nearby, similar habitats that do not contain alien predators. These comparisons can offer great insights into our ecological understanding of invasions and subsequent impacts on amphibians (Diamond & Case, 1986). In these studies, amphibians are then scored as being present or absent and in some cases actual densities of amphibians are estimated. Studies of this type are even more useful if museum records or historical field notes indicate that amphibians were once present in habitats where they are now absent. Valuable information can be obtained from historical records even if amphibian presence/absence data only are known. Fisher & Shaffer (1996) note that museum records, even if there are only a few specimens from a site, help to establish that amphibians were once present in a habitat where they might now be absent. Gamradt & Kats (1996), for instance, in studying the impact of alien crayfish and mosquitofish (Gambusia affinis) on amphibians in the streams of southern California, relied heavily on field surveys that had been conducted roughly 20 years prior to their own (De Lisle et al., 1986). The early surveys did not estimate amphibian densities, yet they established clearly the presence of amphibian species before the introduction of alien predators. Field surveys for amphibians are heavily dependent upon sampling techniques. Today the natural history of many amphibians has been well described for species that tend to inhabit areas where aliens are a problem. Presence and absence of amphibians is relatively straightforward to document by directly counting adults, eggs or larvae. Survey of vocalizing adult frogs can also be used. If surveys occur during or immediately after breeding, most amphibian species can be detected with relative certainty (McDiarmid, 1994).

5 Impact of alien predators on amphibians 103 Experimental studies complement correlative studies. Correlative studies report the final outcome; whether amphibians can co-exist with alien predators or not. Experimental studies frequently provide the mechanisms by which alien predators eliminate amphibians (Table 2). In these studies, alien predators are placed with amphibians in either field or laboratory experiments. Proper controls then compare the success of amphibians without alien predators to amphibians with alien predators. While there has been, in general, minimal criticism of experimental studies examining alien predator impact on amphibians, a potential weakness of some experimental work was conducting experiments in environments that were overly simple (Lawler et al., 1999). They suggested that experiments that place only alien predators and amphibians together might promote the targeting of amphibians as prey by alien predators if no other organisms are part of the system. Mosquitofish, once thought to be mosquito specialists and potentially too small to feed on amphibians were not immediately accepted as alien predators on amphibians. Goodsell & Kats (1999) provided high densities of mosquito larvae in addition to frog tadpoles and demonstrated that even when mosquito larvae are provided, tadpoles are still decimated by mosquitofish within a few hours. Further, wild-caught mosquitofish had tadpoles in their stomachs, providing definitive evidence that even in the complexity of natural habitats, alien mosquitofish still eat amphibians. EFFECTS OF ALIEN PREDATORS ON AMPHIBIANS Many correlative studies have reported that alien predators have eliminated amphibians or have reduced their numbers (Table 1). As suggested previously, this occurs because native amphibians have little or no evolutionary history with alien predators (Diamond & Case, 1986; Gillespie, 2001). While many experimental studies report increased mortality of amphibians with alien predators, other studies report a more indirect impact of alien predators on amphibians (Table 2). Studies have found that amphibian larvae grow less or metamorphose at smaller sizes when they are raised with alien predators than when they are raised without them. Mechanisms for mediating these changes in growth and metamorphosis are probably the result of standard responses to predators; that is, reduced movement and reduced feeding on the part of amphibians in the presence of predators (Kats & Dill, 1998). It is now generally accepted that alien predators can drive local populations of amphibians to extinction (Bradford, 1991; Bradford et al., 1994; Gamradt & Kats, 1996; Matthews et al., 2001). Amphibian populations are now frequently absent in habitats where alien predators have become established. Surveys where alien predators and amphibians co-exist may reflect in part a more recent colonization by the aliens. Surveys in those instances might capture a snapshot of a longer process that might lead ultimately to complete elimination of amphibians by alien predators. Other amphibian populations can be reduced to such low numbers by alien predators that they will probably become isolated from other populations, and may ultimately disappear (Bradford et al., 1993; see also Fig. 1). Recent studies have addressed more complicated interactions that involve more than one alien predator and affects on amphibians. In a study looking at bullfrog and mosquitofish impacts on red-legged frog tadpoles (Lawler et al., 1999), the effects of bullfrogs were so great that they dominated the smaller effects of the mosquitofish. Only bullfrog tadpoles were used and it is not clear if the impact of the bullfrogs came from competitive effects or predation. In another study, Kiesecker & Blaustein (1998) found that the combined effects of bullfrogs (both adults and tadpoles) and smallmouth bass (Micropterus dolomieui) on red-legged frog (Rana aurora) tadpoles was far greater than when each factor was considered separately. Bullfrogs continue to spread to areas outside of North America (see for example, Stumpel, 1992), and are predicted to impact amphibians negatively in these new regions as they have in their expanded range in North America. Patterns have emerged from the studies that have implicated alien predators in causing amphibian declines. Because many of the most damaging aliens (e.g. fish, crayfish, bullfrogs) are dependent on permanent or near permanent water for their survival, amphibians that typically inhabit permanent water are frequently documented as those most impacted by the aliens. For

6 104 L. B. Kats and R. P. Ferrer Fig. 1 The possible outcomes when alien predators are introduced to native amphibian populations. example, in southern California, three species of stream-breeding amphibians inhabit the streams of the Santa Monica Mountains. California newts (Taricha torosa) and California treefrogs (Hyla cadaverina) breed only in permanent streams. Pacific treefrogs (Hyla regilla) are habitat generalists and breed in both permanent streams and temporary pools and ponds. Pacific treefrogs remain common, while both California treefrogs and California newts are becoming increasingly rare (Jennings & Hayes, 1994), in part because of the spread of alien predators in permanent streams (Stebbins, 1985; Gamradt & Kats, 1996). Pacific treefrogs are widespread along the west coast of North America and their continued success may be due in part to their ability to breed in ephemeral habitats and avoid alien predators. Some species of amphibians co-exist naturally with many of the same predators that end up distributed as aliens (Petranka, 1983). These species have evolved defence mechanisms that allow them to co-exist with predators (Kruse & Francis, 1977). Some species, while not currently coexisting with predators may have come from a phylogeny that includes defence mechanisms to many predators. Bufo tadpoles, for instance, are well known to be distasteful to predators and Bufo populations that are not found currently with predators may be preadapted to deal with alien predators if they were to colonize the habitat (Diamond & Case, 1986). In other cases, defence mechanisms that are effective against native predators are apparently unsuccessful against alien predators. Taricha contain a powerful neurotoxin that makes them unpalatable to almost all predators (Petranka, 1998), yet alien crayfish will attack even adult newts, apparently undeterred by the toxin (Gamradt et al., 1997). THE BIGGER PICTURE: ALIENS IMPACTING MORE THAN AMPHIBIANS While numerous studies have examined interactions of alien predators and amphibians, more recent studies have begun to look at the more widespread impacts of alien predators on aquatic communities. For example, a recent study extends the negative correlation between trout and frogs by looking at a third species, an aquatic garter snake that feeds primarily on frogs (Matthews et al., 2002). They found that whenever frog populations were greatly reduced or absent so were aquatic garter snakes (Thamnophis elegans). When habitats did not contain introduced trout, amphibians still existed in lakes and garter snakes were also present (Matthews et al., 2002). This confirmed an earlier observation that suggested that garter snakes might survive the disappearance of some species of amphibians, but would probably not survive if all amphibians were impacted by alien predators (Jennings et al., 1992). In addition, Bradford et al. (1998) noted

7 Impact of alien predators on amphibians 105 that alien trout not only reduced tadpoles, but they also reduced or eliminated microcrustaceans and many macroinvertebrates. Nyström et al. (2001) examined the effects of multiple-introduced predators on a littoral pond community. They found that alien crayfish and rainbow trout (Oncorhynchus mykiss) negatively impacted native common frog (Rana temporaria) tadpoles and had both direct and indirect impacts on multi-trophic levels in the community. For instance, both snail biomass and macrophyte coverage decreased with the alien predators. They found that aliens can have widespread impacts on food webs in pond communities. Ricciardi & Rasmussen (1999) developed a model that predicts that extinction rates for North American freshwater fauna will soon be five times higher than that for terrestrial fauna. There is little doubt that the spread of alien predators throughout North America has contributed to the extinction rates of freshwater fauna including amphibians (Table 1). Our understanding of amphibian population declines will help us to understand the larger picture that includes numerous freshwater taxa. Alien predators will impact freshwater fauna wherever they colonize and unfortunately, the Ricciardi & Rasmussen (1999) predictions will probably hold for habitats outside of North America as well. ALIEN PREDATOR INTRODUCTIONS: POSSIBLE ECOLOGICAL OUTCOMES The ecological outcome of new introductions of alien predators is not predictable (Fig. 1). A review of the literature provides the possible paths that systems may follow after alien introductions. Failed incidences of alien predator introductions will not be well-documented in the literature, particularly if their persistence was so short that the impact on native species were minimal. Knapp et al. (2001) were able to study alpine lakes that fell into three categories: lakes with introduced trout, lakes where trout were unable to persist and lakes that never contained introduced trout. Native mountain yellow-legged frogs (Rana muscosa), crustaceans and macroinvertebrates were greatly reduced in lakes containing fish. In lakes where fish had disappeared, the frogs and both groups of invertebrates began to increase 5 10 years after fish disappeared and converged on fishless lakes years after fish were absent. This study points out that recovery of lakes after the removal of alien species could be a slow process and might also depend on the length of time the alien predators had persisted in the habitat before they disappeared. Funk & Dunlap (1999) studied a similar situation where stocked trout disappeared from certain high elevation lakes. Long-toed salamanders (Ambystoma macrodactylum) had been eliminated from lakes with fish; however, salamanders recolonized lakes where trout had gone extinct within 20 years of fish disappearance despite the fact that dispersal in this amphibian was thought to be minimal. While amphibians have been known to recolonize or increase in numbers after alien predators either go extinct or are removed (see above), not all aquatic species recover quickly after fish removal (Drake & Naiman, 2000). Diatom assemblages in lakes (Mt Rainier National Park, Washington, U.S.A.) where trout were removed did not return to predisturbance assemblages in the years since fish removal. Diatoms are sensitive indicators of ecological conditions and this study suggests that a more thorough recovery in these aquatic communities is complex and that recovery times are often unpredictable (Drake & Naiman, 2000). Similarly, McNaught et al. (1999) found that the invertebrate community in alpine lakes recovered slowly (> 15 years) after the disappearance of stocked salmonids. Just as lack of evolutionary experience of amphibians with aliens can lead to the demise of amphibians, lack of evolutionary experience between alien predators and new habitats might deter their long-term persistence. For instance, African clawed frogs (Xenopus laevis) have colonized habitats in California, yet conditions that included prolonged drought wiped out many populations of these frogs (McCoid et al., 1993). Clawed frogs are permanently aquatic and have few adaptations for dealing with drying habitats. In our own study area, crayfish have been introduced into California as fish bait. These crayfish are native to the slow-moving streams and rivers of the south-eastern United States. In 1997, rainfall during an El Niño winter was twice the normal rainfall in southern California (Los Angeles Flood Control District) and crayfish were swept out of our study streams. Amphibians were able

8 106 L. B. Kats and R. P. Ferrer to breed successfully in those streams during the following spring (Kats, unpublished data). The following year, amphibian breeding was virtually absent because the few remaining crayfish reproduced quickly and returned to pre-el Niño densities. Waiting for natural events to remove alien predators may prove to be too late for many local amphibian populations that are currently decreasing as a result recently introduced predators, and some scientists have proposed removing alien predators aggressively as a way of restoring aquatic habitats for amphibians (see, for example, Knapp & Matthews, 1998). CONSERVATION BIOLOGY: ALIEN PREDATORS AND AMPHIBIANS Like many problems in conservation biology, solutions for dealing with alien predators will be complex. Some biologists have suggested that eliminating alien predators from habitats in which they are established is not necessarily a good idea (Hayes & Jennings, 1986). The concern is that alien predators, in particular bullfrogs, may have become enough of an important game animal that economic costs of removing them should be considered. In addition, many recreational anglers will also oppose removing alien game fish or halting the stocking of game fish. Removal of alien predators will not be met with universal support and acceptance. In some instances the removal of aliens might prove effective, while in other situations removal might be impossible. In streams in the Santa Monica Mountains, alien crayfish predators remain the primary predator on native streambreeding amphibians. These predators have many, if not most, of the general requirements that describe a successful invader (Meffe & Carroll, 1997). For example, they are habitat generalists, have broad dietary requirements and have a high reproductive potential. In addition, they are very aggressive toward other species (Gamradt et al., 1997), a behavioural component that makes them even more successful as an alien (Holway & Suarez, 1999). These predators will probably not disappear naturally and removal of these crayfish will be difficult. As mentioned previously, local populations of amphibians have disappeared since their arrival (Gamradt & Kats, 1996). Recommendations for amphibian recovery plans often call for restoring habitats to predisturbed conditions (Semlitsch, 2002); however, as has already been discussed, this might be virtually impossible in the case of some alien predators, particularly those that prove difficult to remove. In streams where crayfish invasions are recent enough that adult amphibians are still attempting to breed, we have proposed restoring sections of streams by removing crayfish from these stream sections long enough for amphibians to breed and for larvae to metamorphose. While this is not the ideal solution, partial and temporary removal of crayfish combined with occasional natural conditions that lower crayfish numbers might provide enough relief from predation to sustain amphibian populations. Clearly, the best solution would be to increase and preserve the number of aquatic habitats that are free of alien predators. This goal would be accomplished most effectively by two approaches that include more careful regulation of the spread of alien species and land management decisions that include purchasing and preserving habitats free of alien predators. Land management and preservation should consider clearly the current and potential impact of alien species (Meffe & Carroll, 1997). Because aliens are usually found in permanent water, some have suggested more emphasis on protecting ephemeral habitats for amphibians (Adams, 1999). This strategy would probably help amphibians that breed in ephemeral habitats; it does not, however, help amphibian species that, like aliens, are also dependent on more permanent water. Decisions to purchase and protect land should be influenced by current distributions of aliens and the probabilities that aliens will invade (Byers et al., 2002). Unfortunately, models do not currently exist that would help land managers predict invasion of aliens in the future. We are currently collaborating with the U.S. National Park Service and the United States Geological Survey to develop models in the Santa Monica Mountains that may allow land managers to predict future alien invasions based on current and past patterns of alien species distributions. The impact of introduced species is one of the leading causes of biodiversity loss (Meffe & Carroll, 1997), and introduced species are probably the most important anthropogenic impact on freshwater ecosystems (Olsen et al., 1991;

9 Impact of alien predators on amphibians 107 Kolar & Lodge, 2000). The direct effects of alien predators on amphibians are now well documented. We have only begun to explore the more subtle indirect impacts of alien predators on amphibians. For example, recent studies have demonstrated that multiple stressors, when combined, can impact amphibians severely (Relyea & Mills, 2001; Blaustein & Kiesecker, 2002). The role of alien predators as stressors on amphibians in conjunction with other factors has yet to be studied in detail. Clearly, more laws and policies are necessary to prevent and manage the spread of alien species (McNeely, 2000; Scoccianti, 2001). Federal laws that attempt to regulate alien species in the United States date back to 1931 and the Animal Damage Control Act. The most recent significant federal laws that attempt to control the spread of alien species are the Non-indigenous Aquatic Nuisance Prevention and Control Act (NANPCA), 1990, the National Invasive Species Act 1996 and Executive Order (for a complete list of federal laws regulating alien species see The NANPCA involves five U.S. federal agencies and was reauthorized and amended in 1996 as the National Invasive Species Act. It was expanded to include more than species spread from ship ballasts and authorized funding for research on aquatic nuisance species prevention and control. Executive Order calls for a National Invasive Species Council to produce National Management Plans for Invasive Species every two years. States were also encouraged to develop nuisance species management plans by NAN- PCA. These statewide plans led to significant changes in law. For example, because of the ecological damage caused by the spread of the rusty crayfish (Oronectes rusticus), it is now illegal to possess live crayfish while fishing in Wisconsin. Illinois now prohibits the possession and sale of rusty crayfish, and Minnesota and Michigan have similar regulations. While some states have passed laws that will protect amphibians from invasive predators, other states seem to lag behind in making policy. For example, despite several studies that have documented the negative impact of alien mosquitofish and crayfish on native California amphibians, both aliens are still legally obtained in the state. Gambusia are still being used for mosquito control and alien crayfish are still sold as fish bait throughout the state. While economic analyses have prompted effective policies against some aliens (e.g. Mediterranean fruitfly, cabbage butterfly; see Diamond, 1996), the economic costs of losing native amphibians do not appear to be prohibitive enough to always warrant policy change. Economic analyses will rarely make the case to save native amphibians, and costs (both economic and biological) associated with ecosystems damaged by the loss of amphibians and other aquatic species may arrive too late to generate effective policies. Current laws and subsequent enforcement will have to occur at all levels of government to succeed. International agreements will also be necessary to prevent further spread of species from continent to continent (McNeely, 2000). The effectiveness of these laws and policies will be dependent on public education programmes that inform people about the negative impacts of alien species. CONCLUSIONS 1. Sceptical policy makers will be most convinced of the negative impact of alien predators on amphibians when studies include both field correlations and experimental work demonstrating how aliens affect amphibians. 2. Scientists should be prepared to interact with others who do not immediately agree that aliens impact ecosystems negatively and who might argue that alien predators should not be removed. 3. In order to predict long-term success of a newly introduced alien predator, two factors need to be considered: (a) the invasion history of the alien; and (b) the level of preadaptation of the alien for the new habitat. Shortterm success of the invader can still be reversed years later by rare selection pressures (e.g. extreme weather events, prolonged drought, floods) in the new habitat. 4. Community recovery after aliens are removed can be slow. Decades after eradication communities may still not reflect preinvasion species composition. 5. When complete eradication of aliens is not possible alternatives should be considered, including management strategies that attempt to reduce aliens to low numbers to facilitate the recovery of native species.

10 108 L. B. Kats and R. P. Ferrer 6. Models should be developed to predict how sensitive habitats are to invasions by aquatic aliens. These models would be helpful to land managers when decisions are made to purchase land for preservation. 7. Since 1990, the United States federal government has increased focus on managing alien species. Federal policies have required states to develop nuisance species management plans and several states have recently changed laws to limit the spread of aliens. The most effective way that scientists can impact policy on aliens is at the state level. Scientists should work with state policy-makers to protect habitats free of aliens, restore habitats impacted by aliens and create laws and regulations that would further control the spread of aliens. ACKNOWLEDGMENTS We are grateful to C. Vos Strache, D. Swartzendruber, D. Baird, R. Buckskin, N. Watts and A. Ferrer for logistical support. This study was supported by the Seaver College Dean s Office and the Frank R. Seaver endowment. The Santa Monica Bay Restoration Project also provided funds to support this study. We are also grateful to J. Kitz of the Mountains Restoration Trust, R. Sauvajot and S. Riley of the National Park Service and R. Fisher of the U.S.G.S. REFERENCES Adams, M.J. (1999) Correlated factors in amphibian decline: exotic species and habitat change in western Washington. Journal of Wildlife Management 63, Axelsson, E., Nyström, P., Sidenmark, J. & Brönmark, C. (1997) Crayfish predation on amphibian eggs and larvae. Amphibia Reptilia 18, Bence, J.R. (1988) Indirect effects and biological control of mosquitoes by mosquitofish. Journal of Applied Ecology 25, Beringer, J. & Johnson, T.R. (1995) Rana catesbeiana (bullfrog): diet. Herpetological Review 26, 98. Blaustein, A.R. & Kiesecker, J.M. (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5, Bradford, D.F. (1989) Allopatric distribution of native frogs and introduced fishes in high Sierra Nevada lakes of California: implication of the negative effect of fish introductions. Copeia 1989, Bradford, D.F. (1991) Mass mortality and extinction in a high-elevation population of Rana muscosa. Journal of Herpetology 25, Bradford, D.F., Cooper, S.D., Jenkins, T.M. Jr, Kratz, K., Sarnelle, O. & Brown, A.D. (1998) Influences of natural acidity and introduced fish on faunal assemblages in California alpine lakes. Canadian Journal of Fisheries and Aquatic Sciences 55, Bradford, D.F., Graber, D.M. & Tabatabai, F. (1994) Population declines of the native frog, Rana muscosa, in Sequoia and Kings Canyon National Parks, California. Southwestern Naturalist 39, Bradford, D.F., Tabatabai, F. & Graber, D.M. (1993) Isolation of remaining populations of the native frog, Rana muscosa, by introduced fishes in Sequoia and Kings Canyon National Parks, California. Conservation Biology 7, Brönmark, C. & Edenhamn, P. (1994) Does the presence of fish affect the distribution of tree frogs (Hyla arborea)? Conservation Biology 8, Bury, R.B. & Luckenbach, R.A. (1976) Introduced amphibians and reptiles in California. Biological Conservation 10, Byers, J.E., Reichard, S., Randall, J.M., Parker, I.M., Smith, C.S., Lonsdale, W.M., Atkinson, A.E., Seastedt, T.R., Williamson, M., Chornesky, E. & Hayes, D. (2002) Directing research to reduce the impacts of nonindigenous species. Conservation Biology 16, Cory, L. (1963) Effects of introduced trout on the evolution of native frogs in the high Sierra Nevada Mountains. Proceedings of the International Congress of Zoology 16, 172. De Lisle, H., Cantu, G., Feldner, J., O Connor, P., Peterson, M. & Brown, P. (1986) The distribution and present status of the herpeto-fauna of the Santa Monica Mountains of Los Angeles and Ventura counties, California. Special publication no. 2. Southwestern Herpetologists Society. Diamond, J.M. (1996) A-bombs against amphibians. Nature 383, Diamond, J.M. & Case, T.J. (Eds.) (1986) Overview: introductions, extinctions, exterminations, and invasions. Community ecology. Harper & Row, New York, Drake, D.C. & Naiman, R.J. (2000) An evaluation of restoration efforts in fishless lakes stocked with exotic trout. Conservation Biology 14, Fisher, R.N. & Shaffer, H.B. (1996) The decline of amphibians in California s Great Central Valley. Conservation Biology 10, Funk, W.C. & Dunlap, W.W. (1999) Colonization of high-elevation lakes by long-toed salamanders (Ambystoma macrodactylum) after the extinction

11 Impact of alien predators on amphibians 109 of introduced trout populations. Canadian Journal of Zoology 77, Gamradt, S.C. & Kats, L.B. (1996) Effect of introduced crayfish and mosquitofish on California newts. Conservation Biology 10, Gamradt, S.C., Kats, L.B. & Anzalone, C.B. (1997) Aggression by non-native crayfish deters breeding in California newts. Conservation Biology 11, Gillespie, G.R. (2001) The role of introduced trout in the decline of the spotted tree frog (Litoria spenceri) in southeastern Australia. Biological Conservation 100, Goodsell, J.A. & Kats, L.B. (1999) Effect of introduced mosquitofish on Pacific treefrogs and the role of alternative prey. Conservation Biology 13, Hammerson, G.A. (1982) Bullfrog eliminating leopard frogs in Colorado? Herpetological Review 13, Hayes, M.P. & Jennings, M.R. (1986) Decline of Ranid frog species in Western North America: are bullfrogs (Rana catesbeiana) responsible? Journal of Herpetology 20, Holway, D.A. & Suarez, A.V. (1999) Animal behavior: an essential component of invasion biology. Trends in Ecology and Evolution 14, Jennings, W.B., Bradford, D.F. & Johnson, D.F. (1992) Dependence of the garter snake Thamnophis elegans on amphibians in the Sierra Nevada of California. Journal of Herpetology 26, Jennings, M.R. & Hayes, M.P. (1985) Pre-1900 overharvest of California red-legged frogs (Rana aurora draytonii): the inducement for bullfrog (Rana catesbeiana) introduction. Herpetologica 41, Jennings, M.R. & Hayes, M.P. (1994) Amphibian and reptile species of special concern in California. California Department of Fish and Game Inland Fisheries Division, Rancho Cordova. Kats, L.B. & Dill, D.M. (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5, Kiesecker, J.M. (2003) Invasive species as a global problem: insights towards understanding the worldwide decline of amphibians. Amphibian Conservation (ed. by Semlitsh, R.D.), pp Smithsonian Press, Washington, D.C., in press. Kiesecker, J.M. & Blaustein, A.R. (1997) Population differences in responses of red-legged frogs (Rana aurora) to introduced bullfrogs. Ecology 78, Kiesecker, J.M. & Blaustein, A.R. (1998) Effects of introduced bullfrogs and smallmouth bass on microhabitat use, growth, and survival of native red-legged frogs (Rana aurora). Conservation Biology 12, Kiesecker, J.M., Blaustein, A.R. & Miller, C.L. (2001a) The transfer of a pathogen from fish to amphibians. Conservation Biology 15, Kiesecker, J.M., Blaustein, A.R. & Miller, C.L. (2001b) Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82, Knapp, R.A. (1996) Nonnative trout in natural lakes of the Sierra Nevada: an analysis of their distribution and impacts on native aquatic biota. Sierra Nevada ecosystem project: final report to Congress, vol. III, pp Centers for Water and Wildland Resources, University of California, Davis, CA. Knapp, R.A. & Matthews, K.R. (1998) Eradication of nonnative fish by gill-netting from a small mountain lake in California. Restoration Ecology 6, Knapp, R.A. & Matthews, K.R. (2000) Non-native fish introductions and the decline of the mountain yellow-legged frog from within protected areas. Conservation Biology 14, Knapp, R.A., Matthews, K.R. & Sarnelle, O. (2001) Resistance and resilience of alpine lake fauna to fish introductions. Ecological Monographs 71, Kolar, C.S. & Lodge, D.M. (2000) Freshwater nonindigenous species: interactions with other global changes. Invasive species in a changing world (ed. by H.A. Mooney and R.J. Hobbs), pp Island Press, Washington, D.C. Kruse, K.C. & Francis, M.G. (1977) A predation deterrent in larvae of the bullfrog, Rana catesbeiana. Transactions of the American Fisheries Society 106, Kupferberg, S.J. (1997) Bullfrog (Rana catesbeiana) invasion of a California river: the role of larval competition. Ecology 78, Lawler, S.P., Dritz, D., Strange, T. & Holyoak, M. (1999) Effects of introduced mosquitofish and bullfrogs on the threatened California red-legged frog. Conservation Biology 13, Lodge, D.M., Taylor, C.A., Holdich, D.M. & Skurdal, J. (2000) Reducing impacts of exotic crayfish introductions: new policies needed. Fisheries 25, Ludwig, H.R. Jr & Leitch, J.A. (1996) Inter-basin transfer of aquatic biota via anglers bait buckets. Fisheries 21, Matthews, K.R., Knapp, R.A. & Pople, K.L. (2002) Garter snake distribution in high elevation ecosystems: is there a link with declining amphibians and nonnative trout introductions? Journal of Herpetology 36, Matthews, K.R., Pope, K.L., Preisler, H.K. & Knapp, R.A. (2001) Effects of nonnative trout on Pacific treefrogs (Hyla regilla) in the Sierra Nevada. Copeia 2001, McCoid, M.J., Pregill, G.K. & Sullivan, R.M. (1993) Possible decline of Xenopus populations in Southern California. Herpetological Review 24,

12 110 L. B. Kats and R. P. Ferrer McDiarmid, R.W. (1994) Amphibian diversity and natural history: an overview. Measuring and monitoring biological diversity: standard methods for amphibians (ed. by W.R. Heyer, M.A. Donnelly, R.W. McDiarmid, L.C. Hayek and M.S. Foster), pp Smithsonian Institution Press, Washington, D.C. McNaught, A.S., Schindler, D.W., Parker, B.R., Paul, A.J., Anderson, R.S., Donald, D.B. & Agbeti, M. (1999) Restoration of the food web of an alpine lake following fish stocking. Limnology and Oceanography 44, McNeely, J.A. (2000) The future of alien invasive species: changing social views. Invasive species in a changing world (ed. by H.A. Mooney and R.J. Hobbs), pp Island Press, Washington, D.C. Meffe, G.K. & Carroll, C.R. (1997) Principles of conservation biology. Sinauer Associates Inc. Publishers, Sunderland. Miura, T., Takahashi, R.M. & Stewart, R.J. (1979) Habitat and food selection by the mosquitofish, Gambusia affinis. Proceedings of the California Mosquito and Vector Control Association 47, Monello, R.J. & Wright, R.G. (2001) Predation by goldfish (Carassius auratus) on eggs and larvae of the eastern long-toed salamander (Ambystoma macrodactylum columbianum). Journal of Herpetology 35, Moyle, P.B. (1973) Effects of introduced bullfrogs, Rana catesbeiana, on the native frogs of the San Joaquin Valley, California. Copeia 1973, New South Wales National Parks and Wildlife Service (2002) Predation by Gambusia holbrooki: the plague minnow. Draft threat abatement plan. NPWS, Hurstville, NSW. Nyström, P., Svensson, O., Lardner, B., Brönmark, C. & Granéli, W. (2001) The influence of multiple introduced predators on a littoral pond community. Ecology 82, Olsen, M.T., Lodge, D.M., Gapelli, G.M. & Houlihan, R.J. (1991) Mechanisms of impact of an introduced crayfish (Orconectes rusticus) on littoral congeners, snails, and macrophytes. Canadian Journal of Fisheries and Aquatic Science 48, Petranka, J.W. (1983) Fish predation: a factor affecting the spatial distribution of a stream-breeding salamander. Copeia 1983, Petranka, J.W. (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, D.C. Pough, F.H., Andrews, R.H., Cadle, J.E., Crump, M.L., Savitzky, A.H. & Wells, K.D. (1998) Herpetology. Prentice Hall, New Jersey. Relyea, R.A. & Mills, N. (2001) Predator-induced stress makes the pesticide carbaryl more deadly to grey treefrog tadpoles (Hyla versicolor). Proceedings of the National Academy of Sciences USA 98, Ricciardi, A.R. & Rasmussen, J.B. (1999) Extinction rates of North American freshwater fauna. Conservation Biology 13, Riley, S.P.D., Shaffer, H.B., Voss, S.R. & Fitzpatrick, B.M. Hybridization between a rare, native tiger salamander and its introduced congener. Ecological Applications. Scoccianti, C. (2001) Amphibia: aspects of conservation ecology. Guido Persichino Graphics, Piazzo Duomo. Semlitsch, R.D. (2002) Critical elements for biologically based recovery plans of aquatic-breeding amphibians. Conservation Biology 16, Simberloff, D. & Stiling, P. (1996) How risky is biological control? Ecology 77, Stebbins, R.C. (1985) Western reptiles and amphibians. Houghton Mifflin Company, Boston. Stebbins, R.C. & Cohen, N.W. (1995) A natural history of amphibians. Princeton University Press, New Jersey. Stein, B.A., Kutner, L.S. & Adams, J.S. (2000) Precious heritage: the status of biodiversity in the United States. Oxford University Press, Oxford. Stumpel, A.H.P. (1992) Successful reproduction of introduced bullfrogs Rana catesbeiana in northwestern Europe: a potential threat to indigenous amphibians. Biological Conservation 60, Todd, K. (2001) Tinkering with Eden: a natural history of exotics in America. W. W. Norton Co., New York. Towns, D.R. & Daugherty, C.H. (1994) Patterns of range contractions and extinctions in the New Zealand herpetofauna following human colonisation. New Zealand Journal of Zoology 21, Townsend, C.R. (1996) Invasion biology and ecological impacts of brown trout Salmo trutta in New Zealand. Biological Conservation 78, Tyler, T., Liss, W.J., Ganio, L.M., Larson, G.L., Hoffman, R., Deimling, E. & Lomnicky, G. (1998b) Interaction between introduced trout and larval salamanders (Ambystoma macrodactylum) in high-elevation lakes. Conservation Biology 12, Tyler, T.J., Liss, W.J., Hoffman, R.L. & Ganio, L.M. (1998a) Experimental analysis of trout effects on survival, growth, and habitat use of two species of Ambystomatid salamanders. Journal of Herpetology 32, Webb, C. & Joss, J. (1997) Does predation by the fish Gambusia holbrooki (Atheriniformes: Poeciliidae) contribute to declining frog populations? Australian Zoologist 30, Zweifel, R.G. (1955) Ecology, distribution, and systematics of frogs of the Rana boylei group. University of California Publication Zoology 54,