Population differences in responses of red-legged frogs to introduced bullfrogs - Rana aurora

Ecology, Sept, 1997 by Joseph M. Kiesecker, Andrew R. Blaustein

INTRODUCTION

There are numerous examples of losses of native species after the introduction of exotic predators (e.g., Elton 1958, Morton 1990, Lodge 1993). Naive, native prey animals may be susceptible to predation by introduced predators because of their inability to recognize new predators and to execute antipredatory behaviors (Maloney and McLean 1995). Population declines of many ranid frogs native to the western United States have been reported by several workers (e.g., Hayes and Jennings 1986, Blaustein and Wake 1990, Blaustein 1994). Although there are many possible factors contributing to ranid declines, several studies have documented the decline of native ranid frogs after the introduction of bullfrogs (e.g., Moyle 1973, Bury and Luckenbach 1976, Bury et al. 1980, Nussbaum et al. 1983, Blaustein and Wake 1990, Blaustein 1994). However, these studies only suggest a negative association between bullfrogs and other frog species. Few studies have attempted to examine the mechanisms by which introduced bullfrogs may impact ranid frogs (but see Kupferberg 1995). The recent listing by the U.S. Fish and Wildlife Service (Federal Register 1996) of Rana aurora draytonii, a subspecies of the red-legged frog, as "threatened" emphasizes the importance of understanding the impacts of introduced predators on native red-legged frogs.

Failure of a prey animal to recognize and respond to a predator increases the likelihood that it will be captured during an interaction with a predator. However, a prey animal will waste time and energy that could be used for other activities, such as feeding and reproduction, if it exhibits antipredator behaviors upon encountering a nonpredator (Milinski 1986, Werner and Hall 1988, Lima and Dill 1990). Many prey animals respond only to predators with which they have prior experience (Kats et al. 1988, Mathis et al. 1993, Chivers and Smith 1994). As predators expand their ranges or are introduced into areas outside their historical geographic ranges, they may interact with prey animals that are unfamiliar with them. Thus, naive prey may not exhibit antipredator behaviors when exposed to new predators. The ability to recognize predators may have both a genetic (Curio 1975, Mueller and Parker 1980, Hobson et al. 1988, Riechert and Hedrick 1990) and a learned basis (Curio et al. 1978, Conover 1987, Thornhill 1989, Chivers and Smith 1994). The time it takes for prey animals to acquire antipredator behaviors in response to a novel predator may indicate the impact that the new predator can have on populations of these prey (Maloney and McLean 1995). Once the behavior has been acquired, the speed with which it spreads within a population may be indicative of the intensity of predation pressure by the new predator.

Adult bullfrogs (Rana catesbeiana) are highly aquatic predators that are known to feed on a wide variety of invertebrate and vertebrate prey, including other amphibians (Bury and Whelan 1986, Beringer and Johnson 1995, Werner et al. 1995). Larval bullfrogs in Oregon typically take 1-3 years to reach metamorphosis (Nussbaum et al. 1983). Thus, the larvae of native species of frogs such as R. aurora are exposed to larger, older bullfrog tadpoles. Both tadpoles and adults of R. catesbeiana are known to prey on tadpoles of other species (e.g., Ehrlich 1979, Bury and Whelan 1986, Werner et al. 1995), although the extent to which this occurs and the factors that may influence its occurrence, are unknown.

Eight populations of the red-legged frog, R. aurora, were studied to examine responses of predator-naive tadpoles to a new predator (the bullfrog, R. catesbeiana) and to assess if any of the populations have acquired antipredator behaviors since the introduction of bullfrogs into Oregon in the early 1930s (Nussbaum et al. 1983). Four of the populations studied are allotopic with R. catesbeiana and, thus, have no prior experience with bullfrogs. The other four R. aurora populations are syntopic with R. catesbeiana and have had exposure to bullfrogs for [less than or equal to] 60 yr (Nussbaum et al. 1983). To assess differences between populations, we first compared the response of R. aurora larvae from syntopic and allotopic populations to chemical cues of R. catesbeiana. Second, we compared predation rates and survivorship between syntopic and allotopic R. aurora in the presence of R. catesbeiana adults and tadpoles. We also assessed factors that may influence predation of R. aurora by larval R. catesbeiana.

METHODS AND MATERIALS

Collection and maintenance

Red-legged frog eggs were collected from four populations that are syntopic (hereafter S1, S2, S3, and S4) and four populations that are allotopic (hereafter A1, A2, A3, and A4) with bullfrogs (sites are located in Benton, Douglas, Lane, Lincoln, Linn, and Tillamook Counties, Oregon, United States). Eggs were transported to our laboratory for rearing and testing. Syntopic Rana aurora were collected from ponds that had a breeding population of R. catesbeiana present. Thus, larval R. aurora from syntopic populations had been exposed to both larval and adult forms of R. catesbeiana. Allotopic R. aurora were collected from counties (Lincoln and Tillamook) where R. catesbeiana does not occur (Nussbaum et al. 1983). Thus, these allotopic R. aurora had no prior exposure to R. catesbeiana. Bullfrog tadpoles and adults were collected from the E.E. Wilson Wildlife Refuge (Benton County, Oregon, United States), a site where R. aurora historically occurred but is no longer found.