Toxic Frogs Elicit Species‐Specific Responses from a Generalist

vol. 170, no. 6 the american naturalist december 2007 Natural History Note When Dinner Is Dangerous: Toxic Frogs Elicit Species-Specific Responses from a Generalist Snake Predator Ben Phillips* and Richard Shine School of Biological Sciences A08, University of Sydney, Sydney, toxins) traits. In all cases, the individual fitness benefit New South Wales 2006, Australia derived from a particular defense is straightforward: the antelope that escapes the lion lives another day and thus Submitted May 2, 2007; Accepted July 23, 2007; Electronically published October 24, 2007 has a greater chance to reproduce. Predators tend to exert asymmetrically strong selection on their prey whereby selection is strong on prey to evade capture (the prey risks its life) but selection is weak on the predator (which only risks its meal; Abrams 1986, abstract: In arms races between predators and prey, some evolved 2000; Vermeij 1994). This selective asymmetry may well tactics are unbeatable by the other player. For example, many types of prey are inedible because they have evolved chemical defenses. In become more equitable, however, when prey are dangerous this case, prey death removes any selective advantage of toxicity to (Brodie and Brodie 1999). Nevertheless, in all cases there the prey but not the selective advantage to a predator of being able is strong selection on prey to avoid predation. In this to consume the prey. In the absence of effective selection for post- article, we explore a loophole in these adaptive pathways: mortem persistence of the toxicity then, some chemical defenses a route by which predators can deal with prey defenses in probably break down rapidly after prey death. If so, predators can a way that is not opposed by selection working on the overcome the toxic defense simply by waiting for that breakdown prey. This pathway results from an asymmetry in the time before consuming the prey. Floodplain death adders (Acanthophis praelongus) are highly venomous frog-eating elapid snakes native to course over which selective forces operate on prey versus northern Australia. Some of the frogs they eat are nontoxic (Litoria predator during a predator-prey interaction. Individual se- nasuta), others produce gluelike mucus when seized by a predator lection on the prey effectively ceases when the prey animal (Limnodynastes convexiusculus), and one species (Litoria dahlii)is dies because anything that happens after that time does dangerously toxic to snakes. Both the glue and the toxin degrade not affect the animal’s fitness (excepting instances where within about 20 min of prey death. Adders deal with these prey types kin selection operates; Fisher 1930; Brodie and Brodie in different and highly stereotyped ways: they consume nontoxic frogs 1999). In contrast, the benefit to a predator from con- directly but envenomate and release the other taxa, waiting until the chemical defense loses its potency before consuming the prey. suming a prey item persists long after prey death, until other factors such as putrefaction or theft by scavengers Keywords: antipredator tactics, coevolution, evolution, predator-prey removes the nutritional benefit available from the prey. systems, prey release. Hence, we might expect that many of the antipredator tactics exhibited by prey items cease to be effective soon after the prey dies and that predators will evolve to exploit In many predator-prey systems, predators exhibit species- that fact by judicious waiting after prey death until the specific tactics that enable them to capture particular types antipredator mechanism becomes ineffective. Our data on of prey, and prey exhibit a range of antipredator tactics a generalist snake predator reveal an example of this sce- that reduce their vulnerability to predation (Edmunds nario, whereby specific predator behaviors, manifested af- 1974). Prey defenses range from behavioral (e.g., shifts in ter prey death, enable snakes to overcome the chemical diel activity patterns, enhanced vigilance) to morpholog- defenses of toxic frogs. ical (e.g., spines, tail autotomy) and physiological (e.g., First, we briefly review the conceptual basis for the * Corresponding author; e-mail: [email protected]. asymmetry posited above. In the absence of group or kin Am. Nat. 2007. Vol. 170, pp. 936–942. ᭧ 2007 by The University of Chicago. selection, there is no fitness advantage for a prey individual 0003-0147/2007/17006-42581$15.00. All rights reserved. to maintain its antipredator defenses after death. None- DOI: 10.1086/522845 theless, some antipredator mechanisms remain effective: This content downloaded from 137.111.013.200 on June 27, 2019 19:34:27 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). Species-Specific Responses to Toxic Frogs 937 for example, a porcupine’s spines are still capable of Methods wounding after the death of the porcupine. Similarly, toxic Study System and Species prey will likely remain toxic for some time postmortem. Parsimony suggests that such situations are not the result All animals were collected from the Adelaide River flood- of selection but instead are accidental flow-on effects of a plain, near Darwin in the Northern Territory. The Adelaide defensive strategy that worked in life. Nevertheless, post- River floodplain contains many snake and frog species; mortem persistence of antipredator mechanisms does ex- most snake species in the area eat frogs (Shine 1991; B. ert selection on the predator; a predator that kills or maims Phillips, unpublished data). itself on a dead prey item has had its fitness curtailed. The floodplain death adder (Acanthophis praelongus Thus, although dead prey can still exert selection on their hawkei; Wuster et al. 2005) is a dangerously venomous, predators, postmortem prey defenses will not evolve in ambush-foraging elapid snake of northern Australia. direct response to selection by predators, and thus coevo- Floodplain adders grow to a maximum size of 750 mm (mean of 99 field-capturedanimals p 460 mm, SD p lution (sensu stricto) will not proceed with regard to post- 136 mm; B. Phillips, unpublished data). Most of their diet mortem prey defenses. Therefore, predators should evolve consists of frogs, although juvenile adders feed primarily strategies to deal with these risks: if a predator can defeat on lizards, and very large death adders commonly take the defensive tactics of its live prey, it can also develop rats (Webb et al. 2005). strategies to ameliorate any postmortem danger posed by Of the prey species, one (the rocket frog Litoria nasuta) that prey, and there is no selection acting on the prey to is relatively nontoxic and relies on its prodigious leaping prevent this from happening. ability to escape predation (hence the common name). The above is true in the absence of kin selection. In The marbled frog (Limnodynastes convexiusculus) is a bur- situations where kin selection is strong (e.g., social insects), rowing species with short legs (and concomitantly low however, selection can proceed postmortem via indirect jumping ability), which secretes a gluelike substance when fitness benefits accrued by the dead individual’s close rel- irritated. Adhesive secretions are common antipredator atives. Thus, postmortem prey defenses may be selected devices in amphibians (see, e.g., Williams et al. 2000; Ki- for if they give an individual’s relatives increased fitness zirian et al. 2003) and can be devastatingly effective against by, for example, killing a predator that may have preyed snake predators (Arnold 1982; Evans and Brodie 1994). on relatives in the future. More realistically, postmortem Although the chemical basis of Lim. convexiusculus secre- prey defenses may increase predator handling time and tions is unknown, the glue dries rapidly and is difficult to give relatives time to escape. While kin selection can be remove from skin (B. Phillips and R. Shine, personal ob- invoked to explain the evolution or maintenance of post- servation), which presumably poses a risk to snakes. The mortem prey defenses, kin selection is far from ubiquitous third species (Dahl’s aquatic frog Litoria dahlii) is highly (Griffin and West 2002), and so in the absence of strong toxic to most snake species, including floodplain adders evidence suggesting its operation, the evolution of post- (Madsen and Shine 1994). The toxin is composed of active mortem prey defenses should be seen as most likely an peptides (the dahleins; Wegener et al. 2001) that strongly accidental by-product of defenses that act in life (as de- inhibit neuronal nitric oxide synthase, a molecule of major scribed in the previous paragraph). importance to intracellular communication (particularly in the circulatory and nervous systems; Pukala et al. 2006). Toxic food items provide clear examples of prey that The low antimicrobial activity of dahleins suggests that remain dangerous after death. Although toxin detectability they have a purely antipredator function (when force-fed and distastefulness may evolve in response to selection L. dahlii, most snakes died within 20 min; Madsen and from predators (Brodie and Brodie 1990; Vanhoye et al. Shine 1994). 2003; Pukala et al. 2006), there is unlikely to be selection The likelihood of kin selection is low in this system. for toxin longevity postmortem. Thus, although some prey None of our study species show parental care; all simply may remain toxic for days or months after death, others deposit offspring/eggs and have nothing further to do with may remain toxic only briefly after the prey has died. Toxin them. In the frog species there may be a temporary spatial longevity likely will depend on the chemistry of the toxin concentration of relatives around the period when tadpoles involved rather than on the toxin’s defensive role. Thus, first metamorphose, but this represents only a brief mo- a prey item that is too poisonous to eat nonetheless may ment in the life history, and there is no evidence that death become edible sometime after its death.

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