Douglas P. Chivers

Chemical alarm signalling in aquatic predator-prey systems: A review and prospectus

AbstractThe importance of chemical cues in predator-prey interactions has recently received increasing attention from ecologists. The sources of chemicals to which prey species respond often originate as cues released by the predator (reviewed by Kats and Dill, this issue). Alternatively, cues may be released by other prey animals when they detect or are attacked by a predator. Such cues, known as chemical alarm signals, are particularly common in aquatic systems. These signals provide the basis of our current review. Short-term behavioural responses of prey animals to alarm signals have received the most attention. Behavioural responses of prey resemble those exhibited to known predators, and are therefore likely to make receivers less vulnerable to predation. More recently, studies have shown that benefits to alarm signal receivers extend beyond the immediate behavioural response of nearby conspecifics over a few minutes. For example, alarm signals are important in mediating the learning of unknown pred...

THE EVOLUTION OF CHEMICAL ALARM SIGNALS: ATTRACTING PREDATORS BENEFITS ALARM SIGNAL SENDERS

A wide variety of organisms possess damage-released alarm pheromones that evoke antipredator responses in conspecifics. Understanding the evolution of such involuntary alarm signals has been perplexing because it is difficult to see direct benefits to the sender, notwithstanding benefits derived from warning relatives. Recently, it has been proposed that the alarm pheromone, or Schreckstoff, of Ostariophysan fishes may function in a fashion analogous to distress calls of many birds and mammals. The alarm pheromone may attract secondary predators to the proximity of the primary predation event, and, once there, the secondary predators may disrupt the predation event, thus allowing the prey greater opportunity to escape. Previous findings have established that the alarm pheromone of fathead minnows (Pimephales promelas) attracts predators, including northern pike (Esox lucius) to an area. In this study we demonstrate that the probability that fathead minnows will escape after being captured by a northern pike is significantly increased through interference by a second pike. Taken with the previous findings that alarm pheromone attracts predators, these results are the first to provide empirical evidence of benefits to senders of an involuntary alarm signal.

Importance of Predator Diet Cues in Responses of Larval Wood Frogs to Fish and Invertebrate Predators

We examined the effects of predator diet on the antipredator responses of larval woodfrogs (Rana sylvatica). We found that tadpoles showed stronger responses to fish (Perca flavescens) that were fed tadpoles than those fed invertebrates. Similarly, we found that tadpoles responded more strongly to larval dragonflies (Anax spp.) fed tadpoles than to dragonflies fed invertebrates. The overall intensity of response of tadpoles to fish was much stronger than that to dragonflies. Predator diet effects are not ubiquitous in predator–prey systems. We discuss possible reasons why predator diet effects are seen in some, but not all, predator–prey systems.

Shifts in Life History as a Response to Predation in Western Toads (Bufo boreas)

Larval western toads (Bufo boreas) are known to exhibit antipredator behavior in response to both chemical alarm cues released from injured conspecifics and chemical cues of predatory invertebrates. In this study, we tested whether long-term exposure to predator and alarm cues resulted in an adaptive shift in life history characteristics of the toads. We raised groups of tadpoles in the presence of: (1) predatory backswimmers (Notonecta spp.) that were fed toad tadpoles, (2) nonpredatory water boatman (Corixidae), and (3) chemical alarm cues of injured conspecifics. Tadpoles raised in the presence of both chemical alarm cues and cues of predators fed tadpoles metamorphosed in significantly shorter time than those raised in the presence of the nonpredator control. Reducing time taken to reach metamorphosis would reduce exposure to aquatic predators. There was no difference among treatments in the size at metamorphosis. Our results suggest that this shift in metamorphic characteristics may represent a facultative alteration in life history.

Avoidance response of a terrestrial salamander (Ambystoma macrodactylum) to chemical alarm cues

Organisms from a wide variety of taxonomic groups possess chemical alarm cues that are important in mediating predator avoidance. However, little is known about the presence of such alarm cues in most amphibians, and in particular terrestrial salamanders. In this study we tested whether adult long-toed salamanders (Ambystoma macrodactylum) showed an avoidance response to stimuli from injured conspecifics. Avoidance of stimuli from injured conspecifics could represent avoidance of a chemical alarm cue or, alternatively, avoidance of a territorial pheromone or conspecific predator odor. Consequently, we also tested whether salamanders avoided stimuli from noninjured conspecifics. Salamanders avoided stimuli from injured but not from noninjured conspecifics. Therefore, we concluded that the response to injured conspecifics represents avoidance of a chemical alarm cue and not avoidance of a territorial pheromone or predator cue. This is the first clear demonstration of chemical alarm signaling by a terrestrial amphibian and the first report of chemical alarm signaling in an ambystomatid salamander. By avoiding an area containing stimuli from injured conspecifics, long-toed salamanders may lower their risk of predation by avoiding areas where predators are foraging.

Sex recognition and mate choice by male western toads, Bufo boreas

In field-based choice experiments, we examined sex recognition and mate choice in male western toads, Bufo boreas. When given a simultaneous choice between a male and a female of equal size, males did not discriminate between the sexes and attempted to amplex a male or a female with equal frequency. When a test male clasped a stimulus male, the stimulus male uttered a release call that caused the test male to release the stimulus male. Male-male amplexus never lasted more than 3 s, but male-female amplexus was tenacious and prolonged. Furthermore, males discriminated between gravid females that differed in body size, choosing larger gravid females over smaller ones, but they did not discriminate between gravid females or non-gravid females of equal size. In choice tests that excluded chemical cues, males jumped more frequently towards large females than small ones. Given that females are significantly larger than males, selecting larger individuals as potential mates increases the probability that males amplex with a female. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.

DNA REPAIR AND RESISTANCE TO UV-B RADIATION IN WESTERN SPOTTED FROGS

We assessed DNA repair and resistance to solar radiation in eggs of members of the western spotted frog complex (Rana pretiosa and R. luteiventris), species whose populations are suffering severe range reductions and declines. Specifically, we measured the activity of photoreactivating enzyme (photolyase) in oocytes of spotted frogs. In some species, photoreactivation is the most important mechanism for repair of UV-damaged DNA. Using field experiments, we also compared the hatching success of spotted frog embryos at natural oviposition sites at three elevations, where some embryos were subjected to ambient levels of UV-B radiation and others were shielded from UV-B radiation. Compared with other amphibians, photolyase activities in spotted frogs were relatively high. At all sites, hatching success was unaffected by UV-B. Our data support the interpretation that amphibian embryos with relatively high levels of photolyase are more resistant to UV-B radiation than those with lower levels of photolyase. At the embryonic stage, UV-B radiation does not presently seem to be contributing to the population declines of spotted frogs.

Chemical Alarm Signaling by Reticulate Sculpins, Cottus perplexus

The distribution and extent of chemical alarm signaling systems among some families of fishes, including the Cottidae, remains unclear. In laboratory experiments, we tested whether reticulate sculpins, Cottus perplexus, respond to chemical alarm signals released by injured conspecifics. Sculpins decreased movement following exposure to skin extracts from conspecifics, but did not respond to cues of syntopic speckled dace, Rhinichthyes osculus, or allotopic swordtails, Xiphophorous helleri. Additional tests demonstrated that the responses of sculpins to alarm cues were dependent on the hunger level of the test fish. Sculpins deprived of food for 2 days failed to respond to conspecific alarm cues, however, the same individuals fed to satiation did respond to alarm cues.

CONTRASTING BEHAVIORAL RESPONSES BY DETRITIVOROUS AND PREDATORY MAYFLIES TO CHEMICALS RELEASED BY INJURED CONSPECIFICS AND THEIR PREDATORS

Larvae of the mayfly Siphlonisca are predators of the detritivorous mayfly Siphlonurus in floodplain wetlands in Maine (USA). Both mayflies are natural prey of brook trout (Salvelinus fontinalis). We exposed larvae of Siphlonurus and Siphlonisca to chemicals from injured conspecifics and their predators. Significant decreases in movement activity by Siphlonurus were elicited by chemicals released from Siphlonisca, chemicals released from brook trout fed conspecifics, and by chemicals released from injured conspecifics. A significant decrease in movement activity by Siphlonisca was elicited by chemicals released from brook trout fed either conspecifics or Siphlonurus. Movement activity by either Siphlonurus or Siphlonisca was not significantly affected by chemicals released from trout feeding on brine shrimp (Artemia). Both Siphlonurus and Siphlonisca were able to detect chemicals that provided information about past feeding behaviour by brook trout. However, their response to the chemicals used in this study was context-specific. A reduction in movement activity, a behavior that presumably reduces the probability of being consumed by visual predators, occurred only when mayflies were exposed to chemicals released by brook trout feeding on conspecific (Siphlonurus) or confamilial (Siphlonisca) prey.

Brook Charr Alevins Alter Timing of Nest Emergence in Response to Chemical Cues from Fish Predators

Brook charr (Salvelinus fontinalis) lay their eggs in gravel nests called redds. The nests are not defended for extended periods and the eggs and young may be subject to predation from predators that travel through the substrate into the redd. In this study we tested whether long-term exposure of brook charr eggs to chemical cues from predatory sculpins (Cottus cognatus) resulted in an adaptive shift in the timing of emergence of charr alevins from artificial redds. We reared brook charr eggs in the presence of chemical cues from sculpins fed brook charr eggs, sculpins fed brine shrimp, and a well water control. Significantly more alevins emerged during the first week of the emergence period when exposed to chemical cues from sculpins fed eggs than from cues from sculpins fed brine shrimp or from well water. Alevins that emerged sooner were smaller and possessed larger yolk sacs than alevins that emerged later in the emergence period. Our results suggest that alevins that emerge sooner may escape predation in the redd, but may pay a cost in being under-developed upon emergence into the open water of the stream or lake.