Predator avoidance salamanders

In their predator avoidance, salamanders use complex odors that combine chemicals from both predator and prey. In the laboratory, red-backed salamanders, P. cinereus, avoid filter papers soaked with water extracts from garter snakes that had been preying on salamanders, while earthworm-fed snakes lacked this effect. Exudations from unfed snakes and extracts from homogenized salamanders had no such alarming effect (Madison etal, 2002). 

Cupp, P. V., Jr. (1988). Avoidance of predators by salamanders through the detection of chemical odors. American Zoologist 28,156A. 

The red eft stage of the red-spotted newt contains toxic, bad-tasting chemicals in its skin. As a result, many potential predators learn to avoid this animal, and will not eat red efts. The range of the red salamander Pseudotriton ruber) overlaps part of the larger range of the red-spotted newt in the eastern United States. It appears that the superficially similar but non-toxic red salamander may be a mimic of the color of the red eft, taking advantage of the fact that many predators avoid this animal as food. 

Madison, D. M Maerz, J. C., and Mcdaiby, J. H., 1999b, Optimization of predator avoidance by salamanders using chemical cues diet and diel effects. Ethology 105 1073-1086. 

Hileman, K. S., and Brodie, E. D., Jr., 1994, Survival strategies of the salamander Desmognathus ochropihaeus interaction of predator avoidance and anti-predator mechanisms, Anim. Behav. 47 1-6. 

Our data best support the predator avoidance hypothesis, because this hypothesis cannot be rejected, and the other hypotheses can be devalued or rejected based on the available evidence. The interspecific competitor avoidance hypothesis, a potential explanation in the trials involving spotted salamanders, is rejected because the large size difference between the salamander species would result in very little resource competition (Burton Likens, 1975), and the behavior of spotted salamanders toward red-backed salamanders resembles predatory attack and includes the consumption of red-backed salamanders (Ducey, et al., 1994). 

Holomuzki, J. R. 1986. Predator avoidance and diel patterns of microhabitat use by larval tiger salamanders. Ecology, 67, 737-748. 

A non-toxic species of salamander may derive protection from predators by visually resembling a toxic form so closely that predators cannot distinguish between them Batesian mimicry). Free-ranging birds avoid both the toxic red eft Notophthalmus viridescens) and the similar-looking non-toxic red morph of the red-backed salamander Plethodon cinereus). The red-striped morph of P. cinereus, which does not resemble the red eft, is eaten (Brodie and Brodie, 1980). 

Predators learn to avoid distasteful salamanders. When molested, spotted salamanders Ambystoma maculatum) discharge a white slime, mostly in the tail region. They also raise and wag their tail when a predator is near. In one experiment, four out of five chickens learned to avoid these salamanders by sight after... 

The results of our field trials, expressed as a reduction in activity and a tendency to remain beneath rock refuges when exposed to aversive chemical cues (Sullivan at al., 2002), confirm the diet discrimination seen in the laboratory. However, the cues that elicited this discrimination in the field were unexpected. In the field, salamanders did not respond to TSeb in the early night trial (despite laboratory avoidance), and did not respond to either TSpc or TSa late at night. We hypothesize that cues from invertebrate prey were abundant in the field, but not in the laboratory, so salamanders may have disregarded all except the most threatening predator stimuli. The activity of the invertebrate prey consumed by red-backed salamander tends to be highest in the leaf litter... 

Red-backed salamanders Plethodon cinereus) respond to distilled water rinses of garter snakes (Thamnophis sirtalis) that have recently attacked other red-backed salamanders (Madison et al., 2002). These anti-predator behaviors consist of avoidance (Madison et al., 1999a Mcdarby et al., 1999) and altered activity (Madison et al., 1999a), and have been documented in the laboratory and in the field (Sullivan et al., 2002). The responses persist for up to 36 hours in laboratory trials, but no longer than 3 hours in the field (Sullivan et al., 2002). Whether the attenuated response in the field is due to a diminishing of the cue or to field-based shifts in salamander behavior remains unclear. 

CHEMOSENSORY AVOIDANCE OF PREDATORS BY RED-BACKED SALAMANDERS, PLETHODON CINEREVS... 

Amphibians are vulnerable to predation and show diverse predator defenses. We hypothesized that the common red-backed salamander should try to evade two common terrestrial predators, the garter snake and the spotted salamander, by avoiding locations containing their scent. When given a choice of clean substrates or those soiled by these predators, the red-backed salamander avoided the soiled substrates. To test whether they avoided the waste products and not the predator scent, we gave test subjects a choice between substrates soiled by predators and those soiled by red-backed salamanders. Salamanders pref-ered conspecific substrates to predator substrates, and in combination with other findings, our data show that red-backed salamanders probably reduce the likelihood of predation by avoiding locations with the chemical traces of predators. 

Three substrate comparisons were conducted to test whether red-backed salamanders avoid the odors of spotted salamanders (1) a comparison between a blank substrate and a substrate soiled by a spotted salamander, (2) a comparison between a blank substrate and a substrate soiled by the test salamander s odor, and (3) a comparison between substrates soiled by a spotted salamander and the test salamander. The second and third comparisons were attempts to control for a possible aversion to amphibian waste products unrelated to possible predator effects. Each comparison was repeated three times, 10 red-backed salamanders per replicate, giving a sample size of 30 for each comparison. 

Three major explanations have been given for the avoidance response we observed in red-backed salamanders the avoidance of predator odors (Roudebush Taylor, 1987 Brodie, et al., 1991), the avoidance of interspecific competitor odors (Ducey, et al., 1994),... 

The alarm substance hypothesis cannot be excluded in our trials, but it can be rejected based on other studies. We have shown that red-backed salamanders do not avoid substrate traces from red-backed salamanders that have been induced to autotomize their own tail (a stress-induced, anti-predator response Arnold, 1988 Lancaster Wise, 1996), and other red-backed salamanders even attempt to eat the autotomized tails (Madison, unpublished). In addition, the broken skin of sacrificed red-backed salamanders fails to negate the chemosensory avoidance of substrates from garter snakes that had been fed red-backed salamanders (McDarby, 1997). 

The intraspecific competitor avoidance response can be excluded in the trials involving both predators. The spotted salamanders did not have diets that included red-backed salamanders, so pheromones of red-backed salamanders could not have elicited the avoidance observed. The garter snake trials included one comparison that specifically control-... 

In summary, we believe our experiments indicate that red-backed salamanders identify and avoid chemical substances deposited by spotted salamanders and garter snakes, and since the latter two species are either known or probable predators of red-backed salamanders, we believe the avoidance response is an anti-predator mechanism that decreases predation risk. 

Cupp, P.V., Jr. 1994. Salamanders avoid chemicals cues from predators. Anim. Behav., 48, 232—235. 

McDarby, J.H. 1997. Chemosensory avoidance of predators by the red-backed salamander, Plethodon cinereus. M. A. Thesis, State University of New York, Binghamton, N. Y. 

Essentially all animals experience the threat of predation at some point in their life history (Lima Dill, 1990), and selection seems to favor either avoidance mechanisms that reduce the likelihood of contact or anti-predator mechanisms that reduce predator success after contact has occurred (Sih, 1985 Brodie, Formanowicz Brodie, 1991). Avoidance behavior can vary from elevated activity that is associated with seeking locations of comparative safety ( flight response) to inhibited activity that is associated with natural concealment or death feigning ( freeze response). Species (sea urchins, fishes) may show one or the other of these responses corresponding to their natural history (Parker Shulman, 1986 Smith, 1992, 1997), but some species (salamanders, snails) may shift between response types depending on the ecological context (Sih Kats, 1991 Turner, 1994, 1996). These studies indicate that the avoidance of a stimulus may appear to dissociate from (vary independently of) activity level. Thus an animal s activity level may reveal important information about the fine-tuning of behavioral avoidance in the natural context. 

The lower activity levels at night during the goldfish-fed snake trials were probably normal, low-level activity rather than freeze responses. The latter term implies immobility and certainly a reduction in activity below normal levels, which in the absence of a significant avoidance response was unlikely to have occurred. Some of the salamanders in our study may have momentarily shifted into an anti-predator defense mode upon initial exposure to snake odors, but quickly shifted back into an avoidance mode once contact with the predator appeared less imminent. This ambivalence in some salamanders may also have contributed to the 18 minute delay to peak activity. 

The partial dissociation of avoidance and activity in P. cinereus was unexpected. It appeared to be the result of avoidance being a threshold response to predation risk, whereas activity was a graded response to such a risk. But it was unclear why activity should continue to increase during the day after avoidance had reached maximum values. More extreme avoidance scores should logically have occurred during the day, especially in the highest-threat (salamander-diet) trials. 

One explanation for the partial dissociation observed and why avoidance scores were not more extreme during the day is that confinement in the test dishes could have forced the more active salamanders to cross between samples at such a rate that side avoidance was abolished. If a single rushed response from each salamander was the basis for the preference score, a dilution or cancellation effect could have occurred for some salamanders. However, since salamanders in our study had many opportunities to correct for crossings onto snake substrates, and since only 11 out of 20 positions on the water side were needed to count as an avoidance of snake substrate, any tendency to avoid substances on this substrate should have been expressed. In addition, the movements that occurred were not rushed, as in an escape ( anti-predator ) response, but slower deliberate actions with pauses and head movements typical of chemosensory investigation (reviewed by Jaeger, 1986). Thus, we conclude that space restrictions in the petri dishes did not abolish avoidance among the more active salamanders. 

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