Avoidance of predator odors

Laboratory and domestic animals may be poor models for avoidance of predator odors. For example, in one experiment, chickpeas were painted with the sulfur compounds w-propyldithiolane and w-propylthiolane from stoat anal gland secretion and 2,4,5-trimethylthiazoline (Fig. 3.1, p. 37) from fox feces. The chickpeas were planted and wild mice and house mice were tested to see if they would dig up and eat the peas. Wild mice remembered the predator odors better after odor exposure for 1 or 4 weeks and, consequently, may be better than laboratory mice at risk assessment (Coulston etal, 1993). 

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),... 

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

We will examine whether a diurnal rodent, the gray squirrel (Sciurus carolinensis) avoids predator odors and whether this avoidance is specific to certain predator species that pose more of a threat than others. This experiment arose from our course Chemical Ecology of Vertebrates during the autumn of 2000. Surprisingly, we could not find published studies of predator odor effects on squirrels. Dr. Frank Resell, then a student in the course, undertook this experiment as his individual research project and extended it after the end of the course for a publication (Rosell 2001). 

Response to food can be used as an indirect measure of prey response to predator scents. Stimuli can be placed either directly on the food or in close proximity to the food. For example, choice-tests were used to assess the avoidance of lion fecal odors by rabbits (Boag Mlotkiewicz 1994) and deer (Abbot et al. 1990). In both cases, subjects were offered a choice between treated and untreated pelleted food and relative intake was taken to reflect avoidance. Likewise, arena tests have been used to demonstrate that domestic livestock will investigate but reduce their ingestion of feed in the presence of predator odors (Pfister et al. 1990). Odors also can be applied to natural forage to assess whether target species avoid the treated plants (Sullivan et al. 1988 Calder Gorman 1991). Epple et al. (1995) monitored caching behavior to assess the response of mountain beaver to food resources associated with predator odors. 

An example for stimulus generalization are responses of rats to stress-inducing odors. Laboratoiy rats of the Wistar strain respond to predator odors, specifically mercapto compounds in fox droppings, with stress reactions, for example avoidance behavior such as freezing and increased plasma corticosterone concentrations (Vemet-Mauiy et ah, 1984). The rats were trained to avoid water scented with a mercapto odorant that contained both a keto- and a sulfhydryl group (4-mercapto-4-methyl-2-pentanone). As the animals licked a waterspout, a mild electric shock was applied to their tongue. When different compounds were tested thereafter, the rats avoided compounds with similar... 

The mosquitofish, Gamhusiapatruelis, avoids its predators, the chain pickerel, Esox niger, and redfin pickerel, Esox americanus, by swimming to the upper water levels. It also responds to odor from the pickerel mucus coat. This odor survives passage through filter paper and hours of bubbling but loses activity if heated or passed over charcoal (George, 1960). 

Fish avoid more vigorously the odor of predators that have fed on members of their species than that of those on different diets. For example, young Arctic chart avoid water from brown trout fed on Arctic chart and are less wary of that from pellet-fed trout (Hirvonen et ah, 2000). Prey fish also reduce their predator inspection behavior vis-a-vis predators that have eaten members of their own species. For instance, finescale dace, Phoxinus neogaeus, dash toward predators such as yellow perch, Percaflavescens, and withdraw. Dace inspect perch models less often if the model is accompanied by water from perch that had eaten dace than if accompanied hy water from perch on a swordtail, Xiphophorus hdleri, diet. Dace produce alarm pheromone, while swordtails do not. The Central American swordtails do not cooccur with finescale dace (Brown etal, 2001). 

This first of two experiments on predator odor avoidance deals with nocturnal burrowing mammals. The second will involve day-active mammals, such as squirrels (see Chap. 5). 

The predator scents typically used in experiments are urine, extracts of feces, scent gland products, or combinations of these. Behavioral responses of small mammal to predator odor stimuli range from vigilance to avoiding the site, and feeding inhibition. We can test squirrels responses to odors of an arboreal predator (cat), a ground predator (fox), and to humans (in most areas harmless pedestrians, but in others they are squirrel hunters), and compare them with their behavior toward odors of a nondangerous herbivore, such as deer or cattle. 

The chemicals that indicate an increased risk of predation can come from several sources. Perhaps the most widespread are chemicals released by physical damage to a conspecific crustacean. Almost every species tested has shown an increase in behavior patterns that can be related to predation avoidance when odors of crushed conspecifics are presented. There is no indication of crustaceans having specialized cells such as the epidermal club cells (the previously purported source of alarm odor in the narrow sense) found in ostariophysan fish (Smith 1989,1992). But rather some chemical or chemicals, very probably including peptides, found in the hemolymph seem implicated as the cue in crustaceans (Rittschof et al. 1992 Rittschof 1993 Rittschof and Cohen 2004 Acquistapace et al. 2005), as well as in... 

Several fish and crustacean species use chemical alarm cues to avoid predators. The odors are either released by damaged conspecifics or in the feces by the predator preying on the fish or crustacean species (e.g. Ferrari et al. 2007 Hazlett, Chap. 18). Detection of predators is under strong selection as it is important for prey to be able to detect, avoid the predator and assess the risk of being in a certain environment. 

Because the odor of cat urine was not known to our animals before the experimental exposure, one could assume that the response to the predator urine odor has a strong innate basis. This suggestion corresponds with some observations showing that the avoidance reaction to predator odors is innate rather than learned (Miiller-Schwarze, 1972 Gorman, 1984 Merkens, Harestad Sullivan, 1991 Caldera Gorman, 1991 Epple, Maison, Nolte Campbell, 1993 Heth Todrank, 1995 Sullivan et al., 1988a, b). 

Many organisms rely on anti-predator defenses after contact with a predator (Brodie, Formanowicz Brodie, 1991). Because energetic costs and mortality risks are increased during contact, some species avoid these interactions whenever possible. A number of animals chemically detect and avoid predators, including invertebrates (Parker Shulman, 1986 Alexander Covich, 1991 Turner, 1996), fish (Keefe, 1992 Smith, 1992 Mathis Smith, 1993), reptiles (Thoen, Bauwens Verheyen, 1986 Dial, 1989 Cooper, 1990), and mammals (Weldon, 1990). In anuran amphibians, tadpoles commonly avoid the waterborne odors of predators (Petranka, Kats Sih, 1987 Flowers Graves, 1997 Kie-secker, Chi vers Blaustein, 1997), and among caudate amphibians, both larval and adult... 

Small rodents depend on detection of a predator prior to actual contact. Thus, voles are sensitive to the scent of potential predators and respond to such odors without the necessity for other cues. In the wild, field voles Microtus agrestis) have been observed to avoid traps tainted with either weasel (Mustela nivalis) anal gland secretion or red fox (Vulpes vulpes) feces (Dickman Doncaster, 1984 Stoddart, 1976). Similarly, meadow and montane voles (M pennsylvanicus and M. montanus) were observed to avoid traps treated with the principal odiferous component of fox feces, 2,5-dihydro-2,4,5-trimethyl thiazoline (Sullivan, Crump Sullivan, 1988). The laboratory experiments discussed in the present chapter provided a quantitative assessment of locomotor activity levels following exposure to predator odor in laboratory-bred meadow voles. 

When compared with a water control, mice avoided the nest box containing fox fecal odor, spending less time in the box and visiting it less frequently. They also avoided the area surrounding the nest box. When the data obtained from the fox odor and rabbit odor trials was compared, the aversive response to fox odor appeared to be retained. The red fox (Vulpes vulpes) appears to be an opportunistic predator of house mice. MacDonald (1980) has shown that paths used by foxes are marked with urine and feces relative to their frequency of use, hence avoidance of fox feces by house mice may reduce the likelihood of mice being predated. Correspondingly, the odor of fox feces inside nest boxes resulted in a strong avoidance response by house mice when compared with both water and with rabbit fecal odor. 

Two possible sources of repellents from animals are the odors associated with mammalian carnivores and aggressive conspecifics. Rats actively avoid predator odors and this response appears to be innate. Trimethyl thiazoline extracted from fox (Vulpes vulpes) faeces caused an enclosed population of wild rats to alter their activities (Vemet-Maury, Constant Chanel, 1992). In the short-term, which may mean days or weeks, habituation to these predator odors appears to be slow. However, the odors may require reinforcement by some form of encounter with the predator itself to be effective in the longer-term (Muller-Schwarze, 1994). 

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