Laboratory Evaluation of Predator Odors for Eliciting an Avoidance Response in Roof Rats (Rattus rattus)

We evaluated eight synthetic predator odors and mongoose (Herpestes auropunctatus) feces for eliciting avoidance responses and/or reduced feeding by wild captured Hawaiian roof rats (Rattus rattus). In a bioassay arena, we recorded: (1) time until each rat entered the arena, (2) time elapsed until first eating bout, (3) time spent in each half of the arena, (4) number of eating bouts, and (5) consumption. Rats displayed a response to the predator odors in terms of increased elapsed time before initial arena entry and initial eating bout, a lower number of eating bouts, and less food consumption than in the respective control groups. The odor that produced the greatest differences in response relative to the control group was 3,3-dimethyl-1,2-dithiolane [from red fox (Vulpes vulpes) feces and mustelid anal scent gland]. Mongoose fecal odor produced different responses in four of the five variables measured while (E,Z)-2,4,5-trimethyl-³-thiazoIine (red fox feces) and 4-mercapto-4-methylpentan-2-one (red fox urine and feces) odors were different from the control group in three of the five variables measured. These laboratory responses suggest that wild Hawaiian roof rats avoid predator odors.     

Responses of Wild Norway Rats (Rattus norvegicus) to Predator Odors

If rats could be shown to avoid the odors of predators, then conservation managers could manipulate this behavior to exclude rats from important conservation sites. We evaluated the ability of six predator odors to elicit avoidance responses by wild-caught Norway rats (Rattus norvegicus) from two New Zealand populations (Kapiti Island and North Island). Kapiti Island is free of mammalian predators, while the North Island has established populations of felids, canids, and mustelids. Three of the predator odors were real and three were synthesized volatile ingredients of real animal feces or urine. We compared the rats' responses to predator odors with their responses to three natural herbivore odors. We used a Y maze, and rats were offered the choice of an odor in one arm of the maze and distilled water in the other arm. Each choice arm was ducted at the entrance to remove air and the odor. We recorded: (1) the time until the rat left the first arm of the maze, (2) the time until the rat visited each arm, (3) the number of visits to each arm, (4) the amount of time spent in each arm, and (5) a total activity score for each rat. Kapiti rats showed an aversion to five of the six predator odors, despite never having encountered them before. Kapiti rats visited herbivore odors more often than carnivore odors and were less active in the presence of carnivore odors than they were when tested with herbivore odors. In addition, Kapiti rats approached some herbivore odors more quickly than they approached carnivore odors. North Island rats appeared to avoid cat urine, but despite being predator experienced, did not show a consistent aversion to the carnivore odors we tested. Both samples of rats, but particularly the North Island group, showed high individual variation. We conclude that predator odors are unlikely to be an effective management tool for all populations of this species of rat because of this high individual variability and the likelihood that each island population will differ in its responses to a given odor.     

Exposure to Predator Odor Reduces Locomotor Activity Levels in Adult Male Rats: Lack of Effect of Hippocampal Lesion

The hippocampus has been implicated in mediating responses to predators. Involvement of the hippocampus was tested in the present study in which a multivariate analysis of the locomotor activity of intact and hippocampectomized (destruction of dentate and CA1 cells) laboratory rats, Rattus norvegicus, was conducted following exposure to a predator odor. Levels of various activity variables were monitored in an automated activity monitoring system following a brief 3-min exposure to 2-propylthietane (weasel odor), caproic acid (goat odor), toluene (organic solvent), and a no-odor condition in hippocampal-lesioned (using colchicine) and sham-operated control male rats. Rats of both groups displayed reduced levels of total distance, movement time, vertical activity, and number of movements following exposure to weasel odor and toluene in comparison to the no-odor condition. Exposure to goal odor resulted only in reduced levels of vertical activity and number of movements. There were no differences in activity levels between hippocampal-lesioned and sham-operated rats during baseline activity recording or following exposure to any of the odors. However, hippocampal-lesioned rats spent less lime in the center of the activity boxes than sham-operated control rats across all conditions. This study demonstrates that laboratory rats show marked changes in locomotion in response to the odor of a predator and suggests that an intact hippocampus is not essential for mediating these responses.     

Field Testing Synthetic Predator Odors for Roof Rats (Rattus Rattus) in Hawaiian Macadamia Nut Orchards

Field trials were conducted to determine whether the synthetic predator odors 3,3-dimethyl-l,2-dithiolane (DMDIT) and (E,Z)-2,4,5-tri-methyl-³-thiazoline (TMT) were effective at eliciting a behavioral response in wild roof rats (Rattus rattus). The study site was a Hawaiian macadamia nut (Macadamia integrifotia) orchard with a recent history of roof rat feeding damage. The synthetic predator odors were encapsulated in urethane devices secured to tree branches. Mark-recapture data from live-trapping of rats and radio telemetry location data were used to assess behavioral responses of rats to the predator odors. Mark–recapture data indicated that DMDIT and TMT had no effect on capture numbers, reproduction, or body weight of rats. There was some indication that distribution of captures and number of locations relative to treated trees in TMT areas were less than in controls, but this pattern was not significant. The predator odors had no effect on home range or median distance from center of activity (MDIS) of rats as measured by telemetry. There was a trend of increasing values of MDIS on TMT areas in session 1 but not session 2. Overall we could not detect significant differences or consistent trends in responses of rats to DMDIT or TMT in these field trials.     

Pheromone-Induced Priming of a Defensive Response in Western Flower Thrips

The Western flower thrips Frankliniella occidentalis produces conspicuous anal droplets that function as a direct defense against various predators. These droplets also function in pheromonal communication in that they contain a mixture of decyl acetate and dodecyl acetate, which acts as an alarm. Exposure of thrips to synthetic pheromone is known to promote takeoff or refuge seeking, but the effect of the natural pheromone has not yet been studied. Here, we not only studied the response to natural pheromone, but also tested the new hypothesis that the alarm pheromone primes a defensive response in thrips. This test was carried out by measuring the reaction time to a simulated predator attack after exposure to synthetic or natural alarm pheromone (against a control with no pheromone at all). The reaction was quantified in terms of the time it takes a thrips larva to produce a droplet after attack. We found that thrips larvae produce droplets of alarm pheromone faster when cues associated with danger are present. There were no significant differences in reaction times of responses to synthetic pheromone, natural pheromone, or odors from a patch with a predator attacking a thrips larva. This implies that the synthetic pheromone mimics the natural pheromone, and that other cues emanating from the predator play a minor role. We conclude that the alarm pheromone increases the vigilance of the thrips, and this may promote its survival.An erratum to this article can be found at     

Effect of predator odors on heart rate and metabolic rate of wapiti (Cervus elaphus canadensis)

We measured the heart rate (HR) and oxygen consumption ( ) of wapiti (Cervus elaphus canadensis) before, during, and after presentation of biologically irrelevant odors (pentane, thiophene, and a perfume), artificial predator odors (an ether extract of cougar feces, and PDT, a compound found in mustelid anal gland secretion), stale predator odors (dog feces and urine and fox urine, kept at ambient temperature for a few weeks), and fresh predator odors (wolf, coyote, and cougar feces and the odor of a dead coyote, kept frozen between collection and test). Overall, responses to odors were small compared to other stressful stimuli. Individual variability was high among scents and among wapiti, but two of the fresh predator odors (cougar and wolf feces) produced larger HR and responses than the other scents and were more often successful at producing responses. As a group, fresh predator odors produced larger tachycardias and elicited a larger number of significant HR responses than biologically irrelevant novel odors. although the two classes of odors did not differ in their effect on . Although several other studies have shown that ungulates have reduced feeding levels when their food is scented with predator odors, it is not clear if this is due to reduced palatability or antipredator behavior. This study is the first demonstration that a wild ungulate species reacted more strongly to predator odors than to other odors in a nonfeeding situation.     

Laboratory and field evaluation of predator odors as repellents for kiore (Rattus exulans) and ship rats (R. rattus)

Predator odors may serve to stop rats from entering conservation areas or to decrease predation, food consumption, and other damage by rats in areas tainted with predator odor. We compared the efficacy of real predator odors and synthetic odors (derived from the urine and feces of carnivores) as rat repellents with real herbivore odors as controls in a Y maze. We tested six predator odors: cat (Felis catus) urine and feces, mongoose (Herpestes auropunctatus) feces, n-propylthietane, S-methyl, methyl butanol, and isopentyl-methyl sulphide. The herbivore odors we used were: red deer (Cervus elaphus) urine, guinea pig (Cavia porcellus) feces, and white rabbit (Oryctolagus cuniculus) urine. Ship rats (Rattus rattus) and kiore or Polynesian rats (R. exulans) showed no aversion to any of the six predator odors when compared with herbivore odors. Ship rats, however, may have avoided synthesized odors more than real ones. We applied two odors (S-methyl, methyl butanol and n-propylthietane) to purpose-built feeders in native forest but recorded no change in either visitation rate or duration of visits for rodents [rats and mice (Mus musculus)] or possums (Trichosurus vulpecula). The consumption of maize at feeders was correlated with the number and duration of possum visits, but only weakly correlated with the number of visits by rodents. Consumption of maize was unaffected by the odor associated with the feeder. It is unlikely that the odors we tested will be useful in deterring rodents or possums from areas where they have been removed for economic, public health or conservation reasons.     

Why are predator urines aversive to prey?

Predator odors often repel prey species. In the present experiments, we investigated whether changes in the diet of a predator, the coyote (Canis latrans) would affect the repellency of its urine. Furthermore, because predator odors have a high sulfur content, reflecting large amounts of meat in the diet, we investigated the contribution of sulfurous odors to repellency. Our results were consistent with the hypothesis that diet composition and sulfurous metabolites of meat digestion are important for the repellency of predator odors to potential prey.     

Toluene and weasel (2-propylthietane) odors suppress feeding in the rat

The odors of toluene and 2-propylthietane have been shown to elicit fast wave bursts of 15–30 Hz in the olfactory bulb and dentate gyrus of rats. The odors of cadaverine, butyric acid, and caproic acid were found to be ineffective by comparison. The present study investigated feeding in rats offered a choice between food pellets treated with one of the above mentioned odors or untreated pellets. Unscented pellets were also presented in a control condition. The results indicate that 2-propylthietane or toluene scented food is avoided; cadaverine scented food is preferred; but caproic acid and butyric acid scents have no effect. Toluene and 2-propylthietane may activate central pathways involved in predator detection/avoidance, while cadaverine may activate pathways involved in approach and feeding behavior.     

Orientation of the fiddler crab,Uca cumulanta: responses to chemical and visual cues

Behavioral responses of the fiddler crab Uca cumulanta to flat geometric shapes mimicking natural objects were measured in a circular arena by using zonal recovery as a behavioral measurement. Crabs were tested either in presence or absence of odors from two common predator species, the blue crab Callinectes sapidus, and the pufferfish Sphoeroides testudineus. The study tested the hypothesis that U. cumulanta have different behavioral responses to visual cues in the presence of chemical cues associated with predators. Escape direction tests demonstrated that U. cumulanta is able to show zonal recovery behavior based upon astronomical references. When tested in water lacking predator odor, crabs failed to exhibit a consistent orientation if a single silhouette target was interposed in the landward direction. However, when animals were tested in different predator odor concentrations, an orientation response was obtained at 10 and 20 g/liter/hr blue crab odor and 10 g/liter/hr pufferfish odor, demonstrating U. cumulanta ability to detect the potential presence of its natural predators by this odor. Thus, the hypothesis was supported, and the results suggest that behavioral responses to chemical and visual cues are involved in predator avoidance.     

Responses of beaver (Castor canadensis Kuhl) to predator chemicals

Free-ranging beaver (Castor canadensis) in two different beaver populations in New York State were exposed to predator chemicals to test feeding inhibition. Solvent extracts of feces were applied to stem sections of aspen, the preferred food tree of beavers, permitting smelling and tasting the samples. Predator odors were from wolf (Canis lupus), coyote (Canis latrans), dog (Canis familiaris), black bear (Ursus americanus), river otter (Lutra canadensis), lynx (Lynx canadensis), and African lion (Panthera leo). The experiment was repeated. The predator odors reduced feeding compared to untreated or solvent-treated controls. One population consumed 17.0% of the samples with predator odor and 27.0% of the controls in summer, and 48.4% and 60.0%, respectively, in autumn. The other population accepted 3.15% of the predator odor samples and 11.05% of the controls in summer. Coyote, lynx, and river otter odors had the strongest effects. Diesel oil and bitter-tasting neem extract had weaker effects. Predator odors are promising as feeding repellents for beaver.     

Isolation,Identification, and Quantification of Potential Defensive Compounds in the Viceroy Butterfly and its Larval Host–Plant,Carolina Willow

The viceroy-monarch and viceroy-queen butterfly associations are classic examples of mimicry. These relationships were originally classified as Batesian, or parasitic, but were later reclassified as Müllerian, or mutalistic, based on predator bioassays. The Müllerian reclassification implies that viceroy is unpalatable because it too is chemically defended like the queen and the monarch. However, unlike the queen and the monarch, the viceroy defensive chemistry has remained uncharacterized. We demonstrate that the viceroy butterfly (Limenitis archippus, Nymphalidae) not only sequesters nonvolatile defensive compounds from its larval host-plant, the Carolina willow (Salix caroliniana, Salicaceae), but also secretes volatile defensive compounds when disturbed. We developed liquid chromatography-mass spectrometry-mass spectrometry methods to identify a set of phenolic glycosides shared between the adult viceroy butterfly and the Carolina willow, and solid phase microextraction and gas chromatography-mass spectrometry methods to identify volatile phenolic compounds released from stressed viceroy butterflies. In both approaches, all structures were characterized based on their mass spectral fragmentation patterns and confirmed with authentic standards. The phenolics we found are known to deter predator attack in other prey systems, including other willow-feeding insect species. Because these compounds have a generalized defensive function at the concentrations we described, our results are consistent with the Müllerian reclassification put forth by other researchers based on bioassay results. It seems that the viceroy butterfly possesses chemical defenses different from its monarch and queen butterfly counterparts (phenolic glycosides vs. cardiac glycosides, respectively), an unusual phenomenon in mimicry warranting future study.     

Chemically mediated associative learning: An important function in the foraging behavior ofMicroplitis croceipes (Cresson)

When experienced by contact with feces from hosts feeding on cowpeas, laboratory-reared females ofMicroplitis croceipes, a larval parasitoid ofHeliothis spp., orient and fly to odors of the same feces, whereas naive laboratory-reared females do not. Flight-tunnel studies revealed that associative learning occurs during female encounters with hosts and host products. When females antennate host feces, they learn to recognize the volatile odors associated with the feces. Females even can be conditioned to respond to novel and otherwise unattractive odors such as vanilla extract by exposure to these volatile substances in association with a water extract of the feces. They apparently link the volatile odors with a nonvolatile hostspecific recognition chemical found in the feces. The antennating stimulant, 13-methylhentriacontane, was found to be a valuable ingredient, apparently as a facilitator of the initial antennation and subsequent linkage of the volatiles to the nonvolatile host recognition cue.     

Aversive responses of white-tailed deer,Odocoileus virginianus,to predator urines

We tested whether predator odors could reduce winter browsing of woody plants by white-tailed deer (Odocoileus virginianus). Urine from bobcats (Lyra rufus) and coyotes (Canis latrans) significantly reduced browsing of Japanese yews (Taxus cuspidata), and repellency was enhanced when urine was reapplied weekly as a topical spray. Urine of cottontail rabbits (Sylvilagus floridanus) and humans did not reduce damage, suggesting that deer do not respond aversively to odors of nonpredatory mammals or occasional predators with which they lack a long evolutionary association. Bobcat and coyote urine were more effective in tests conducted with eastern hemlock (Tsuga canadensis), which is less palatable to white-tailed deer than Japanese yew. A dichloromethane extract of bobcat urine was as effective as unextracted urine in reducing damage to hemlocks. Testing of the organic components of bobcat urine, particularly the volatile components, may enable identification of the compounds responsible for the repellency we observed.     

Effect of the Presence of a Nonhost Herbivore on the Response of the Aphid Parasitoid <Emphasis Type="Italic">Diaeretiella rapae</Emphasis> to Host-infested Cabbage Plants

The vast majority of studies of plant indirect defense strategies have considered simple tritrophic systems that involve plant responses to attack by a single herbivore species. However, responses by predators and parasitoids to specific, herbivore-induced, volatile blends could be compromised when two or more different herbivores are feeding on the same plant. In Y-tube olfactometer studies, we investigated the responses of an aphid parasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae), to odors from cabbage plants infested with the peach-potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae), in both the presence and absence of a lepidopteran caterpillar, Plutella xylostella L. (Lepidoptera: Plutellidae). Female parasitoids chose aphid-infested plants over uninfested plants but did not distinguish between caterpillar-infested and uninfested plants. When given a choice between odors from an aphid-infested plant and those from a plant infested with diamondback moth larvae, they significantly chose the former. Furthermore, the parasitoids responded equally to odors from a plant infested with aphids only and those from a plant infested with both aphids and caterpillars. The results support the hypothesis that the aphid and the caterpillar induce different changes in the volatile profile of cabbage plants and that D. rapae females readily distinguish between the two. Furthermore, the changes to the plant volatile profile induced by the caterpillar damage did not hinder the responses of the parasitoid to aphid-induced signals.     

Chemical Defense in Harvestmen (Arachnida,Opiliones): Do Benzoquinone Secretions Deter Invertebrate and Vertebrate Predators?

Two alkylated 1,4-benzoquinones were identified from the defensive secretion produced by the neotropical harvestman Goniosoma longipes (Gonyleptidae). They were characterized as 2,3-dimethyl-1,4-benzoquinone and 2-ethyl-3-methyl-1,4-benzoquinone. We tested the effectiveness of these benzoquinone secretions against several predator types, including invertebrates and vertebrates. Different predators were exposed to the harvestmen's gland secretion or to distilled water in laboratory bioassays. Our results indicate that secretions containing the 1,4-benzoquinones released by G. longipes can be an effective defense against predation, and that the effectiveness of the secretion is dependent on the predator type. The scent gland secretion repelled seven ant species, two species of large wandering spiders, and one frog species, but was not an effective defense against an opossum. Our study also demonstrates that the scent gland secretion of G. longipes can work as a chemical shield preventing the approach of three large predatory ants for at least 10 min. The chemical shield may protect the harvestman against successive attacks of the same ant worker and also allow the harvestman to flee before massive ant recruitment. Our data support the suggestion that chemical defenses may increase survival with some but not all potential predators. This variation in defense effectiveness may result from many interacting factors, including the attack strategy, size, learning ability, and physiology of the predators, as well as the chemical nature of the defensive compounds, type of emission, and amount of effluent released by the prey.     

Airborne differences in odors emitted byRattus norvegicus in response to reward and nonreward

To test the hypothesis that rats (Rattus norvegicus) emit airborne, differential odors in response to reward and nonreward, donor rats received random sequences of rewarded and nonrewarded placements in small compartments and an airstream transported odors from these compartments to test rats in a separate chamber. When donors remained in the compartments during, or were removed just prior to, air transport, test rats utilized transported odors as discriminative cues signaling their own reward and nonreward for a lever-press response. When the airstream was passed through a clean compartment containing paper flooring extracted from donor compartments, test rats were not able to discriminate. Test trials to assess for control by food odors suggest that donor-produced odors, rather than food odors per se, provided the discriminative signals for test rats. Results confirm the existence of somewhat volatile, although apparently stable, odors emitted in response to reward and nonreward, and implicate a differential in amount and/or type of odor produced by donors to these two events as the source of discriminative control.     

Chemical and Olfactory Characterization of Odorous Compounds and Their Precursors in the Parotoid Gland Secretion of the Green Tree Frog, Litoria caerulea

When stressed or challenged by a predator, the Australian green tree frog, Litoria caerulea, emits a characteristic nutty odor from its parotoid glands. This study identifies the source of the odor as the cyclic amide 2-pyrrolidone (2-PyrO). In addition, we demonstrate the presence of 2-PyrO's straight chain form, -aminobutyric acid or GABA, in the frog's glandular secretion and propose an odorant–precursor relationship. What role both compounds play in the frog's defensive strategy remains unknown. Prolonged exposure to the odor is shown to result in adverse effects that may be attributed to a GABAergic mechanism. It is our hypothesis, however, that the odor acts as an aposematic signal, indicating the toxicity of the frog's nonvolatile secretion.     

The Chemical Basis of Species,Sex, and Individual Recognition Using Feces in the Domestic Cat

Scents emitted from excretions provide important information about the owner. Volatile compounds with higher levels in a species and/or sex, or that vary among individuals could be odor cues for species and/or sex, or individual recognition. However, such compounds have been identified in only a few vertebrate species. In domestic cats (Felis silvestris catus), it is known that unburied cat feces are territorial markers asserting the border of their home range, but little was known which fecal compounds are scent cues for species, sex, and individual recognition in cats. In the present study, we demonstrated the chemical basis for species, sex, and individual recognition using feces of cats. For males, major contents were fatty acids and 3-mercapto-3-methyl-1-butanol (MMB), a derivative of the unusual amino acid, felinine. MMB emission levels from feces had sex-based differences (male > female) and dynamic temporal changes during aging. Cats distinguished fecal odors with and without MMB, and different fatty acid compositions among individuals. No cat-specific compound, such as MMB, was detectable from their anal odor emitting fatty acids. We concluded that fecal MMB is a male sex recognition pheromone in cats and also provides a temporal trace of the owner. After sensing MMB, they may distinguish individual differences of conspecific feces with variable subsets of fatty acids. In contrast to scent marks, since cats can obtain species information from visual cues before sniffing conspecific anal odors, they may use their efforts to distinguish individual differences of anal odors during sniffing.     

Cover and efficacy of predator-based repellents for Townsend's voleMicrotus townsendii

Predator-based repellents have been used experimentally to control wildlife damage in both agriculture and forestry, but they have not always been effective. We examined the relative importance of cover and predator odors in forage patch selection by Townsend's vole,Microtus townsendii, and its behavior related to cover and predator cues. Experiments were conducted in which forage patch and area choices were related to available habitat alternatives. Outdoor enclosures were divided into halves: one side was treated and the other used as a control. Treatments consisting of cover, repellent, and cover plus repellent were compared to controls (no cover, no repellent). In the absence of cover, voles preferred to feed on the side without repellents. When cover was present, voles preferred to feed on the side with cover, regardless of whether or not repellents were present. Voles visited more feeding stations on the side without cover when repellents and cover were present than they visited during cover-only treatments. These additional feeding stations, visited outside of cover, were used only lightly as food sources. The amounts of oats eaten by voles decreased with increasing distance from cover. This inverse relationship had a steeper slope in coveronly treatments compared to cover plus repellent treatments. A selection model based on forage patch selection and a habitat preference hierarchy is proposed. We conclude that predator odors are effective as repellents, but their efficacy depends on habitat conditions. Managers intending to use predator-based repellents must ensure that alternative sites available to pests are better quality habitat than in areas to be protected.