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.     

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.     

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.     

Foraging Behavior and Microhabitat Use by Spiny Mice, Acomys cahirinus and A. russatus, in the Presence of Blanford's Fox (Vulpes cana) Odor

We investigated the responses of common and golden spiny mice (Acomys cahirinus and A. russatus, respectively) to the fecal odor of Blanford's fox (Vulpes cana), a predator of Acomys, which overlaps in habitat use with the mice. Neither species of mouse showed a significant response to the presence of fox odor compared with the presence of the fecal odor of a local herbivore (Nubian ibex, Capra ibex nubia). One explanation is that the impact of predation from V. cana may be sufficiently low that the cost of avoidance, in terms of missed feeding opportunities, conveys little selective advantage. Alternatively, fecal odor may not provide a focused cue of immediate danger for spiny mice. The diurnal A. russatus showed a stronger (near significant) response than the nocturnal A. cahirinus to fecal odor of this nocturnal predator. This may be a legacy of the underlying nocturnal activity rhythm of A. russatus or may indicate a generally more cautious response to predator odors, as A. russatus has a much stronger preference for sheltered microhabitats than A. cahirinus.     

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.     

Exposure to Urine of Canids and Felids, but not of Herbivores, Induces Defensive Behavior in Laboratory Rats

Predator odors induce defensive behavior in many prey species. For various reasons, studies carried out up to now have been unable to establish whether predator odor recognition is innate or not. Mostly, only particular odors or wild-living (i.e., experienced) test animals have been used in these studies, restricting the conclusiveness of the observations. In the present study, the behavioral effects of exposure to different predator odors on predator odor-naive laboratory male rats were compared with the effects of different nonpredator odors and of a no-odor control stimulus. Results show that exposure to urine of canids and felids, but not of herbivores or conspecifics, induce defensive behaviors. Taken together, the study provides support for the hypothesis that there is an innate recognition of predator odors in laboratory rats.     

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.     

Role of prey odor in food recognition by rock crabs,Cancer irroratus say

Rock crabs,Cancer irroratus, respond to food odors in low concentration as measured by changes in antennular flicking rate. The responses of rock crabs to prey odor were tested in the presence and absence of visual cues to determine the role of chemical cues in prey recognition. Crabs were attracted to the source of mussel odor introduced into one arm of a Y maze. Natural and artificial prey shells and resin boxes were presented to crabs with and without the presence of mussel extract. The crabs were able to see, handle, and manipulate these objects. Crabs opened and consumed contents that emitted chemosensory cues and ignored identical objects that did not. Rock crabs were attracted to food odors and are capable of utilizing chemical cues to detect, locate, and identify food items.     

Behavioral responses ofLittoraria irrorata (SAY) to water-borne odors

Behavioral responses of the gastropod molluscLittoraria (=Littorina)irrorata indicate that it can discriminate among environmental odors. Snails were assayed for responses to 11 odors from plants and animals potentially representing food, shelter, location in the environment, and predators. Crushed conspecifics were included as an alarm odor. Except for odor of crushed conspecifics, all odor sources were water-borne from living intact organisms. Behavioral responses were categorized as no response, positive response, or negative response. For some analyses, negative responses were subdivided into withdrawing and turning responses. Snails responded positively to several plant odors. They did not respond to odors of intact conspecifics, fiddler crabs, or grass shrimp. They responded negatively to odors of a plant found at the upper limit of their minimal habitat, predatory blue crabs, crushed conspecifics, predatory gastropods, and ribbed mussels. Odors of blue crabs on different diets affect the type of negative response the snails display.     

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.     

Effect of experience with pine (Pituophis melanoleucus) and king (Lampropeltis getulus) snake odors on Y-maze behavior of pine snake hatchlings

The abilities of hatchling pine snakes (Pituophis melanoleucus) and king snakes (Lampropeltis getulus) to discriminate the chemical trails of pine and king snakes was investigated inY-maze experiments. Pine snakes were housed for 17 days either with shavings impregnated with pine snake odor, king snake odor, or no odor to test for the effect of experience on choice. Both pine and king snake hatchlings entered the arm with the pine snake odor and did not enter the arm with the king snake odor. The data support the hypothesis that hatchlings of both species can distinguish conspecific odors from other odors and that our manipulation of previous experience was without effect for pine snake hatchlings.     

Acquired Predator Recognition by Fathead Minnows: Influence of Habitat Characteristics on Survival

In this study we conditioned fathead minnows (Pimephales promelas) to recognize the odor of a perch (Perca flavescens) by exposing them to perch odor coupled with minnow alarm cue. We then staged encounters between the predator and prey in order to assess whether the predator odor training had any effect on survival of the prey. We tested for a survival effect in the presence and absence of shelter. Our results indicate that fish trained with alarm signals to recognize predators gained a survival benefit during staged encounters with a predator and that habitat characteristics influenced the survival of conditioned fish.     

Recognition of Dominance Status By Chemoreception in the Red Swamp Crayfish, Procambarus clarkii

We tested the hypothesis that chemical signals play a role in the recognition of dominance status in the red swamp crayfish, Procambarus clarkii. Dominance was judged on the outcome of dyadic interactions in all male or female groups of three individuals. This resulted in a dominant, intermediate, and subordinate individual within each population. A choice paradigm in a flow-through Y maze was used to judge whether crayfish were able to recognize dominance through chemical cues alone. Both individuals that interacted with the animal producing the odor and naive individuals were tested. Irrespective of sex and previous experience, individuals increased their rates of locomotion in the presence of conspecific odor. Naive males investigated the dominant arm first, spent more time at the dominant nozzle, and responded more aggressively (as measured by meral spread) to dominant male odor and subordinate female odor. Intermediate males spent more time at the dominant male nozzle and responded more aggressively to dominant male odor. Naive females spent more time at the dominant nozzle. These results show that males recognize dominant animals. Since both naive and experienced males respond to water from dominant animals, we concluded that this is recognition of dominance and not just individual recognition. This signal may be important for the formation or reinforcement of dominance relationships. Based on the change in behavior between odors, we suggest that crayfish can use chemical cues to recognize the dominance status of conspecifics.     

Trirhabda canadensis (Coleoptera: Chrysomelidae) responses to plant odors

The responses of the goldenrod leaf beetleTrirhabda canadensis to host and nonhost volatile odors were tested in a Y-tube olfactometer in the laboratory. Beetles preferred host to nonhost odors and were sensitive to concentrations of host odor. Beetles distinguished between host and nonhost volatiles of only one of the two nonhostSolidago species; host volatiles were preferred to all nonhost volatiles at the family and order levels. In other words, all nonhosts above the genus level had similar effects on beetle responses. Although the odors of most nonhosts were neutral (i.e., neither attractive nor repellent) to the beetles as tested against air, this neutrality disappeared if the odors of two or more nonhosts were added to the host odor and beetles were given a choice between this mixture and pure host odor. Given this choice, they strongly preferred pure host odor, which suggests that diversity of odors per se is unattractive to the beetles. Beetles walked rather than flew to locate their hosts in the field, and their movements suggest that they used olfactory cues to locate hosts.     

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.     

Induction of volatile emissions in maize by different larval instars of Spodoptera littoralis

Maize plants under attack by caterpillars emit a specific blend of volatiles that is highly attractive to parasitic wasps. The release of these signals is induced by elicitors in the caterpillar regurgitant. Studies suggest that plants respond differently to different herbivore species and even to different herbivore stages, thus providing parasitoids and predators with specific signals. We tested if this is the case for different larval instars of the noctuid moth Spodoptera littoralis when they feed on maize plants. Cut maize plants were incubated in diluted regurgitant from second, third, or fifth instar caterpillars. There were no differences in total amount released after these treatments, but there were small differences in the release of the minor compounds phenethyl acetate and -humulene. Regurgitant of all three instars contained the elicitor volicitin. To test the effect of actual feeding by the larvae, potted plants were infested with caterpillars of one of the three instars, and volatiles were collected the following day. The intensity of the emissions was correlated with the number of larvae feeding on a plant, and with the amount of damage inflicted, but was independent of the instar that caused the damage. We also used artificial damage to mimic the manner of feeding of each instar to test the importance of physical aspects of damages for the odor emission. The emission was highly variable, but no differences were found among the different types of damage. In olfactometer tests, Microplitis rufiventris, a parasitoid that can only successfully parasitize second and early third instar S. littoralis, did not differentiate among the odors of maize plants attacked by different instar larvae. The odor analyses as well as the parasitoid's responses indicate that maize odors induced by S. littoralis provide parasitoids with poor information on the larval developmental stage. We discuss the results in the context of variability and lack of specificity in odorous plant signals.     

The Role of Fresh <Emphasis Type="Italic">versus</Emphasis> Old Leaf Damage in the Attraction of Parasitic Wasps to Herbivore-Induced Maize Volatiles

The odor produced by a plant under herbivore attack is often used by parasitic wasps to locate hosts. Any type of surface damage commonly causes plant leaves to release so-called green leaf volatiles, whereas blends of inducible compounds are more specific for herbivore attack and can vary considerably among plant genotypes. We compared the responses of naïve and experienced parasitoids of the species Cotesia marginiventris and Microplitis rufiventris to volatiles from maize leaves with fresh damage (mainly green leaf volatiles) vs. old damage (mainly terpenoids) in a six-arm olfactometer. These braconid wasps are both solitary endoparasitoids of lepidopteran larvae, but differ in geographical origin and host range. In choice experiments with odor blends from maize plants with fresh damage vs. blends from plants with old damage, inexperienced C. marginiventris showed a preference for the volatiles from freshly damaged leaves. No such preference was observed for inexperienced M. rufiventris. After an oviposition experience in hosts feeding on maize plants, C. marginiventris females were more attracted by a mixture of volatiles from fresh and old damage. Apparently, C. marginiventris has an innate preference for the odor of freshly damaged leaves, and this preference shifts in favor of a blend containing a mixture of green leaf volatiles plus terpenoids, after experiencing the latter blend in association with hosts. M. rufiventris responded poorly after experience and preferred fresh damage odors. Possibly, after associative learning, this species uses cues that are more directly related with the host presence, such as volatiles from host feces, which were not present in the odor sources offered in the olfactometer. The results demonstrate the complexity of the use of plant volatiles by parasitoids and show that different parasitoid species have evolved different strategies to exploit these signals.     

The Role of Indole and Other Shikimic Acid Derived Maize Volatiles in the Attraction of Two Parasitic Wasps

After herbivore attack, plants release a plethora of different volatile organic compounds (VOCs), which results in odor blends that are attractive to predators and parasitoids of these herbivores. VOCs in the odor blends emitted by maize plants (Zea mays) infested by lepidopteran larvae are well characterized. They are derived from at least three different biochemical pathways, but the relative importance of each pathway for the production of VOCs that attract parasitic wasps is unknown. Here, we studied the importance of shikimic acid derived VOCs for the attraction of females of the parasitoids Cotesia marginiventris and Microplitis rufiventris. By incubating caterpillar-infested maize plants in glyphosate, an inhibitor of the 5-enolpyruvylshikimate-3-phospate (EPSP) synthase, we obtained induced odor blends with only minute amounts of shikimic acid derived VOCs. In olfactometer bioassays, the inhibited plants were as attractive to naive C. marginiventris females as control plants that released normal amounts of shikimic acid derived VOCs, whereas naive M. rufiventris females preferred inhibited plants to control plants. By adding back synthetic indole, the quantitatively most important shikimic acid derived VOC in induced maize odors, to inhibited plants, we showed that indole had no effect on the attraction of C. marginiventris and that M. rufiventris preferred blends without synthetic indole. Exposing C. marginiventris females either to odor blends of inhibited or control plants during oviposition experiences shifted their preference in subsequent olfactometer tests in favor of the experienced odor. Further learning experiments with synthetic indole showed that C. marginiventris can learn to respond to this compound, but that this does not affect its choices between natural induced blends with or without indole. We hypothesize that for naïve wasps the attractiveness of an herbivore-induced odor blend is reduced due to masking by nonattractive compounds, and that during oviposition experiences in the presence of complex odor blends, parasitoids strongly associate some compounds, whereas others are largely ignored.     

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.