Chemical discrimination of prey by naive neonate Gould's monitorsVaranus gouldii

Previous studies have demonstrated that actively foraging autarchoglossan lizards rely in part on chemoreception to detect and locate prey. In one of two experiments, neonate Gould's monitorsVaranus gouldii were studied to determine whether they were able to discriminate between multiple prey odors and control odors by tongue-flicking. Responses of lizards to deionized water, a pungency control (cologne), mouse, gecko, and cricket odors on cotton-tipped applicators were studied in experiments using repeated-measures designs and using the tongue-flick attack score (TFAS) as the primary measure of response strength. The TFAS was greater in response to cricket odors than to other prey odors or to either of the control stimuli, and there was no statistically significant difference in response between control stimuli. Range of tongue-flicks elicited by cricket odor were greater than those for other prey odors and control stimuli. Only applicators bearing cricket odor were bitten. In the second experiment, lizards were tested to determine whether they respond differently to chemical stimuli taken from the exoskeleton vs. internal fluids of crickets. TFAS were slightly higher for chemical stimuli taken from internal fluids, but not significantly so. Lizards bit applicators in both conditions. Details of responses to experimental trials are discussed in relation to the feeding behavior of this species.     

Responses to major categories of food chemicals by the lizard Podarcis lilfordi

Many lizards are capable of identifying food using only chemical cues from food surfaces, but almost nothing is known about the types of compounds that are effective stimuli. We experimentally studied lingual and biting responses by a lacertid lizard, Podarcis lilfordi, to single representatives of three major categories of food chemicals, sucrose as a carbohydrate, pure pork fat as a mixture of lipids, and bovine gamma globulin as a protein. In 60-sec trials in which stimuli were presented on cotton swabs, the lizards detected all three stimuli, exhibiting more tongue-flicks, licks, or bites, or a greater tongue-flick attack score (TFAS; overall measure of response strength to prey stimuli) than to deionized water. The initial response to all stimuli was tongue-flicking, but the lizards discriminated among the types of chemical stimuli. After preliminary tongue-flicks, the lizards responded to sucrose solutions by licking at high rates, to pure pork fat by biting, and to protein by a combination of additional tongue-flicks and biting. Biting is a feeding response to prey or solid plant material. Licking is a feeding response to sugars in nectar or ripe fruit. Its frequency increased with sucrose concentration. Our data suggest that lizards can identify several types of chemicals associated with food and direct feeding attempts to sources of such chemicals in the absence of visual cues.     

Tongue-flicking and biting in response to chemical food stimuli by an iguanid lizard (Dipsosaurus dorsalis) having sealed vomeronasal ducts: Vomerolfaction may mediate these behavioral responses

In the iguanid lizardDipsosaurus dorsalis, chemical food stimuli were discriminated from other odorants by vomerolfaction. This was demonstrated in a 2 × 3 experiment in which groups of lizards with sealed vomeronasal ducts or sham-sealed vomeronasal ducts responded to carrot chemical stimuli, cologne, and distilled water presented on cotton-tipped applicators. Abilities to detect and discriminate food chemicals were abolished in lizards having sealed vomeronasal ducts. For tongue-flick attack score and number of lizards biting, the sham-sealed group responded more strongly to carrot stimuli than to the control stimuli, but the group having sealed ducts did not. Lizards having sham-sealed ducts responded more strongly to carrot stimuli than did lizards having sealed ducts; responses by the two groups of lizards to control stimuli did not differ. Tongue-flicking occurred when the vomeronasal system detected a chemical stimulus from either carrot or cologne. Biting occurred only when the vomeronasal organ detected food stimuli (from carrot). Most duct-sealed lizards opened their mouths, some repeatedly. Mouth-opening thus occurs when the vomeronasal organ does not detect chemicals. It may be an attempt to stimulate or prime the vomeronasal organ or to dislodge the sealant.     

Discrimination of Prey, But Not Plant, Chemicals by Actively Foraging, Insectivorous Lizards, the Lacertid Takydromus sexlineatus and the Teiid Cnemidophorus gularis

Sampling environmental chemicals to reveal prey and predators and to provide information about conspecifics is highly developed in lizards. Actively foraging lizards can discriminate between prey chemicals and control stimuli, but ambush foragers do not exhibit prey chemical discrimination. Recent experiments on a few species of herbivorous lizards have also demonstrated an ability to identify plant food chemicals. We studied chemosensory responses to chemicals from prey and palatable plants in two species of actively foraging, insectivorous lizards. Both the lacertid Takydromus sexlineatus and the teiid Cnemidophorus gularis exhibited strong responses to prey chemicals, but not to plant chemicals. These findings increase confidence in the relationship between prey chemical discrimination and foraging mode, which is based on data for very few species per family. They also provide data showing that actively foraging insectivores in two families do not respond strongly to plant cues. Such information is essential for eventual comparative studies of the relationship between plant diet and responses to food chemicals. The traditional method of presenting stimuli by using hand-held cotton swabs worked well for T. sexlineatus but could not be used for C. gularis due to repeated escape attempts. When stimuli were presented to C. gularis on ceramic tiles and no experimenter was visible, the lizards responded readily. Presentation of stimuli on tiles in the absence of a visible experimenter may be a valuable approach to study of food chemical discrimination by active foragers in which antipredatory behavior interferes with responses to swabs.     

Correspondence Between Diet and Food Chemical Discriminations by Omnivorous Geckos (Rhacodactylus)

Chemosensory responses to food are correlated with geographic variation in diet of some colubrid snakes, but the influence of diet on chemosensory behavior has not been established generally in snakes or lizards. Most lizards are generalist predators of small animals, making it difficult to study effects of diet, but herbivory and omnivory have evolved in several lineages, providing an excellent opportunity to study the effects of dietary change on chemosensory behavior. Based on ecological considerations, I argue that inclusion of plants in the diet of lizards that evolved from ambush foragers lacking prey chemical discrimination might be expected to evolve responsiveness to plant food chemicals. If animal prey also are retained in the diet, then responsiveness to prey chemicals should evolve as well. I experimentally studied tongue-flicking and biting responses by omnivorous geckos of the genus Rhacodactylus to chemical stimuli from plant and animal foods and control substances presented on cotton swabs. The lizards exhibited significantly greater responses to plant stimuli than to control stimuli. One of two species tested responded strongly to cricket chemicals, but the other showed no significant response to mouse surface chemical stimuli. The results support the hypothesis that dietary shifts induce corresponding changes in chemosensory response, but establishment of correlated evolution between diet and food chemical discriminations in lizards will require study of many herbivores/omnivores and insectivores as controls.     

Discriminative Response to Animal, But Not Plant, Chemicals by an Insectivorous, Actively Foraging Lizard, Scincella lateralis, and Differential Response to Surface and Internal Prey Cues

Responses by the insectivorous, actively foraging scincid lizard, Scincella lateralis, to chemical cues from a plant food favored by herbivorous lizards, its ability to discriminate prey chemicals from control substances, and its relative response to internal and surface prey chemicals were studied experimentally. We presented chemical cues to the lizards on cotton swabs and recorded their tongue-flicks and biting attacks on the swabs. The lizards exhibited significantly greater tongue-flick rates and biting frequencies to prey surface cues than to plant surface chemicals from romaine lettuce, diluted cologne (pungency control), and deionized water. Responses to the plant stimuli did not differ from those to the two control stimuli, in contrast with strong responses to the same plant cues by herbivores. This finding provides the first information suggesting that chemosensory response may be adapted to diet, with responsiveness to plant stimuli evolving de novo in herbivores. Biting and tongue-flicking responses were significantly greater to cricket chemicals than to all other stimuli, among which there were no differences. Thus, the lizards are capable of prey chemical discrimination, which may be ubiquitous among actively foraging lizards. The lizards exhibited more frequent biting and higher tongue-flick rates to internal than surface prey chemicals. Although different methods of stimulus preparation are appropriate for different purposes, we conclude that prey surface chemicals available to foraging lizards are most desirable for studies bearing on location and identification of prey.     

How contact foraging experiences affect preferences for host-related odors in the larval parasitoidCotesia marginiventris (Cresson) (Hymenoptera: Braconidae)

Responses of individual females of the parasitoidCotesia marginiventris to the odors of four different complexes of host larvae feeding on leaves were observed in a four-arm olfactometer. The plant-host complexes were composed of fall armyworm (FAW) larvae or cabbage looper (CL) larvae feeding on either corn or cotton seedlings. Prior to testing, each female was given a brief foraging experience on a plant-host complex and was then exposed to the odors of the same complex in the olfactometer. The experienced females responded to familiar odors in a dose-related manner, and these responses were virtually identical to all four complexes. Preferences for the odors of one of two plant-host complexes were tested in dual choice situations. Generally, FAW odors were preferred over CL odors and corn odors over cotton odors. A short foraging experience significantly affected the females' odor preferences in favor of the odors released by the experienced complex. Additional experiments revealed that neither longer bouts of experience nor bouts that included ovipositions resulted in a stronger change in preference. Experience affected preference in combinations where only the host species was varied as well as in combinations where only the plant species was varied. The results, therefore, strongly indicate that both the plants and the hosts somehow are involved in the production and/or release of the semiochemicals that attractC. marginiventris.Mention of a proprietary product does not constitute an endorsement or the recommendation for its use by the USDA.     

Responses to prey chemicals by a lacertid lizard,Podarcis muralis: Prey chemical discrimination and poststrike elevation in tongue-flick rate

The ability to discriminate prey chemicals from control substances and the presence of a poststrike elevation in tongue-flicking (PETF) rate are experimentally demonstrated in the lacertid lizard,Podarcis muralis, The tongue-flick attack score, a composite index of response strength, was significantly higher in response to integumental chemicals from cricket than to cologne or distilled water. The cricket chemicals additionally elicited a significantly greater rate of tongue-flicking and higher proportion of attacks by the lizards than did control stimuli. PETF combined with apparent searching movements strongly suggest the presence of strike-induced chemosensory searching (SICS). Experimental evidence indicates that both PETF and SICS occur in insectivorous representatives of three families of actively foraging autarchoglossan lizards, suggesting their widespread occurrence in such lizards. The adaptive roles of chemosensory behavior in the foraging behavior of P.Muralis are discussed. It is proposed that these lizards may form chemical search images and that PETF and SICS may have been present in the lacertilian ancestors of snakes.     

Crayfish feeding responses to zebra mussels depend on microorganisms and learning

Three species of crayfish (Orconectes virilis, O. rusticus, andCambarus robustus) were tested for feeding responses to potential food odors from mollusks (either zebra mussels,Dreissena polymorpha, or native gastropods). In all three crayfish species, feeding responses to odor cues were shown only by individuals experienced with feeding on a prey type. Individuals exposed to just the smell of prey organisms did not show feeding responses, indicating the role of associative learning in diet breadth. Establishment of a learned association took more than one feeding experience but once established lasted more than three weeks. When microbial enzymatic degradation of food protein was eliminated, either by UV radiation or microfiltration, feeding responses were eliminated even for crayfish experienced with a prey type.     

Predatory response of brown tree snakes to chemical stimuli from human skin

The brown tree snake (Boiga irregularis) is an exotic pest species on Pacific islands, most notably on Guam where it has caused considerable ecological and economic damage. On Guam, the snake commonly associates with people and can be found near or in human habitations. Bites are common, approximately 1 of 1200 emergency room visits to Guam hospitals were reported to be the result of B. irregularis bites; 80% of these victims were attacked while sleeping. Most of the attacks occurred on fingers and hands and the attacks appeared to be predatory, rather than defensive, in nature. In order to characterize the mechanism releasing this unusual behavior, we measured the predatory response of B. irregularis to chemical stimuli from humans and controls using a lab population that originated from Guam and a wild population from the species' native range in Queensland, Australia. To quantify behavior we measured the proportion of snakes displaying predatory behavior to each of the stimuli, the latency to attack, and the number of tongue-flicks displayed. We quantified predatory behavior using the tongue-flick attack score for repeated measures [TFAS(R)], a common method for quantifying predatory behavior in squamate reptiles. Captive brown tree snakes responded to human skin stimuli with feeding behavior, including predatory attacks, at the same frequency as they did to prey stimuli derived from mice, while never responding to controls with such behavior. Captive snakes also responded to human skin stimuli and prey stimuli with significantly higher TFAS(R) scores than to controls, although there were no differences between the human and mouse stimuli. Wild-caught animals in Australia also responded with predatory attacks to human skin stimuli, while not showing predatory behavior to a blank control and with higher TFAS(R) scores to human skin stimuli than to the control. As B. irregularis is a generalized predator that relies heavily on chemical signals to recognize prey, we hypothesize that the snakes recognize compounds on human skin that may be shared with other prey.     

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 Ecology of the host searching behavior in an Egg Parasitoid: are Common Chemical Cues exploited to locate hosts in Taxonomically Distant Plant Species?

Parasitoids are known to exploit volatile cues emitted by plants after herbivore attack to locate their hosts. Feeding and oviposition of a polyphagous herbivore can induce the emission of odor blends that differ among distant plant species, and parasitoids have evolved an incredible ability to discriminate them and locate their hosts relying on olfactive cues. We evaluated the host searching behavior of the egg parasitoid Cosmocomoidea annulicornis (Ogloblin) (Hymenoptera: Mymaridae) in response to odors emitted by two taxonomically distant host plants, citrus and Johnson grass, after infestation by the sharpshooter Tapajosa rubromarginata (Signoret) (Hemiptera: Cicadellidae), vector of Citrus Variegated Chlorosis. Olfactory response of female parasitoids toward plants with no herbivore damage and plants with feeding damage, oviposition damage, and parasitized eggs was tested in a Y-tube olfactometer. In addition, volatiles released by the two host plant species constitutively and under herbivore attack were characterized. Females of C. annulicornis were able to detect and significantly preferred plants with host eggs, irrespectively of plant species. However, wasps were unable to discriminate between plants with healthy eggs and those with eggs previously parasitized by conspecifics. Analysis of plant volatiles induced after sharpshooter attack showed only two common volatiles between the two plant species, indole and β-caryophyllene. Our results suggest that this parasitoid wasp uses common chemical cues released by many different plants after herbivory at long range and, once on the plant, other more specific chemical cues could trigger the final decision to oviposit.

     

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.     

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.     

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.     

Postbite elevation in tongue-flicking rate by an iguanian lizard,Dipsosaurus dorsalis

The herbivorous iguanid lizardDipsosaurus dorsalis exhibited PETF (postbite elevation in tongue-flicking rate), an increase in tongue-flicking rate after experimental removal from the mouth of food that had been bitten. This was demonstrated by a significantly higher tongue-flick rate after having bitten food than in three experimental conditions controlling for responses to the experimental setting, sight of food, and mechanical disturbance caused by the experimental removal of food from a lizard's mouth. As in most other families of lizards, PETF was brief, occurring only during the first minute. Lizards are divided into two major suprafamilial taxa, Iguania and Scleroglossa, consisting of carnivorous species characterized by two major foraging modes, ambush and active, and of herbivores and omnivores. PETF is absent in the two families of carnivorous iguanian lizards studied that are ambush foragers but present in three families of scleroglossan lizards that are active foragers. However, PETF is absent in the two species studied in a scleroglossan family, Gekkonidae, which forages by ambush, and present in an iguanian herbivore, as reported herein. We propose that the presence or absence of PETF, in addition to its phylogenetic determinants, is adaptively adjusted to foraging mode.     

Responses by king snakes (Lampropeltis getulus) to chemicals from colubrid and crotaline snakes

Four litters of king snakes (Lampropeltis getulus), a snake-eating species, were tested for responses to chemicals from colubrid and crotaline snakes. King snakes presented with swabs rubbed against the dorsal skin of living snakes and with swabs treated with methylene chloride extracts of shed snake skins tongue-flicked more to swabs from a northern copperhead (Agkistrodon contortrix), a crotaline, than to swabs from some colubrid snakes or to blank swabs. Six out of 10 king snakes in one litter attacked and attempted to ingest swabs treated with snake skin chemicals, implicating these chemicals as feeding stimuli for these ophiophagous snakes. Ingestively naive king snakes presented with plain air and snake odors in an olfactometer tongue-flicked more to snake odors. This study and others suggest that crotaline and colubrid snakes can be distinguished by chemical cues.     

Chemical Ecology of Fruit Bat Foraging Behavior in Relation to the Fruit Odors of Two Species of Paleotropical Bat-Dispersed Figs (<Emphasis Type="Italic">Ficus hispida</Emphasis> and <Emphasis Type="Italic">Ficus scortechinii</Emphasis>)

We investigated the fruit odors of two bat-dispersed fig species in the Paleotropics, in relation to the foraging behavior of fruit bats, to test the following hypotheses: 1) fruit odor plays a critical role for detection and selection of ripe figs by fruit bats; 2) bat-dispersed fig species are characterized by the same, or similar, chemical compounds; and 3) total scent production, in bat-dispersed figs, increases when fruits ripen. We performed bioassays to test the effect of both natural and synthetic fig fruit odors on the foraging behavior of the short-nosed fruit bat (Cynopterus brachyotis)—an important disperser of figs within the study area. Fruit bats responded to both visual and chemical (olfactory) cues when foraging for figs. However, the strongest foraging reaction that resulted in a landing or feeding attempt was almost exclusively associated with the presence of a ripe fruit odor—either in combination with visual cues or when presented alone. Fruit bats also used fruit odors to distinguish between ripe and unripe fruits. By using gas chromatography (GC) and GC/mass spectrometry (MS), a total of 16 main compounds were identified in the ripe fruit odor of Ficus hispida and 13 in the ripe fruit odor of Ficus scortechinii—including alcohols, ketones, esters, and two terpenes. Additional compounds were also recorded in F. hispida, but not identified—four of which also occurred in F. scortechinii. Total scent production increased in both species when fruits ripened. Both natural and synthetic fruit odors resulted in feeding attempts by bats, with no feeding attempts elicited by unscented controls. Reaction rates to natural fruit odors were higher than those to synthetic blends.     

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.     

Attractant or Pheromone: The Case of Nasonov Secretion and Honeybee Swarms

Honeybees are attracted to a variety of odors, including the secretion of their Nasonov glands, a secretion that has been widely assumed to be an orientation and attraction pheromone. A crossover design experiment comparing synthetic Nasonov secretion with linalool, oil of clove, skatole, and wax moth sex pheromone was established to determine if Nasonov secretion serves as a true pheromone or is simply a general attractant for honeybee swarms. None of the test odors was more attractive than odorless controls, and in all comparisons, synthetic Nasonov secretion was significantly more attractive than the test odors or odorless controls. The results confirm that Nasonov secretion is a true pheromone in the context of attracting honeybee swarms to nest cavities and that environmentally present or apparent odors play little or no role in honeybee nest-seeking behavior.