Discrimination of integumentary prey chemicals and strike-induced chemosensory searching in the ball python,Python regius

Experimental tests show that the ball python (Python regius) has the ability to discriminate prey chemicals from control substances by tongue-flicking and exhibits a poststrike elevation in tongue-flicking rate (PETF). Prey chemical discrimination was revealed by significantly higher number of tongue-flicks and tongue-flick attack score in response to integumental chemicals from mice than to cologne or distilled water and by a higher frequency of biting in response to prey than control chemicals. PETF was indicated by higher tongue-flicking rates after biting than in several control conditions. Concurrent movements of the body suggest the operation of strike-induced chemosensory searching (SICS). Ecological factors affecting responses to prey chemicals, including defensive behaviors and characteristics of foraging behavior related to reliance on different sensory modalities, are discussed. The presence of PETF and SICS in a henophidian snake and in scleroglossan lizards suggests that these behaviors are plesiomorphic in snakes.     

Food chemical discriminations by an herbivorous lizard, Corucia zebrata

Adjustment of chemosensory response to diet should be apparent in evolutionary changes corresponding to dietary shifts. Because most lizards are generalist predators of small animals, relationships between chemosensory behavior and diet are difficult to detect. Nevertheless, the evolution of herbivory by a small number of lizards provides an opportunity to detect any corresponding change in response to plant chemicals. I studied tongue-flicking and biting by the large, herbivorous scincid lizard Corucia zebrata in response to chemical cues from crickets, romaine lettuce, and control stimuli presented on cotton swabs. The skinks exhibited significantly stronger response to plant and animal chemicals than to controls for several variables: greater number of individuals that bit swabs, shorter latency to bite, greater rate of tongue-flicks, and greater tongue-flick attack score. The clearest differences were observed for tongue-flick attack score, a composite variable that combines the effects of tongue-flicking and biting. An insectivorous member of the same subfamily, Scincella lateralis, shows strong tongue-flicking and biting response to chemical prey cues, but not to plant chemicals. This suggests that response to plant chemicals by C. zebrata may have evolved in tandem with the incorporation of plants into the diet and that response to cricket chemicals has been retained, perhaps due to similarities between plant and animal food. The findings support the hypothesis that dietary shifts induce corresponding changes in chemosensory response, but provide only a single independent contrast for a study of correlated evolution between plant diet and chemosensory response to plants. J. Exp. Zool. 286:372-378, 2000.     

Responses to chemical cues from animal and plant foods by actively foraging insectivorous and omnivorous scincine lizards

If tongue-flicking is important to lizards to sample chemical cues permitting identification of foods, tongue-flicking and subsequent feeding responses should be adjusted to match diet. This hypothesis can be examined for plant foods because most lizards are insectivores, but herbivory/omnivory has evolved independently in many lizard taxa. Here we present experimental data on chemosensory responses to chemical cues from animal prey and palatable plants by three species of the scincine lizards. When tested with chemical stimuli presented on cotton swabs, the insectivorous Eumeces fasciatus responded strongly to prey chemicals but not to chemicals from plants palatable to omnivorous lizards or to pungent or odorless control stimuli. Two omnivorous species, E. schneideri and Scincus mitranus, responded more strongly to chemical cues from both prey and food plants than to the control chemicals. All available data for actively foraging lizards, including these skinks, show that they are capable of prey chemical discrimination, and insectivores do not exhibit elevated tongue-flicking or biting responses to chemical cues from palatable plants. In all of the several species of herbivores/omnivores tested, the lizards show elevated responses to both animal and plant chemicals. We suggest two independent origins of both omnivory and plant chemical discrimination that may account for the evolution of diet and food chemical discriminations in the eight species of skinks studied, five of which are omnivores. All data are consistent with the hypothesis that acquisition of omnivory is accompanied by acquisition of plant chemical discrimination, but data on a broad diversity of taxa are needed for a definitive comparative test of the evolutionary hypothesis. J. Exp. Zool. 287:327-339, 2000.     

Prey Odor Discrimination in the Varanoid Lizards Heloderma suspectum and Varanus exanthematicus

Use of chemical senses to detect prey is believed to be an important component of foraging behavior in actively foraging lizards. Ability to detect prey odors and discriminate them from control odors by tongue-flicking was studied in representatives of two families of lizards having highly forked, elongated, retractile tongues. Responses of gila monsters (Heloderma suspectum) and savannah monitors (Varanus exanthematicus) to deionized water, a control for pungency (cologne), and mouse odor on cotton swabs were studied in experiments using repeated-measures designs and employing the tongue-flick attack score (TFAS) as the primary measure of response strength. TFAS differed among treatments for gila monsters and monitors. Both species had greater TFAS to mouse odors than to either of the control stimuli, but responses to cologne were not statistically distinguishable from those to water. Numbers of tongue-flicks elicited by prey odors were greater than those for control stimuli in V. exanthematicus, but not for H. suspectum. Gila monsters, but not savannah monitors, bit in a significantly greater proportion of tests with prey odors than with control stimuli. Details of responses, including frequency of biting, apparent search behavior in the vicinity of applicators bearing mouse odors, and responses to control stimuli are discussed in relation to the foraging behavior of these two species and their relatives. Evidence from this and other studies suggests that the vomeronasal sense (and perhaps other chemical senses) is an important means of locating and recognizing prey in widely foraging autarchoglossan lizards.     

Food chemical cues elicit general and population-specific effects on lingual and biting behaviors in the lacertid lizard Podarcis lilfordi

Actively foraging lizards are capable of identifying prey using only chemical cues sampled by tongue-flicking, and the relatively few omnivorous and herbivorous lizards tested similarly can identify both animal and plant foods from chemical cues. Whether lizards that eat plants respond to cues specific to preferred plant types and whether there is geographic variability in responses to cues from various plants correlated with the importance of those plants in local diets is unknown. In three populations of an omnivorous lacertid, the Balearic lizard Podarcis lilfordi, we studied chemosensory sampling and feeding responses to chemical cues from plant and animal foods presented on cotton swabs. Each lizard population is endemic to one islet off the coast of Menorca, Balearic Islands, Spain. Lizards in all three populations discriminated chemical cues from plant and animal foods from control substances. Our results extend findings of prey chemical discrimination and plant chemical discrimination in omnivores, increasing confidence that correlated evolution has occurred between plant diet and chemosensory response to palatable plants. There were no consistent differences among populations in tongue-flicking and biting responses to stimuli from flowers of syntopic and allopatric plant species. The lizards may respond to cues indicative of palatability in a wide range of plant species rather than exhibiting strong responses only to locally available plant species. Nevertheless, tongue-flicking and biting frequencies varied among plant species, perhaps indicating food preferences. In addition, there were differences among populations in tongue-flick rates, latency to bite, and licking behavior. Licking was observed in only one lizard population as a response to floral chemicals from only one of the plants species tested, raising the possibility of a population-specific linkage between identification of a particular plant species and performance of an appropriate feeding response.     

Insect chemosensory responses: a chemical legacy hypothesis

Abstract. 1. Changes in the chemosensory responses and physiological host tolerance of phytophagous insects and parasitoids may result in new host associations. This paper considers the origin of those changes in ecological and evolutionary time.
2. The chemical legacy hypothesis postulates that effects of larval chemosensory environment on adult chemosensory responsiveness depend not (or not only) on persistent neural changes ('memory'), but on traces of chemical cues, inside or outside the insect's body, which influence adult behaviour, perhaps particularly during a 'sensitive period' associated with adult emergence or hatching of the egg.
3. Chemical cues bequeathed by earlier stages may affect adults or larvae by reducing peripheral sensitivity. Depending on the form of the dose–response curve, this change could decrease aversion or increase a positive response to a previously deterrent stimulus.
4. Attention is drawn to a possible link between this behavioural induction and the induction of detoxification enzymes. This link might be of practical importance if exposure to host allelochemicals were to influence insects' responses to insecticides, and vice versa.
5. An influence on the chemosensory responsiveness of an individual by chemical cues derived from its parents would be hard to distinguish from a genetic effect.
6. Some testable postulates of the chemical legacy hypothesis are identified.     

Chemosensory responses to foods by an herbivorous acrodont lizard, <Emphasis Type="Italic">Uromastyx aegyptius</Emphasis>

Actively foraging lizards use the lingual-vomeronasal system to identify prey by chemical cues, but insectivorous ambush foragers do not. The major clade Iguania includes numerous herbivores and omnivores; among them, two iguanid and one agamine species identify plant and animal foods by tongue flicking, and data suggest that the leiolepidine Uromastyx acanthinurus may as well. We conducted experiments on chemosensory response to food by the herbivorous U. aegyptius. When chemical stimuli were presented on cotton balls in experiment 1, the lizards exhibited greater responsiveness (tongue-flick attack scores) to chemical stimuli from crickets and a preferred plant food (dandelion flowers) than from deionized water. When chemical stimuli were on ceramic tiles in experiment 2, the lizards exhibited greater total tongue flicks to cricket stimuli than to any other stimuli, and to dandelion than to deionized water. Lizards bit more frequently in response to cricket and dandelion cues than to stimuli from a nonpreferred plant (carrot) and deionized water. Tongue-flick attack scores were greater in response to cricket and dandelion stimuli than to carrot or water stimuli. These findings are consistent with the hypothesis that herbivores, even those having ambush-foraging ancestors, use chemical cues to identify potential foods. The data support the hypothesis that chemosensory responses correspond to diet. Because most lizards are generalist predators, studies of herbivorous species can provide important information on possible evolutionary adjustment of chemosensory response to dietary shifts. Electronic Publication     

Coordinated Ontogeny of Food Preference and Responses to Chemical Food Stimuli by a Lizard Ctenosaura pectinata (Reptilia: Iguanidae)

When important ecological factors change predictably during the life of an organism, the ontogeny of related behaviors must be timed to maintain appropriate behavioral responsiveness to current ecological conditions. In the brown iguana, Ctenosaura pectinata , hatchlings in natural populations eat primarily insects, consuming little plant matter, whereas adults eat primarily plants, consuming some insects as well. We conducted laboratory experiments on diet preferences and responses to chemical cues that the lizards sampled by tongue-flicking and used to identify food. All hatchlings ate crickets, but only one of six ate romaine lettuce. They responded strongly to chemical cues from prey, as indicated by elevated tongue-flick rates, but not from romaine lettuce. All older individuals ate both crickets and romaine lettuce. They responded much more strongly to chemical cues from both crickets and romaine lettuce than to control chemicals, as indicated by higher proportions of individuals that bit and higher tongue-flick attack scores.
Thus, an ontogenetic change to increased responsiveness to plant chemical stimuli was coordinated with an ontogenetic change to an herbivorous diet. The mechanisms underlying these ontogenetic changes are unknown, but folivory may be unprofitable before juveniles acquire intestinal flora that degrade cellulose by ingestion of feces of adult conspecifics. Possible mechanisms are discussed, including the detection of chemical cues from appropriate food plants during consumption of feces from older individuals. Studies of other squamate reptiles suggest that exposure to these chemicals might affect both future responsiveness to the chemical cues and a tendency to eat the corresponding plants.     

An Adaptive Difference in the Relationship between Foraging Mode and Responses to Prey Chemicals in two Congeneric Scincid Lizards

Sensory abilities must allow efficient detection of prey, but the senses used and their relative importance may vary with hunting methods. In lizards, ambush foragers locate prey visually and active foragers use a combination of vision and vomerolfaction, the chemical sense associated with the vomeronasal system. Active foragers, but not ambush foragers, discriminate between prey chemicals and other chemical stimuli sampled by tongue-flicking. In active foragers, features of the tongue that may improve chemical sampling, such as elongation and forking are more pronounced and density of vomeronasal chemoreceptors is greater, than in ambush foragers. Foraging mode is fixed in most lizard families, and correlated evolution has been demonstrated among foraging mode, discrimination of prey chemicals, and lingual-vomeronasal morphology by interfamilial comparisons. Here I present information on a rare case of an intrageneric difference in foraging mode in the genus Mabuya . Laboratory experiments on the discrimination of prey chemicals showed that the active forager M . striata sparsa exhibits prey chemical discrimination, but the ambush forager M . acutilabris does not. The active forager also has a slightly more elongated tongue with deeper notching at the tip than the ambush forager, which might be a response to a change in foraging behavior or a reflection of unrelated differences in head shape. These findings confirm predictions based on correlated evolution between the hunting method and use of the chemical sense to locate food. They further show that chemosensory behavior is adjusted to change in foraging mode more rapidly than was previously known and suggest that behavioral changes may occur more rapidly than associated modifications of chemosensory morphology.     

Post-bite Elevation in Tongue-flick Rate by Neonatal Garter Snakes (Thamnophis radix)

A post-biting elevation in tongue-flicking rate was demonstrated experimentally in neonatal, ingestively naive garter snakes (Thamnophis radix). That the snakes also exhibited apparent searching movements suggests that strike-induced chemosensory searching occurs in nonvenomous snakes lacking previous experience with food or prey chemicals. Two litters of neonates differed in numbers of tongue-flicks emitted, but had similar relative magnitudes of response across experimental conditions. The existence of post-bite elevation in tongue-flick rate (and presumably strike-induced chemosensory searching) argues for a genetic basis for these chemosensory behaviors in a nonvenomous species of snake, extending the recent finding that strike-induced chemosensory searching is fully developed in ingestively naive neonatal rattlesnakes. Possible patterns of evolution of post-bite elevation in tongue-flick rate, and the strike-release-trail strategy of highly venomous snakes are discussed.     

Necromone Death Cues and Risk Avoidance by the Cricket <Emphasis Type="Italic">Acheta domesticus</Emphasis>: Effects of Sex and Duration of Exposure

We document that the cricket, Acheta domesticus, avoids “necromone” chemical cues of death associated with treated surfaces and shelters (i.e., ethanol extracts of cricket bodies, oleic acid or linoleic acid). Initially we tested male responses to male body extract, oleic acid, or linoleic acid associated with shelters. Body extract was more repellent than either oleic or linoleic acid at a dose of 10 body equivalents per shelter. At 15 or 20 body equivalents/shelter extract and oleic acid were similarly repellent but linoleic acid was weaker. We next tested responses of males or females to shelters and surfaces treated with body extracts of males, females, a male-female mixture, or oleic acid. Repellency was evaluated at 1, 16, and 22 h following introduction. Body extracts elicited more immediate aversion than did authentic oleic acid (1 h). Females showed declining aversion with time (1, 16, 22 h), especially with regard to male extract. Alternatively, males showed increasing aversion with time, particularly to female extract. Both sexes showed weak responses to oleic acid at 1 h, but significant aversion at 16 and 22 h. We suggest that females may be less risk aversive as they seek out singing males holding established territories (i.e., mobility makes risk transient). Alternatively, males may respond more strongly to female necromone as this would reduce attraction of females to their territory. Finally, we consider a classic paper that documents a strong cricket repellent associated with tissue-covered perches. We provide new evidence that this repellent was likely an unsaturated fatty acid.     

Prenatal Alcohol Exposure Increases Postnatal Acceptability of Nicotine Odor and Taste in Adolescent Rats

Human studies indicate that alcohol exposure during gestation not only increases the chance for later alcohol abuse, but also nicotine dependence. The flavor attributes of both alcohol and nicotine can be important determinants of their initial acceptance and they both share the component chemosensory qualities of an aversive odor, bitter taste and oral irritation. There is a growing body of evidence demonstrating epigenetic chemosensory mechanisms through which fetal alcohol exposure increases adolescent alcohol acceptance, in part, by decreasing the aversion to alcohol''s bitter and oral irritation qualities, as well as its odor. Given that alcohol and nicotine have noteworthy chemosensory qualities in common, we investigated whether fetal exposure to alcohol increased the acceptability of nicotine''s odor and taste in adolescent rats. Study rats were alcohol-exposed during fetal development via the dams'' liquid diet. Control animals received ad lib access to an iso-caloric, iso-nutritive diet throughout gestation. Odorant-induced innate behavioral responses to nicotine odor (Experiment 1) or orosensory-mediated responses to nicotine solutions (Experiment 2) were obtained, using whole-body plethysmography and brief access lick tests, respectively. Compared to controls, rats exposed to fetal alcohol showed an enhanced nicotine odor response that was paralleled by increased oral acceptability of nicotine. Given the common aversive component qualities imbued in the flavor profiles of both drugs, our findings demonstrate that like postnatal alcohol avidity, fetal alcohol exposure also influences nicotine acceptance, at a minimum, by decreasing the aversion of both its smell and taste. Moreover, they highlight potential chemosensory-based mechanism(s) by which fetal alcohol exposure increases the later initial risk for nicotine use, thereby contributing to the co-morbid expression with enhanced alcohol avidity. Where common chemosensory mechanisms are at play, our results suggest broader implications related to the consequence of fetal exposure with one substance of abuse and initial acceptability of others.     

Absence of Prey Chemical Discrimination by Tongue-flicking in an Ambush-foraging Lizard Having Actively Foraging Ancestors

Lingually mediated detection of prey chemicals is widespread in one major clade of lizards, Scleroglossa, but rare in the other, Iguania. It is absent in all ambush-foraging families tested and present in all actively foraging families. In Iguania, prey chemical discrimination is known only in the herbivorous Iguanidae; in Scleroglossa, it was heretofore known to be absent only in ambush-foraging gekkonids. Because ambush foraging precludes lingual sampling of a wide area and tongue-flicking would disrupt the crypticity ambushers maintain by immobility, we predicted that prey chemical discrimination would be absent in scleroglossans that have secondarily adopted ambush foraging. The Cape girdled lizard, Cordylus cordylus, is member of Cordylidae, a family of ambush foragers considered derived from active foragers in the Autarchoglossa, a group of scleroglossan families having highly developed lingual chemosensory behaviours. As predicted, this species did not discriminate surface chemicals of three prey species from control substances in a series of standardized experiments in which prey chemicals were presented on cotton-tipped applicators. Thus, even in taxa having highly developed prey chemical discrimination, adoption of ambush foraging may induce loss of prey chemical discrimination, providing further and stronger evidence that prey chemical discrimination is adaptively adjusted to foraging mode.     

Human foetuses learn odours from their pregnant mother's diet

Olfactory responsiveness was assessed in 24 neonates born to mothers who had or had not consumed anise flavour during pregnancy. Both groups of infants were followed-up for behavioural markers of attraction and aversion when exposed to anise odour and a control odour immediately after birth and on day 4. Infants born to anise-consuming mothers evinced a stable preference for anise odour over this period, whereas those born to anise non-consuming mothers displayed aversion or neutral responses. This study provides the first clear evidence that through their diet human mothers influence the hedonic polarity of their neonates' initial olfactory responses. The findings have potential implications for the early mother-to-infant transmission of chemosensory information relative to food and addictive products.     

Chemosensory signaling in C. elegans

The nematode Caenorhabditis elegans can sense and respond to hundreds of different chemicals with a simple nervous system, making it an excellent model for studies of chemosensation. The chemosensory neurons that mediate responses to different chemicals have been identified through laser ablation studies, providing a cellular context for chemosensory signaling. Genetic and molecular analyses indicate that chemosensation in nematodes involves G protein signaling pathways, as it does in vertebrates, but the receptors and G proteins involved belong to nematode-specific gene families. It is likely that about 500 different chemosensory receptors are used to detect the large spectrum of chemicals to which C. elegans responds, and one of these receptors has been matched with its odorant ligand. C. elegans olfactory responses are also subject to regulation based on experience, allowing the nematode to respond to a complex and changing chemical environment.     

Generalization of predator recognition: Velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes

Many prey species detect chemical cues from predators and modify their behaviours in ways that reduce their risk of predation. Theory predicts that prey should modify their anti-predator responses according to the degree of threat posed by the predator. That is, prey should show the strongest responses to chemicals of highly dangerous prey, but should ignore or respond weakly to chemicals from non-dangerous predators. However, if anti-predator behaviours are not costly, and predators are rarely encountered, prey may exhibit generalised antipredator behaviours to dangerous and non-dangerous predators. In Australia, most elapid snakes eat lizards, and are therefore potentially dangerous to lizard prey. Recently, we found that the nocturnal velvet gecko Oedura lesueurii responds to chemicals from dangerous and non-dangerous elapid snakes, suggesting that it displays gen-eralised anti-predator behaviours to chemicals from elapid snakes. To explore the generality of this result, we videotaped the be-haviour of velvet geckos in the presence of chemical cues from two small elapid snakes that rarely consume geckos: the nocturnal golden-crowned snake Cacophis squamulosus and the diurnal marsh snake Hemiaspis signata. We also videotaped geckos in tri-als involving unsceted cards (controls) and cologne-scented cards (pungency controls). In trials involving Cacophis and Hemi-aspis chemicals, 50% and 63% of geckos spent long time periods (> 3 min) freezing whilst pressed flat against the substrate, re-spectively. Over half the geckos tested exhibited anti-predator behaviours (tail waving, tail vibration, running) in response to Ca-cophis (67%) or Hemiaspis (63%) chemicals. These behaviours were not observed in control or pungency control trials. Our re-sults support the idea that the velvet gecko displays generalised anti-predator responses to chemical cues from elapid snakes. Generalised responses to predator chemicals may be common in prey species that co-occur with multiple, ecologically similar, dangerous predators.     

Feeding and selection of saccharin after injections of bombesin, LiCl, and NaCl

Rats injected with bombesin of LiCl showed similar suppression of food-deprivation-induced liquid diet intake, but only rats receiving LiCl avoided water-deprivation-induced consumption of a novel saccharin solution paired with injection. The data demonstrate that bombesin reduces feeding but does not induce conditioned aversion, and suggest that bombesin does not act to suppress food intake by production of gastrointestinal malaise.     

A Comparative Study of Snake and Lizard Tongue-flicking,with an Evolutionary Hypothesis

Many lizards and all snakes flick their tongues. It is known that this unique behavioral pattern serves to collect airborne and substrate chemicals which give the animal information via Jacobson's Organ about the location of food, conspecifics, and possibly other environmental factors. However, a comparative topographic analysis of tongue movements in squamate reptiles is lacking, and it might shed light on the evolution of this behavior. In this study, a survey was made of the lizards and snakes which tongue-flick. Observations and films were made of 25 lizard species representing 10 families and 30 snake species representing 5 families. The information from observations and film analyses of representative species was used to hypothesize the steps of the evolution of tongue-flicking from the simple downward extensions of primitive lizards to the complex multiple oscillations of snakes.     

Involvement of Serotonin Transporter Gene Polymorphisms (5-HTT) in Impulsive Behavior in the Japanese Population

The serotonergic pathway has been implicated in the pathogenesis of impulsivity, and sensitivity to aversive outcomes may be linked to serotonin (5-HT) levels. Polymorphisms in the gene that encodes the serotonin transporter (5-HTT), which have differential effects on the level of serotonin transmission, display alternate responses to aversive stimuli. However, recent studies have shown that 5-HT does not affect motor function, which suggests that the functioning of the serotonin-transporter-linked polymorphic region (5-HTTLPR) does not directly affect the behavioral regulatory process itself, but instead exerts an effect via the evaluation of the potential risk associated with particular behavioral outputs. The aim of the present study was to examine the effect of specific 5-HTTLPR genotypes on the motor regulatory process, as observed during a Go/Nogo punishment feedback task. 5-HTT gene-linked promoter polymorphisms were analyzed by polymerase chain reaction, using lymphocytes from 61 healthy Japanese volunteers. Impulsivity was defined as the number of commission errors (responding when one should not) made during a Go/Nogo task. We found that the s/s genotype group made fewer impulsive responses, specifically under aversive conditions for committing such errors, compared to those in the s/l group, without affecting overall motor inhibition. These results suggest that 5-HTTLPRs do not directly affect the behavioral regulatory process itself, but may instead exert an effect on the evaluation of potential risk. The results also indicate that under such aversive conditions, decreased expression of 5-HTT may promote motor inhibitory control.     

腹侧被盖区多巴胺能神经元对奖赏/厌恶刺激反应的异质性

中脑多巴胺奖赏系统,由腹侧被盖区及其投射靶区组成,参与药物依赖、精神疾病等病理过程的调控.奖赏和厌恶刺激是衡量上述病理过程的重要手段.一直以来,不同研究在该系统对奖赏和厌恶刺激的反应上存在分歧,越来越多的研究倾向于认为该系统,特别是腹侧被盖区多巴胺能神经元存在较大的异质性.本文从腹侧被盖区多巴胺能神经元判定标准、解剖定位和投射特异性等角度对其在奖赏和厌恶刺激中的功能异质性进行综述,并对未来研究方向进行展望.