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Sex recognition in the leopard gecko, Eublepharis macularius (Sauria: Gekkonidae) Possible mediation by skin-derived semiochemicals

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Abstract

Male leopard geckoes,Eublepharis macularius, rely on skin-derived semiochemicals to determine the sex of conspecifics. Males respond to other males with agonistic behavior while females elicit courtship behavior from males. While females were shedding, males responded to them with agonistic behavior. The same females were courted both before and after shedding. An initial survey of hexane-extracted skin lipids from male and female geckoes revealed fatty acids common to both sexes. Several steroid analogs of cholesterol were unique to males while long-chain methyl ketones were unique to females. Results are discussed in the context of skin lipids serving as pheromones in reptiles.
... Chemical communication in lizards comes by means of the secretions of chemical signals and its vomerolfactory reception [5]. Chemical signals are secreted by epidermal glands such as the femoral follicular glands and the preanal glands, although metabolites in skin or in feces may also be important [8][9][10]. In addition to chemical signaling, visual signaling is widespread across lizards and consists of the context-dependent presentation of visually distinctive skin ornaments like dewlaps, proboscides, colorful parts of the body, changes in coloration, movement of the head, limbs or tail, among others [11]. ...
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It has been suggested that gymnophthalmids, like most semi-fossorial lacertoids, rely more in chemical cues to communicate, in comparison to other groups, like Iguanids, on which communication is mostly based on visual signaling. We present the first description of visual signaling in the Andean lizard Pholidobolusmontium (Gymnophthalmidae) and a complete ethogram based on ex situ observations (34 different types of behaviors including positions and simple movements). Through the design of conspecific stimulus experiments, we were able to recognize leg-waving as a visual signal, as it is only displayed in presence of conspecifics or in presence of a mirror and was one of first and most frequent displays in this context. We also detected other visual displays like neck-arching and tail-undulation which may also be relevant as visual signals. Based on our results, we propose that visual signaling is also possible in semi-fossorial lizards; however, further studies regarding chemical signal recognition and color detection are required to confirm our hypothesis.
... Lizards have multiple types of follicular epidermal glands, including femoral (Cole 1966;Garc ıa-Roa et al. 2017), precloacal (Escobar et al. 2001;Pincheira-Donoso et al. 2008), and cloacal glands, similar to some snake species (Trauth et al. 1987;Siegel et al. 2014). Some lizard (Mason and Gutzke 1990;Whiting et al. 2009) and snake species (Shine et al. 2002) also use skinderived chemical signals. For example, female snakes actively eject epidermal lipids to solicit male courtship using a suite of behaviors including scale movements, skin stretching, and hyperventilation (Garstka and Crews 1981). ...
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Lizards use chemical communication to mediate many reproductive, competitive, and social behaviors, but the neuroendocrine mechanisms underlying chemical communication in lizards are not well understood and understudied. By implementing a neuroendocrine approach to the study of chemical communication in reptiles, we can address a major gap in our knowledge of the evolutionary mechanisms shaping chemical communication in vertebrates. The neuropeptide arginine vasotocin (AVT) and its mammalian homologue vasopressin are responsible for a broad spectrum of diversity in competitive and reproductive strategies in many vertebrates, mediating social behavior through the chemosensory modality. In this review, we posit that, though limited, the available data on AVT-mediated chemical communication in lizards reveals intriguing patterns that suggest AVT plays a more prominent role in lizard chemosensory behavior than previously appreciated. We argue that these results warrant more research into the mechanisms used by AVT to modify the performance of chemosensory behavior and responses to conspecific chemical signals. We first provide a broad overview of the known social functions of chemical signals in lizards, the glandular sources of chemical signal production in lizards (e.g., epidermal secretory glands), and the chemosensory detection methods and mechanisms used by lizards. Then, we review the locations of vasotocinergic populations and neuronal projections in lizard brains, as well as sites of peripheral receptors for AVT in lizards. Finally, we end with a case study in green anoles (Anolis carolinensis), discussing findings from recently published work on the impact of AVT in adult males on chemosensory communication during social interactions, adding new data from a similar study in which we tested the impact of AVT on chemosensory behavior of adult females. We offer concluding remarks on addressing several fundamental questions regarding the role of AVT in chemosensory communication and social behavior in lizards.
... Different organs, femoral, precloacal, or urodaeal glands, can produce pheromones (Cooper and Trauth 1992;Cooper 1994;Sánchez-Martínez et al. 2007;Labra 2008). Less specific sources can also be involved such as the exudates of the body surface and feces (Mason and Gutzke 1990;López et al. 1998;Bull et al. 2000;Aragón et al. 2006;Labra 2008). ...
Chapter
The reproductive cycle of Galapagos giant tortoises has primarily been studied in captive individuals via noninvasive methodologies, including hormonal studies, radiographs, and ultrasound. During the annual reproductive cycle, mating peaks occur during the hot season months (December–June), followed by nesting during the cool season (June–December). Females dig flask-shaped holes in the soil typically in flat areas at lower elevations where soil suitable for digging accumulates. Females deposit 1–26 eggs and close nests with a mixture of urine, feces, and soil, which then dries into a hard cap, which seals in moisture and provides a protective layer for developing embryos. Rate of development and sex of the embryos depend on the temperature of the nest: when incubation temperatures are high (above 29.5°C) embryos become female and when temperatures are low (below 28°C) male. Eggs hatch after between 90 and 270 days of incubation. Young remain in the nest for up to 1 month until all eggs have hatched and consumed their yolk reserves. Hatchlings then dig an exit hole and emerge from the nest.
... One such combination of multimodal presentation could include sensory cues such as visual and/or olfactory presentation of a single characteristic (i.e. the colour or scent of floral blooms advertising a nectar reward; Faegri and Van Der Pijl (1971); Kelley et al. (2017)) or a complex whole conspecific presentation (i.e. presence of a female red-sided garter snake, leopard gecko, or Spanish terrapin, respectively, with high levels of integumental semiochemicals that serve as pheromones; Mason et al. (1989; Mason and Gutzke (1990); Ibáñez et al. (2012)), in which the visual sighting of a conspecific and/or the olfactory recognition of volatized chemical exudates from a conspecific could alert others to social or mating opportunities. While it is difficult to ascertain if visual or olfactory cues are more important in stimulating social interactions in most species, namely, if conspecifics prioritize sensory cues for maintaining those social interactions, a simpler question would be to ask about the role or importance of one type of information when other information is already present. ...
Article
Multimodal signalling reinforces specific messages in communication. In gopher tortoises, similar to other reptilian species, visualization of conspecific and chemical exudates from the skin may serve as a multimodal display advertising information about conspecific species, sex, or individual qualities, but this has not been fully elucidated. For gopher tortoises, one such possible source of chemical cues could be secretions from seasonally enlarged mental glands (MG). Here, we used both sexes of gopher tortoises in a paired choice presentation of MG secretions vs. distilled (DI) water on resin tortoise models to assess visual presence with tortoise-specific secretions. We examined behaviours to treatments to examine if MG secretions are recognizable olfactory cues and if visual cues alone are sufficient to maintain social interactions using a simple visual presentation vs. a complex visual and olfactory presentation. Tortoises of both sexes spent more total time (p < 0.001) and performed a greater number of behaviours (p < 0.001) towards the MG-treated model, relative to the neutral control (DI-treated model), suggesting that olfactory MG secretions are also required, along with visual presence of a tortoise, to engage in social behaviours. Our results are among the first for this species suggesting that pheromone usage may drive social interactions in social behaviours.
... Different organs, femoral, precloacal, or urodaeal glands, can produce pheromones (Cooper and Trauth 1992;Cooper 1994;Sánchez-Martínez et al. 2007;Labra 2008). Less specific sources can also be involved such as the exudates of the body surface and feces (Mason and Gutzke 1990;López et al. 1998;Bull et al. 2000;Aragón et al. 2006;Labra 2008). ...
Chapter
Reptiles have physiological, morphological, and behavioral adaptations that allow them to survive in desert environments, at high altitudes and in cold climates, such as the Patagonia region in southern Argentina. Knowledge of the ecology of Patagonian lizards is limited and fragmentary. The objective of this chapter is to present a synthesis of the current state of knowledge of the ecology of Patagonian lizards with regard to the use of (1) spatial resources (home range, use of microhabitats), (2) temporal resources (daily and seasonal patterns of activity), and (3) trophic resources (diet and nutrition strategies). We also discuss inter- and intra-species interactions, including predation, seed dispersal, parasitism, behavior, and resource partitioning. Keywords: Diet. Habitat. Use time. Behavior. Predation. Parasitism. Seed dispersal. Competition. Resource partitioning. Teiidae. Liolaemidae. Phyllodactylidae. Leiosauridae.
... Chemical cues are thoroughly studied in lizards for their roles in intrasexual aggression via male territoriality and mate competition, where substrate licking and rubbing are commonly exhibited behaviors [6]. In multiple species, male responses are contextual: they respond with courtship behavior to female scent and with aggression to male scent [22][23][24][25]. ...
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Squamate reptiles (snakes and lizards) rely on chemical cues from conspecifics to search the environment for potential mates. How such cues are used by invasive species to facilitate reproduction, especially seasonally, is a key question that can inform management practices. The Argentine black and white tegu (Salvator merianae) is an invasive reptile species in south Florida threatening native fauna in biodiverse regions such as Everglades National Park. While some information exists on the reproductive ecology of this species in its native range in South America, the chemical ecology of S. merianae is unclear especially in its invasive range. By testing both male (n = 7) and female (n = 7) tegus in a Y-maze apparatus, we assessed if either sex follows chemical trails left by conspecifics and if behaviors were sex- or season-specific. We conducted three types of trials where conspecifics created odor trails: Male-only (male scent only in base and one arm of Y), Female-only, and Male vs. female. Males did not preferentially follow scent trails from either sex, but they did differentially investigate conspecific scent from both sexes. Seasonally, males showed increased rates of chemosensory sampling (rates of tongue-flicking) during the spring (breeding season; March-May) compared to fall (non-breeding season; September-November). Males also had reduced turning and pausing behavior while trailing in the spring. Female tegus exhibited stronger conspecific trailing abilities than males, following both male and female scent trails, and they explored the maze less before making an arm choice. Females also investigated the scent trails intensely compared to males (more passes in scented arms, more time with scent trails). Our results demonstrate for the first time that females of an invasive reptile species can follow conspecific scent trails. Given the strong female responses to odor, sex-specific targeting of tegus via application of a conspecific chemical cue in traps could enhance removal rates of females during the breeding season.
... Males of the Leopard gecko routinely lick all individuals they meet. If the encountered animal is a female in breeding condition, the male starts his courting (Mason and Gutzke, 1990) with stilting postures, usually accompanied by tail vibrations (Ferkin and LaDage, 2006). Those are expressed only in the courting context in this species (Brillet, 1993). ...
Article
Complex visual signaling through various combinations of colors and patterns has been well documented in a number of diurnal reptiles. However, there are many nocturnal species with highly sensitive vision, being able to discriminate colors in night conditions, as was shown in geckos. Because of their sensitivity to chromatic signals, including UV (ultraviolet), they may have potential hidden features in their coloration, which may play role in intraspecific communication (e.g. mate choice) or interspecific signals (e.g. antipredatory function). We explored this hypothesis in nocturnal Leopard geckos (Eublepharis macularius), a species using visual signals in both antipredation defense and courtship, having ontogenetic color change accompanied by a shift in behavior. We used UV photography and visual modelling in order to compare various aspects of their coloration (luminance, contrast, color proportions) between sexes, age groups and populations. We found that Leopard geckos have considerable UV reflectance in white patches on their tails (and on the head in juveniles). Though, no prominent differences were detected in their coloration between various groups. We hypothesize that the limitation of UV reflectance to the head and tail, which are both actively displayed during defense, especially in juveniles, might potentially boost the effect of antipredation signaling.
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Self-recognition is the ability to recognise stimuli originating from oneself. Humans and most great apes show evidence of true self-recognition in the mirror test. They use their reflection to remove a mark that is only visible in the mirror. Not all animals, however, rely primarily on vision. In lizards, chemical cues are important in social interactions. A number of lizard species show chemical self-recognition but it has never been investigated in a gecko species. Here, we test the tokay gecko (Gekko gecko) a territorial species with parental care on their ability to discriminate their own skin and faecal chemicals from those of same-sex, unfamiliar conspecifics. Geckos show a higher response rate towards chemicals from unfamiliar individuals compared to self-produced chemicals and a water control. Lizards showed self-directed behaviour, responded stronger to skin chemicals and females responded more than males. Our study provides first evidence towards self-recognition and for a social function of chemical present on faeces in tokay geckos but further tests are needed to confirm true self-recognition. Tokay geckos are an excellent model species to investigate individual recognition to demonstrate more sophisticated social cognitive abilities than have previously been attributed to reptiles.
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All animals must move efficiently throughout their world. However, the mechanisms through which they accomplish this potentially vary among species. Previous work exploring the use of feature information and geometric information in movement through space has indicated that geometric information is commonly used and that some species sometimes also use feature information. Here, I investigated if a cold-blooded species, leopard geckos (Eublepharis macularius), would use geometric and/or feature information. In training, geckos learned to move to a correct corner within the box with a distinctive feature. In test when only geometric information was available, geckos chose either their assigned corner or its geometric opposite. In another test when feature information conflicted with geometric information, geckos did not use feature information and instead made choices consistent with using geometric information. This suggests geckos used geometric information preferentially to feature information in this experiment after both had been available throughout training when they were placed in conflict.
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Novelty recognition helps organisms identify changes over time. Studies to date have usually involved mammals, particularly rodents. We explored leopard geckos’ (Eublepharis macularius; Experiment 1) and tiger salamanders’ (Ambystoma tigrinum, Experiment 2) sensitivity to spatial and object novelty. We used an exploratory paradigm adapted from rodents where time spent near objects in an open-field box was compared. Subjects first habituated to three objects. To evaluate spatial novelty recognition, one object was moved to a new location. Subjects again habituated to the objects’ locations. To evaluate object novelty recognition, one object that had not been moved earlier was replaced with an unfamiliar object. Results indicated when one object was moved to a new location, geckos and salamanders spent more time near that spatially-displaced object. Additionally, when a familiar object was replaced with a new object, geckos and salamanders spent more time near the substituted object. These results suggest geckos and salamanders recognized changes in objects’ identities and locations. Geckos and salamanders acted differentially depending on familiarity in both spatial and object domains. These results support attempts to include lesser-studied species in our efforts to characterize cognition.
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