Chemosensory discrimination of male age by female Psammodromus algirus lizards based on femoral secretions and feces

Chemical communication plays an essential role in several social and reproductive behaviors of many animals. In lizards, the main sources of semiochemicals are femoral or pre‐anal gland secretions and feces. In male lizards Psammodromus algirus, there are age‐related differences in the chemical composition of femoral gland secretions and in the reproductive strategies, with older males defending territories and females, while younger males adopting sneak‐mating strategies. Females flee more often from mating advances of young males than from those of old males, which are more successful in obtaining matings. This suggests that age discrimination of males may be important for females. We tested here whether females showed differential chemosensory responses to chemical cues (femoral gland secretion and feces) of males of two age classes, and whether females use information from substrate scent marks of males of different ages to select where to stay. We found that females elicited more tongue‐flicks to the secretion and feces of old males than to control or secretion and feces of young males. Also, the time spent by females on a scented paper depended on the treatment, suggesting that females tended to spend more time on scent marks made with femoral secretions of old males. Adult females seemed capable to discriminate between young and old males based on chemical cues alone and showed more interest in scents of old males. However, substrate scent marks did not seem to entirely determine site selection by females, suggesting that females might need additional cues to perform the choice. These results can be explained by the different age‐dependent reproductive strategies of males, which can affect differentially to females.     

鳄蜥对熟悉和陌生个体气味的辨别

个体辨别对于减少同种争斗以及配偶选择具有重要意义。我们用棉棒粘取鳄蜥(Shinisaurus crocodilurus)尿液作为气味源,以香水作为对照,测定鳄蜥对熟悉个体气味、陌生个体气味以及香水的舔舌次数和舔舌潜伏期,来探讨鳄蜥通过化学信息辨别熟悉和陌生个体的能力。结果显示,不论是雌性还是雄性,对不同个体尿液的舔舌次数均显著高于对香水的,舔舌潜伏期显著短于香水的;尽管雄性对陌生同性个体气味与熟悉同性个体气味的舔舌次数无显著差异,但对前者的舔舌潜伏期显著短于后者;雄性对陌生雌性气味的舔舌次数显著多于熟悉雌性气味的,对前者的舔舌潜伏期显著短于后者;雌性对陌生雄性气味的舔舌潜伏期显著短于对熟悉雄性气味的;雄鳄蜥对陌生雌性气味的舔舌次数显著多于雌鳄蜥对陌生雄性的。结果表明,鳄蜥能辨别同种个体的化学信息,并能通过化学信息来辨别熟悉和陌生个体,推测鳄蜥的这种辨别能力对其领域分配以及繁殖交配有重要作用。     

Chemosensory Recognition of Familiar and Unfamiliar Conspecifics by the Scincid Lizard Eumeces laticeps

The ability of broad-headed skinks (Eumeces laticeps) to distinguish familiar from unfamiliar individuals of the opposite sex and themselves from other individuals of the same sex using only chemical stimuli was examined experimentally. Cloacal chemical stimuli were presented to lizards on moistened cotton swabs and numbers of tongue-flicks performed in 60 s were recorded. Males emitted significantly greater numbers of tongue-flicks in response to chemical cues from unfamiliar females than of female cagemates. Response rates of males housed with females and males housed alone to chemical stimuli from unfamiliar females did not differ. Chemical stimuli from unfamiliar males elicited significantly more tongue flicks from males than their own or deionized water, but their own stimuli elicited no more than the odourless control. Females tongue-flicked significantly more in response to cloacal chemical stimuli from unfamiliar males than from male cagemates. The findings indicate that both sexes of broad-headed skinks can discriminate between chemical stimuli of familiar and unfamiliar individuals of the opposite sex and that males can distinguish their own cloacal chemicals from those of unfamiliar males. The possible functions of these chemosensory capacities, including location of mates by scent-trailing and assessment of the presence of sexual competitors, are discussed in relation to the social behaviour of E. laticeps.     

Pheromonal discriminations of sex,reproductive condition,and species by the lacertid lizard Podarcis hispanica

In some vertebrate taxa, pheromones provide important information about species, sex, reproductive condition, kinship, and even individual identity. Because they possess highly developed nasal chemosensory systems, lizards are capable of many chemical discriminations, but many aspects of their pheromonal communication remain poorly understood even in major families. We report that males of a lacertid lizard, Podarcis muralis, are capable of differential response to surface chemical cues from conspecific males and females, from gravid and nongravid females, and from conspecific females and females of the closely related sympatric congener, P. bocagei carbonelli. In 60 sec trials in which stimuli from the femoral, cloacal, lateral, and upper body surfaces were presented to males on cotton swabs, males tongue-flicked at significantly higher rates to stimuli from conspecific females than males, from conspecific nongravid than gravid females, and from conspecific than heterospecific females. Responses to stimuli from conspecific males did not differ from those to distilled water. Together with previous findings that males can distinguish between chemical cues from familiar and unfamiliar males, these findings suggest that pheromones provide male P. hispanica important information regarding the presence of sexual rivals and the reproductive condition of potential mates without visually encountering other lizards. A growing body of literature indicates that lacertids are capable of sophisticated pheromonal discriminations that may play important roles in their social behavior.     

Lipophilic compounds in femoral secretions of male collared lizards,Crotaphytus bicinctores (Iguania,Crotaphytidae)

In many lizards, chemical compounds from the femoral gland secretions are used in intraspecific communication, but most studies describing these chemicals are for lizard species included in the Scleroglossa clade, whereas lizards within the Iguanian clade have been much less studied, probably because these lizards were considered to rely more on visual cues. However, many iguanian lizards have abundant femoral secretions and are able of chemosensory conspecific recognition, which might be based on compounds secreted by femoral glands. By using GC–MS analyses, we found 58 lipophilic compounds in femoral gland secretions of male Great Basin collared lizard, Crotaphytus bicinctores (Iguania, Crotaphytidae). Main compounds were steroids (mainly two triunsaturated steroids and cholesterol), carboxylic acids (mainly hexadecanoic acid), waxy esters of long chain fatty acids, alcohols (mainly hexadecanol), aldehydes and other minor compounds. We compared these compounds with those found in other lizard species and discussed the potential signaling function of some compounds and how the xeric habitat of this lizard could have conditioned the composition of secretions.     

Rival recognition in the territorial tawny dragon (Ctenophorus decresii)

The ability to discriminate between familiar and unfamiliar conspecifics is important in territorial animals as it allows animals to distinguish neighbours from non-neighbours. This prevents wasting time and energy in unnecessary aggressive interactions. I investigated the ability of adult males of a territorial lizard, the tawny dragon (Ctenophorus decresii), to distinguish familiar from unfamiliar rivals in a laboratory setting. Males significantly reduced their aggression levels in repeat interactions with familiar rivals and increased their aggression levels towards unfamiliar males. The time taken for interactions to be settled was also significantly lower towards familiar than unfamiliar males. The results of this study suggest that adult male tawny dragons can discriminate familiar from unfamiliar conspecifics. Furthermore, animals were presented with three new rivals in succession and showed a robust ability to discriminate between familiar and unfamiliar males.     

Male collared lizards,Crotaphytus collaris (Sauria: Crotaphytidae), signal females by broadcasting visual displays

The signalling function of displays broadcast when animals are distant from conspecifics can be difficult to determine. I tested the extent to which visually transmitted broadcast displays given by free‐ranging territorial male collared lizards signalled same‐sex rivals or females. One test involved recording the frequency of broadcast displays, aggressive contests with rivals, and courtship encounters with females during ten reproductive seasons when local sex ratios varied markedly. The frequency of broadcast displays decreased as the ratio of male competitors to females increased. The frequency with which males initiated contests with rivals was not related to the ratio of competitors to females, whereas the frequency of courtship interactions decreased with sex ratio because there were fewer females to court. The behaviour of males that defended territories during two successive seasons showed a similar pattern. Broadcast display frequency was positively correlated with courtship frequency, but not with the frequency of contests with rivals. Lastly, individual males gave more broadcast displays during focal observations when they also engaged in courtship encounters with females than other observations when they engaged in aggressive conflicts with rival males. Although these results do not reject the possibility that broadcast displays may also signal male rivals, they support a major role of these displays in advertisement to females. © 2013 The Linnean Society of London     

Chemical communication in the lacertid lizard Podarcis muralis: the functional significance of testosterone

Chemical signals are essential for intersexual communication in many animals, including lizards. While faeces have been suggested to contain socially relevant chemical stimuli, epidermal gland secretions are generally believed to be the leading source of chemosignals involved in lizard communication. Early research has shown that sex hormones affect epidermal gland activity, with androgens stimulating gland/pore size and/or gland productivity. However, the functional significance of hormone‐induced glandular activity in lizard chemical communication remains unclear. In this study, we manipulated testosterone (T) concentrations in male Podarcis muralis lizards. While T‐supplementation did not change pore size, it did increase secretion production substantially. Chemosensory tests showed that female conspecifics tongue‐flick at a higher rate and more quickly towards the secretion of males with experimentally increased T levels than towards the secretion of control males, suggesting that females can discriminate between males with dissimilar T levels based on chemical cues of secretion alone. Based on the scent of faeces, however, females were unable to discriminate between males with differential T levels. Also, females reacted more quickly when offered larger amounts of secretion – irrespective of whether secretions were obtained from control or T‐increased males. This result indicates that secretion quantity affects chemosignal detectability in Podarcis muralis.     

Vitamin D supplementation increases the attractiveness of males' scent for female Iberian rock lizards

Evolutionary theory proposes that signals used in sexual selection can only be stable if they are honest and condition dependent. However, despite the fact that chemical signals are used by many animals, empirical research has mainly focused on visual and acoustic signals. Vitamin D is an essential nutrient for lizards, but in some lizards its precursor (cholesta-5,7-dien-3-ol=provitamin D) is found in femoral gland secretions, which males use for scent marking and intraspecific communication. By allocating provitamin D to secretions, males might need to divert vitamin D from metabolism. This might be costly and condition dependent. We tested whether diet quality affected chemical signals of male Iberian rock lizards (Lacerta monticola) and its consequences for sexual selection. After experimental supplementation of dietary vitamin D, males increased the proportion of provitamin D in femoral secretions. Further experiments showed that females detected these changes in males' signals by chemosensory cues, and discriminated provitamin D, and changes in its concentration, from similar steroids (i.e. cholesterol) found in secretions. Moreover, females preferred areas scent marked by males with more provitamin D in their secretions. This mechanism would confer honesty to chemical signals of male lizards, and, thus, females may rely on it to select high-quality males. We suggest that the allocation of vitamins and other essential nutrients to either visual (e.g. carotenoids) or chemical ornaments might be the common basis of honest sexual displays in many animals.     

Lipophilic compounds in femoral secretions of males and females of the El Hierro giant lizard Gallotia simonyi (Lacertidae)

Many lizards use femoral gland secretions in reliable intraspecific communication. Based on mass spectra, obtained by GC–MS, we found 57 lipophilic compounds in femoral secretions of males and females of El Hierro giant lizards, Gallotia simonyi (fam. Lacertidae). Compounds included steroids (mainly cholesterol) and fatty acids ranging between n-C₁₆ and n-C₂₂ (mainly hexadecanoic and octadecanoic acids), followed by aldehydes, alcohols, ketones, squalene and waxy esters. There were important intersexual differences in the presence, abundance and number of compounds (more numerous in males). Males had higher proportions of the most odoriferous compounds (fatty acids and aldehydes), while females had higher proportions of more stable compounds (steroids, waxy alcohols, waxy esters and terpenoids). This suggests sexual differences in function of femoral secretions. In addition, some compounds could reflect the physiological state, allowing monitoring health of lizards from secretions samples, which is especially important given the critical conservation status of this lizard.     

Discrimination of chemical stimuli in conspecific fecal pellets by a visually adept iguanid lizard,Crotaphytus collaris

Iguanid lizards are known for visual acuity and a diminished vomeronasal organ, which has led to mixed conclusions on whether iguanids use chemical cues. The collared lizard, Crotaphytus collaris, is a territorial iguanid that lives in open rocky habitats. Fecal pellets placed prominently on open rocky perches may provide an ideal mechanism for intraspecific chemical signaling. In order to determine whether collared lizards can discriminate between chemical stimuli found in conspecific fecal pellets, we collected 24 males and 25 females to analyze sex-specific behavioral responses via tongue-flicks and a newly observed behavior for the species, gular pumps, to cotton swabs containing water, cologne, chemical stimuli from conspecific male and female fecal pellets, and the lizard’s own fecal pellet. Both sexes were able to discriminate chemical stimuli from water via at least one behavior. Male collared lizards exhibited greater rates of response (tongue-flick and gular pumps) toward male fecal pellets when compared to the negative water control. Our results also suggest individuals may be able to discriminate between fecal pellets, as indicated by generally greater (but non-significant) counts of male tongue-flick responses to male fecal pellets when compared to their own. Collared lizard chemical discrimination appears to utilize tongue-flick and gular pump behaviors, possibly associated with distinct chemosensory modes (vomerolfaction and olfaction). Based on this study, we suggest that chemical signals may play a greater role in intraspecific communication than previously thought in this highly visual lizard.     

Scent may signal fighting ability in male Iberian rock lizards

Intrasexual competition favours the evolution of conspicuous fighting ability badges. However, in spite of the fact that chemoreception is important in sexual selection of many animals, such as lizards, the role of chemical signals in males' contests is relatively unknown. Here, we show that proportions of cholesterol in femoral gland secretions of male Iberian rock lizards were related to their body size (which confers a competitive advantage in fights). Males discriminated chemically and responded aggressively to cholesterol stimuli presented on swabs. Moreover, we experimentally increased cholesterol in the scent of males, and staged encounters in neutral cages between two unfamiliar and size-matched males. Focal males lost more agonisitic interactions against males manipulated with cholesterol than in control tests. We suggest that differences in scent composition may reliably signal fighting ability in many lizard species, which would help to avoid the costs of fighting.     

Epidermal glands in cordylid lizards,with special reference to generation glands

We investigated inter‐ and intraspecific variation in epidermal gland characteristics in cordylid lizards. Our particular interest was whether a causal relationship exists between the presence of generation glands and lifestyle, i.e. in rock‐dwelling or ground‐dwelling lizards. We established that both femoral and generation glands are always present in adult males, but that species can be divided into three categories on the basis of the presence of these glands in adult females: both femoral and generation glands absent; femoral glands present, but generation glands absent; and both femoral and generation glands present. The absence of epidermal glands in females appears to be the basal condition in the Cordylidae. All cordylid species are sexually dimorphic as far as generation gland number is concerned, with females having consistently less glands than males. Gland number in females is strongly affected by climate, being lower in cooler compared with warmer environments. In males, there is no clear geographical pattern, although in some clades males of high‐altitude species have more generation glands than males of species occurring at lower altitudes. At least four of the five ground‐dwelling species in the family display unique generation gland characteristics, compared with rock‐dwelling species, reflecting the continued importance of generation glands in terrestrial environments. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158 , 312–324.     

Conspecific odor detection by the male broad-headed skink, Eumeces laticeps: effects of sex and site of odor source and of male reproductive condition

Olfactory stimuli are sufficient for detection and discrimination of sex of conspecific lizards by the male broad-headed skink, Eumeces laticeps, a member of a large group of lizards with pronounced chemosensory abilities, the Autarchoglossa. The capacity of male broad-headed skinks to detect conspecific odors was assessed by measuring tongue extrusion rates in response to odor stimuli presented on moist cotton applicators. Tongue-flick rates of postreproductive males were significantly higher for cloacal odors of postreproductive conspecifics of both sexes than to distilled water and higher to female than male odors over the initial 20- and 60-sec intervals. In a second experiment using testosterone-treated males and estrogen-injected females, testosterone-treated males emitted significantly more tongue flicks to female cloacal odors than to the other stimuli, and two males bit applicators bearing male odors. Testosterone did not affect reaction to male cloacal odors, but markedly increased tongue-flick rates in response to cloacal odors of estrogen-treated females. Postreproductive males also responded to female, but not male, skin odors at a significantly higher rate than to water. Possible sources and presumed adaptive significance of conspecific odors are discussed.     

In Space and Time: Territorial Animals are Attracted to Conspecific Chemical Cues

Territorial animals lay scent marks around their territories to broadcast their presence, but these olfactory signals can both attract and repel conspecifics. Attraction or aversion can have a profound impact in terms of space use and thereby influence an individual's access to resources and mates. Here, we test the impact of chemical signals on the long‐term space use and activity of receivers, comparing the response of males and females, territory holders, and temporary visitors in Sceloporus undulatus lizards in the field. We placed either male femoral gland secretions (chemical) or blank (control) cues on resident male landmarks, repeatedly over 5 d, while monitoring the activity and location of all lizards in the vicinity. We found that resident males and females, but not non‐resident males, were active on more days near landmarks treated with chemical cues than landmarks treated with control cues. Non‐resident males remained closer to chemical than control cues. These results suggest that territorial scent marks are attractive to conspecifics and impact space use, but that the specific effects depend on receiver sex and residency status. Such subtle or gradual changes in behavior may frequently be overlooked by short‐term choice experiments. Future studies investigating the behavioral significance of a communicative signal should consider these finer details of behavior for a more comprehensive assessment.     

Responses to oral gland scents from different males in Columbian ground squirrels

Acrylic cubes carrying oral gland scents from strange, neighbouring, and resident male Columbian ground squirrels (Spermophilus columbianus), plus a cube with no scent, were presented near the home burrows of squirrels in the field. Adult males and adult females sniffed scented cubes longer than unscented cubes, sniffed cubes with scent from other (strange and neighbouring) males longer than cubes with the resident male's own scent, and sniffed cubes with scent from strange males longer than cubes with scent from neighbouring males. Males also scent-marked the cubes on a number of occasions; differences in the frequency with which the cubes were marked followed the same pattern. It thus appears that adult Columbian ground squirrels can recognize familiar as opposed to unfamiliar males, and may also be able to determine individual identity, through oral gland scent. An ability to distinguish familiar from unfamiliar males by scent could be advantageous in facilitating differential treatment of wandering strange males versus established neighbours.     

Size-Dependent Chemosensory Responses to Familiar and Unfamiliar Conspecific Faecal Pellets by the Iberian Rock-Lizard, Lacerta monticola

We conducted a field study to analyse the social relationships between males of the Iberian rock lizard (Lacerta monticola). The degree of familiarity was determined based on the degree of overlap between their home ranges. We then designed a laboratory experiment to test whether the same males were able to discriminate between familiar and unfamiliar conspecifics using faecal pellet odours. Differential tongue‐flick rates suggest that large males (snout‐to‐vent length, SVL > 75 mm), at least, may discriminate between odours of familiar and unfamiliar males. The behavioural responses were dependent on relative differences in body size between the responding male and the male that donated the faecal pellet. Thus, as responding small males increased in size relative to their corresponding familiar male, their rate of tongue‐flicking significantly decreased; this was not the case in response to unfamiliar males. In contrast, there were no significant correlations between the response of large males to familiar or unfamiliar male stimuli, regardless of size differences. These results suggest that chemical cues contained in faecal pellets allow individual recognition in male L. monticola, and that the response depends on body size. We suggest that faecal pellets might be used to scent‐mark home ranges, which would contribute to lowering the costs of aggressive interactions.     

New compounds, sexual differences, and age-related variations in the femoral gland secretions of the lacertid lizard Acanthodactylus boskianus

Integumental gland secretions in lizards have been postulated to play a role as semiochemicals, but few studies have analysed the chemical nature of the gland secretions used in communication. We analysed the femoral gland secretions of Acanthodactylus boskianus using GC–MS, compared secretions of both sexes and different ages of males. For the first time in reptiles monoglycerides of fatty acids and glycerol monoethers of long chain alcohols were identified. In addition, alcohols, steroids, carboxylic acids, alkanes, amides, aldehydes, carboxylic acid esters, and squalene occurred. Sexual differences and age correlation in the amount of all major groups of compounds occurred, as such these results strengthen the theory that these secretions are used as semiochemicals. This work lays the foundations to test in future the role of chemical cues in mate choice and dominance hierarchies in lizards and to test the activity of compounds in behavioural assays to eventually identify the pheromones.     

Interpopulational Variations in Sexual Chemical Signals of Iberian Wall Lizards May Allow Maximizing Signal Efficiency under Different Climatic Conditions

Sexual signals used in intraspecific communication are expected to evolve to maximize efficacy under a given climatic condition. Thus, chemical secretions of lizards might evolve in the evolutionary time to ensure that signals are perfectly tuned to local humidity and temperature conditions affecting their volatility and therefore their persistence and transmission through the environment. We tested experimentally whether interpopulational altitudinal differences in chemical composition of femoral gland secretions of male Iberian wall lizards (Podarcis hispanicus) have evolved to maximize efficacy of chemical signals in different environmental conditions. Chemical analyses first showed that the characteristics of chemical signals of male lizards differed between two populations inhabiting environments with different climatic conditions in spite of the fact that these two populations are closely related genetically. We also examined experimentally whether the temporal attenuation of the chemical stimuli depended on simulated climatic conditions. Thus, we used tongue-flick essays to test whether female lizards were able to detect male scent marks maintained under different conditions of temperature and humidity by chemosensory cues alone. Chemosensory tests showed that chemical signals of males had a lower efficacy (i.e. detectability and persistence) when temperature and dryness increase, but that these effects were more detrimental for signals of the highest elevation population, which occupies naturally colder and more humid environments. We suggest that the abiotic environment may cause a selective pressure on the form and expression of sexual chemical signals. Therefore, interpopulational differences in chemical profiles of femoral secretions of male P. hispanicus lizards may reflect adaptation to maximize the efficacy of the chemical signal in different climates.     

Chemosensory Recognition of Familiar and Unfamiliar Conspecifics by Juveniles of the Iberian Wall Lizard Podarcis hispanica

Chemosensory recognition of familiar conspecifics has been reported in studies with members of several lizard families and may be advantageous to distinguish between intruders and neighbors or group members. However, few species have been studied and information on the ability to discriminate between familiar and unfamiliar conspecifics by chemosensory means is lacking for most lizard families. In this paper we ask whether juveniles of the Iberian wall lizard Podarcis hispanica (Lacertidae), can discriminate between chemical signals from familiar conspecifics with whom they have shared a terrarium for several months and those from unfamiliar conspecifics housed in a different terrarium. Experimental trials were conducted by transferring juveniles to a test terrarium with a filter paper substrate. We tested the responses of lizards to paper substrates labeled by familiar cage-mates, unfamiliar conspecifics, or unlabeled. Tongue-flicks and other behaviors in response to pheromonal stimuli were recorded for 10 min Juveniles directed more chemosensory behavior towards paper substrates bearing chemicals from familiar conspecifics than towards similar paper substrates labeled by unfamiliar conspecifics. These results indicate that juveniles in this lizard species can recognize familiar conspecifics and discriminate between familiar and unfamiliar individuals using only chemical stimuli. We discuss the role of habituation in familiar conspecific recognition and review possible explanations of the functional significance of this type of discrimination in lizards.