Chemical rival recognition decreases aggression levels in male Iberian wall lizards, <Emphasis Type="Italic">Podarcis hispanica</Emphasis>

In an agonistic interaction, the assessment of the probable outcome of future encounters with the same individuals may be the best way of decreasing costs of fighting, but this may only be accomplished if animals are able to recognize individual conspecifics. We staged encounters between male lizards, Podarcis hispanica, to examine whether odoriferous cues are involved in rival recognition during agonistic interactions. We experimentally manipulated the odour of intruding males, creating familiar males with their own odour or bearing odours of unfamiliar males, and unfamiliar males bearing unfamiliar odours or odours of familiar males. The results showed that when familiar males were impregnated with scents from unfamiliar males, they elicited an aggressive response by resident unmanipulated males similar to that observed for a new unfamiliar male with unfamiliar odour. This suggests that resident males were unable to recognize familiar males when their own scents were removed. In contrast, responding males were less aggressive towards familiar males impregnated with their own odour and towards unfamiliar males impregnated with scents of familiar males, suggesting that when two males have already interacted, their scents become familiar for both males, and that the detection in successive encounters of the familiar scent suffices to reduce the aggressive response of territorial males. Therefore, recognition mechanisms based on chemical cues during agonistic encounters may contribute to reducing the intensity and the costs of fighting in P. hispanica and may play an important role in the organization of their social system.     

Boldness and body size of male Spanish terrapins affect their responses to chemical cues of familiar and unfamiliar males

Recognition and avoidance of conspecifics based on chemical cues could reduce the risk of aggressive interactions between males. Success in agonistics encounters with unfamiliar males should be lower than with previously known familiar males. Then, males should avoid the chemicals from unfamiliar males with respect to those from familiar males. However, boldness and size could affect the outcome of encounters between males and, consequently, the response to chemical cues of conspecific males. We compared the time spent by male turtles Mauremys leprosa in water pools with chemical stimuli from unfamiliar or familiar males or with their own chemical stimuli. We also performed a behavioral test to estimate boldness of turtles in an antipredatory situation. Turtles avoided the chemicals from unfamiliar males respect to familiar ones and their own odors, but their responses depended on boldness and size of the tested turtle. Bold turtles avoided water with chemicals of unfamiliar males, but not with chemicals of familiar males, whereas shy turtles avoided chemicals of both familiar and unfamiliar males. On the other hand, large males avoided the odor from unfamiliar males, but small males did not avoid water with the odor from other males. Results suggest that male M. leprosa can detect chemicals released to water from conspecific males and discriminate between familiar and unfamiliar males. However, responses to these chemicals depended on boldness and body size of the responding turtle because these factors may affect intrasexual competition.     

Femoral secretions and copulatory plugs convey chemical information about male identity and dominance status in Iberian rock lizards (Lacerta monticola)

Socially dominant males often signal their status to rival males and/or females. We tested the hypotheses that Lacerta monticola femoral gland secretions and copulatory plugs convey chemical information about male identity and dominance status. We estimated male dominance status by staging male–male agonistic encounters in a neutral arena. We then conducted two experiments to compare male tongue-flick behavior toward chemical stimuli consisting of cotton swabs bearing (1) deionized water (control), the lizard’s own femoral secretions, and the femoral secretions of another male and (2) phosphate-buffered saline solution (control), the lizard’s own plug products, and the plug products of another male. Results indicate that males discriminated their own femoral secretions and plugs from those of other males. They also discriminated morphological attributes of other males that were associated with dominance status based on chemical cues arising from femoral secretions and discriminated the dominance status of other males based on chemical cues arising from the plugs. Femoral secretions that convey information about male identity and dominance status may be hypothesized to function in the establishment of L. monticola dominance hierarchies through scent-marking of territories. We suggest that copulatory plugs and femoral secretions may allow males to scent-mark the female body and postulate that this behavior may influence male and female reproductive decisions under selective pressures of sperm competition.     

Does reproductive state affect a lizard's behavior toward predator chemical cues?

We examined how reproductive state affected shifts in behavior of adult female Podarcis sicula toward chemical cues from a natural snake predator (Coronella austriaca). The oviparous P. sicula lizards do not experience a major physical burden during reproduction, but gravid females substantially increase duration of basking. Therefore, gravid lizards are likely to experience a greater risk of mortality because they are exposed to predators for longer periods. Both gravid and non-gravid females shifted patterns of locomotion when confronted with snake chemical cues, but the change was notably larger when females were non-gravid. When non-gravid, lizards responded to predator scent by increasing the number of stand-ups and starts, while such a response was not observed when females were gravid. By contrast, gravid lizards clearly reduced the time spent basking in the presence of predator scent, whereas no change in basking behavior was observed when females were non-gravid. Thus, females exhibit differential behavioral responses to predator scents that is dependent on reproductive state.     

Discrimination between related and unrelated individuals in the Australian lizard Egernia striolata

We examined evidence for kin-related signal discrimination in the Australian scincid lizard Egernia striolata, using 41 juvenile lizards from 14 litters from a population in the Mount Lofty Ranges, South Australia. We characterised each juvenile at four polymorphic microsatellite DNA loci, determined genetic relatedness among pairs of juveniles, and assigned for each litter one other litter that was genetically closest and one other litter that was genetically most distant. Lizards responded significantly more strongly, with tongue flicks and time in contact, to skin secretion stimuli from more distant than genetically close, unfamiliar conspecific juveniles. When presented with an intruder, juvenile lizards basked for shorter periods when the intruder was more distantly related, and aggressive lizards directed more aggressive acts towards more distantly related than closely related conspecific intruders. We deduce from these results that there is kin recognition in juvenile E. striolata, and that they are able to discriminate related from unrelated individuals among unfamiliar conspecifics.     

Effects of testosterone supplementation on chemical signals of male Iberian wall lizards: consequences for female mate choice

In some lizards, female mate choice is influenced by chemicals secreted by males, e.g., via the femoral glands. Secretions of the femoral glands are under direct androgenic control and vary seasonally with androgen production. However, whether increased testosterone (T) levels affect the concentration and chemical composition of secretions or their attractiveness to females is unknown. We manipulated T levels of male Iberian wall lizards, Podarcis hispanica, with silastic implants. Differential tongue-flick rates indicated that females detected and discriminated between femoral secretions of control and T-implanted males based on chemical cues alone. Females showed greater responses to secretions of T-males, which might suggest that T increased the concentration of chemical signals. Further analyses by gas chromatography–mass spectrometry indicated that T supplementation induced qualitative changes in lipid composition of femoral secretions. T-males had decreased relative proportions of cholesta-5,7-dien-3-ol in secretions, which might be related to the negative effects of T on the immune system and on lipid metabolism. However, experiments of choice of males’ scent showed that females neither preferred nor avoided the scent marks of T-males but preferred males that maintained higher proportions of cholesta-5,7-dien-3-ol in secretions, independently of the experimental manipulation. Thus, because this steroid is negatively affected by T, there might be trade-offs among increasing T levels to increase the production of chemical secretions, maintain metabolism, and attract females.     

Interpopulational differences in chemical composition and chemosensory recognition of femoral gland secretions of male lizards Podarcis hispanica: implications for sexual isolation in a species complex

Summary. Molecular studies suggest that the Iberian wall lizard, Podarcis hispanica, forms a species complex with several monophyletic types. In Central Spain two of these types are spatially not isolated and may interact. Sex pheromones are important for species recognition and, thus, differences between lizards’ types in chemicals used in intraspecific communication could lead to reproductive isolation. Analyses by GC-MS showed that the femoral gland secretions of adult males of different types were different. Males of one type had twelve exclusive compounds, and proportions of some shared compounds differed. This presumably would reflect selection for the persistency and efficiency of chemical signals in different environments; less volatile compounds and with a higher chemical stability being favoured in the type of lizards inhabiting more humid climatic conditions. Differential tongue-flick rates to scents from femoral secretions indicated that males were able to detect and discriminate between males of different types based on chemical cues alone. In contrast, females detected but did not seem able to discriminate between scents of the two types of males. Thus, multiple factors might be simultaneously acting either against or in favor of speciation, leading, on the one hand, to genetic differences between types, but, on the other hand, probably precluding an effective reproductive isolation in areas where both types of lizards may interact.     

The scent of sun worship: basking experience alters scent mark composition in male lizards

Signals used in female choice should honestly advertise the benefits that males can provide, with direct benefits often argued as being more important than indirect benefits. However, the nature of direct benefits in species without paternal care or nuptial gifts is poorly understood. Previous studies on lizards suggest that females decide where to settle and assumedly who to mate with based on information contained in scent marks from territorial males. Access to high-quality thermal resources is crucial for female reproductive success. Females may therefore be able to detect and exploit thermal-induced variation in the chemical composition of male scent marks when assessing the quality of his territory. We show that the amount of time male wall lizards (Podarcis muralis) are allowed to bask significantly alters the chemical composition of their femoral secretions used in scent marking. The direction of the change is consistent with adaptive plasticity to maintain signalling efficacy under warm conditions that increase evaporation of femoral secretions. The compounds affected by basking experience included those previously associated with male quality or shown to mediate male–male competition in lizards. However, whilst female lizards could discriminate between scent marks of males that had experienced different basking conditions, they did not preferentially associate with the scent from males from high-quality thermal conditions. These results highlight the potential importance of a previously neglected environmental effect on chemical signalling. We suggest thermal effects may have significant consequences for scent-mark composition in variable environments, with potential repercussions on olfactory communication in lizards.     

Chemosensory assessment of rival body size is based on chemosignal concentration in male Spanish terrapins

Assessment of the fighting ability of potential opponents is an essential skill to minimize the costs of agonistic interactions between males. Previous research showed that chemical cues released in the water by male turtles may convey information about body size, which is important for intrasexual competition. However, the mechanistic basis of such chemical signaling of body size remains poorly understood. Here, we aimed to experimentally examine whether the release of chemosignals is quantitatively or qualitatively dependent on body size in male Spanish terrapins Mauremys leprosa. We compared the time that turtles spent in a pool with clean water versus water containing chemical stimuli of conspecific males of different body sizes at two different concentrations (“diluted” or “undiluted”). Male terrapins avoided water with chemicals secreted by relatively larger males when these chemicals were undiluted, but not after the chemical stimuli were diluted. In contrast, male terrapins did not avoid chemicals of relatively smaller males in any treatment. Thus, male M. leprosa may assess the size of their rivals on the basis of the concentration or the amounts of their chemical cues released into the water and consequently avoid occupying these ponds with higher concentrations of chemicals. This study gives important hints about the mechanism of chemical signaling in freshwater turtles and demonstrates that male turtles may discriminate different concentrations of chemosignals of conspecifics and modify their behavior accordingly. Likewise, our results support the notion that relative body size is a key factor during male interactions in Spanish terrapins.     

Roles of male residence and relative size in the social behavior of Iberian rock lizards, Lacerta monticola

Many studies on contest competition used residency asymmetry as a discrete variable. However, the probability of winning an interaction may change as a continuous function of the value of the location where the encounter occurs. We performed a field study to examine the importance of location within a home range and relative body size to the outcomes of agonistic interactions between male lizards, Lacerta monticola. The distances to activity centers (the most used locations based on a density function of sightings) and relative size play important roles in agonistic interactions and had interacting effects in natural conditions. On the other hand, previous studies with lizards suggested that inferior competitors are able to avoid agonistic interactions in the field. Thus, we staged encounters in the laboratory to examine the behavioral responses of smaller individuals. The responses of each focal smaller male were measured in its own home cage (resident), in the cage of a larger male (intruder) and in a cage in which no male was previously present (control). The predominant behavioral tactics of smaller males were avoidance when they are the intruders and displaying when they are the residents. Submissive displays by smaller males may help reduce the costs of agonistic encounters.     

Habituation in the green frog, Rana clamitans

Habituation and its role in the dear enemy effect was investigated in a population of green frogs, Rana clamitans. Green frogs have a prolonged breeding season, and males defend territories centered around suitable oviposition sites. We tested the prediction that male green frogs will habituate to broadcasts of synthetic conspecific stimuli. Our results indicate that male green frogs can discriminate familiar from unfamiliar stimuli. We suggest that habituation helps to mediate the territorial interactions between male green frogs. Strangers present a greater threat than familiar neighbors. By habituating to the advertisement vocalizations of their near neighbors, males avoid costly interactions with individuals that are not a major threat to their territories. Received: 20 July 1998 / Accepted after revision: 6 September 1998     

Responses of female lizards,<Emphasis Type="Italic"> Lacerta monticola</Emphasis>, to males' chemical cues reflect their mating preference for older males

Female mate choice based on visual traits appears to be rare in lizards. Field observations suggest that females of the lizard Lacerta monticola preferred to mate with larger/older males. Although older males are usually green and larger, and younger males brown and smaller, there is some overlap in size and coloration between age classes. Thus, visual cues may not always be reliable indicators of a male's age. We hypothesized that female mate-choice preferences may be based on males' pheromones, which might transmit information about characteristics such as age. In a laboratory experiment, we analyzed the effect of age of males on attractiveness of their scents to females. When we offered scents of two males of different age, females associated preferentially with scents of older males. This suggested that females were able to assess the age of males by chemical signals alone, and that females preferred to be in areas scent-marked by older males. Thus, females may increase their opportunities to mate with males of high quality, or may avoid harassment by sneaking young males. This result agreed with field observations on females mating with old males, and rejection of advances by young males. Our results also suggested that female preference for older males may depend on their own body size. Large females showed a strong preference for older males, whereas smaller females were not so selective. This, together with males' preference for large females, might lead to size-assortative matings. We suggest that the quality and/or quantity of male pheromones could communicate to the female heritable male genetic quality (i.e. age) and thereby serve as the basis of adaptive female choice in lizards.Communicated by W.E. Cooper     

Symmetry, male dominance and female mate preferences in the Iberian rock lizard, Lacerta monticola

Female preference for dominant males is widespread and it is generally assumed that success in male-male competition reflects high quality. However, male dominance is not always attractive to females. Alternatively, relatively symmetric individuals may experience fitness advantages, but it remains to be determined whether males with more symmetrical secondary sexual traits experience advantages in both intra- and intersexual selection. We analysed the factors that determine dominance status in males of the lizard Lacerta monticola, and their relationship to female mate preference, estimated by the attractiveness of males' scents to females. Sexually dimorphic traits of this lizard (head size and femoral pores) appear to be advanced by different selection pressures. Males with relatively higher heads, which give them advantage in intrasexual contests, were more dominant. However, head size was unimportant to females, which preferred to be in areas marked by relatively heavier males, but also by males more symmetric in their counts of left and right femoral pores. Chemicals arising from the femoral pores and other glands might honestly indicate quality (i.e. related to the symmetry levels) of a male to females and may result from intersexual selection. Females may use this information because the only benefit of mate choice to female lizards may be genetic quality. Chemical signals may be more reliable and have a greater importance in sexual selection processes of lizards than has previously been considered.     

Sexual selection and species recognition in the pygmy swordtail, Xiphophorus pygmaeus: conflicting preferences

Sexual selection and species recognition play important roles in mate choice; however, sexual selection preferences may overlap with traits found in heterospecifics, producing a conflict between sexual selection and species recognition. We examined female preferences in Xiphophorus pygmaeus for male traits that could provide both types of information to determine how females use multiple cues when preferences for these cues would conflict. We also examined X. pygmaeus behavior in the field to determine if females have the opportunity to choose mates. As no male-male competition was observed in the field, and females occasionally chased males from feeding areas, females apparently have the opportunity to exercise mate choice in their natural habitat. In the laboratory, female X. pygmaeus used body size as a sexual selection cue, preferring large heterospecifics (X. cortezi) to small conspecifics. Females also preferred barless X. cortezi over barred X. cortezi when males were size matched. Because X. pygmaeus males do not have bars, this preference suggests that X. pygmaeus females use vertical bars in species recognition, and that large body size and vertical bars are conflicting cues. However, X. pygmaeus females did not have a preference for males of either species when sexual selection and species recognition cues were presented concurrently. This result was surprising, because preferences for species recognition cues are often assumed to be stronger than sexual selection cues. We suggest that females may be using additional species-specific cues in mate choice to prevent hybridization.     

Male Iberian rock lizards may reduce the costs of fighting by scent matching of the resource holders

Animals should adopt strategies to minimize the costs of intraspecific aggressive interactions. For example, individuals should be able to identify resource holders in advance and avoid fighting with them because residents are generally more likely than intruders escalate aggression. It has been suggested that scent marks function mainly to allow competitor assessment by conveying the costs of entering a scent-marked area. Individuals may identify territory owners by comparing the scent of substrate marks with the scent of any conspecific they encounter nearby, assessing whether these two scents match or not, a mechanism known as scent matching. Here, we examined the response of male Iberolacerta cyreni lizards to areas scent-marked by other males and the potential role of scent matching in agonistic interactions. We designed a laboratory experiment where we allowed a male to explore the scent-marked substrate of another male, and then we immediately staged agonistic encounters in a nearby clean neutral area with either the male that had produced the scent marks (matching treatment) or with a different non-matching individual male. The higher chemosensory exploratory rates of substrate scent marks in comparison to clean substrates suggested that males detected and spent more time exploring scent marks to obtain information on the donor male. Moreover, this information was later used to decide the fighting strategy. Intruding males delayed time until the first agonistic interaction, reduced the intensity of fights and the number of aggressive interactions, and won less interactions with males which scent matched that of scent marks (because they would be considered as the territory owners) than with other non-matching individuals. Our results show that male I. cyreni lizards use scent matching as a mechanism to assess the ownership status of other males, which could contribute to modulate intrasexual aggression, reducing costs of agonistic interactions.     

Courting male garter snakes (Thamnophis sirtalis parietalis) use multiple cues to identify potential mates

Mating aggregations of red-sided garter snakes (Thamnophis sirtalis parietalis) in Manitoba provide a unique opportunity to identify the cues that attract a male snake and induce him to court. The snakes are abundant, tolerate human presence, and males direct courtship to a subset of other males ("she-males") as well as to females. Previous work has emphasised the role of pheromonal cues (skin lipid profiles) as sexual attractants in snakes. However, pheromones are so widely distributed throughout the den area that these chemical cues may be difficult for males to use to localise females. Our field studies show that males and females differ in several other attributes such as size (females are larger than males), body temperature (very cold snakes are often females), muddiness (females are often covered in mud) and whether or not they are solitary (most females are surrounded by courting males). Experiments show that males use all of these cues to identify possible sexual partners. Visual and thermal cues are particularly important for solitary mate-searching males; but after a mating ball forms around a female, pheromones may be most important. Our study also reveals substantial variation among individuals: females vary in attractiveness, and males vary in their intensity of courtship as well as in the magnitude of their preference for one potential partner versus another. Thus, a male snake's "decision" whom to court depends not only on visual and thermal as well as chemical cues, but also on the male's own preferences and on subtle differences among potential sexual "targets".     

Does responsiveness to predator scents affect lizard survivorship?

Many prey organisms respond to predator scent by shifting behaviour. These alterations to behaviour are often assumed to increase an animal's chances of evading predators. Responsiveness to predator scents is therefore believed to ultimately increase a prey's chances of surviving encounters with predators. This notion is widely accepted among behavioural ecologists but has rarely been empirically tested. I staged encounters between adult snakes (Demansia psammophis) and pairs of unrestrained adult lizards (Lampropholis guichenoti) that responded strongly to snake predator scent ("responsive") or weakly to snake predator scent ("non-responsive"). Responsive lizards decreased activity and mobility during the staged encounters with snake predators. In turn this shift in behaviour decreased the chances that snakes detected responsive lizards. Since snakes almost always captured lizards that were detected, responding strongly to predator scent decreased a lizard's chances of being captured by predators. This finding is the first experimental demonstration in any terrestrial animal that responsiveness to predator scents can function to increase survival probability.     

Chemosensory recognition of the marbled whiptail lizard, Aspidoscelis marmorata (Squamata: Teiidae) to odors of sympatric lizards (Crotophytus collaris, Coleonyx brevis, Eumeces obsoletus and Uta stansburiana) that represent different predation risks

The ability of the whiptail lizard Aspidoscelis marmorata (Teiidae) to detect and discriminate chemical stimuli associated with the integument of a sympatric saurophagous lizard (Crotaphytus collaris) was tested. Females of A. marmorata were presented with cotton swabs containing chemical cues from C. collaris and three species of nonsaurophagous lizards, as well as water and cologne (pungency control), and total number of tongue-flick (TF) recorded. Other responses were assessed including directed TF rate, time from initial presentation of the stimulus to first TF (latency), time spent fleeing from the stimulus, and number of flight bouts. The number of TFs, directed TF rate, and number of attempts at fleeing exhibited by were significantly greater when females were presented with swabs containing cues from C. collaris as compared to nonsaurophagous lizards and both control treatments. A. marmorata required significantly less time to elicit their first TF when presented with cues from C. collaris as compared to all other treatments. Most previous studies have focused on the responses of lizards to cues associated with snake predators. This study provides the first available data on responses of a teiid to cues associated with a saurophagous lizard.     

Homing behaviour in the sleepy lizard (Tiliqua rugosa): the role of visual cues and the parietal eye

To investigate how visual cues are integrated into a navigational strategy for homing in the Australian sleepy lizard (Tiliqua rugosa), lizards were displaced beyond their home range, either with full access to visual cues or with no access to visual cues during the displacement. Homeward orientation was significantly worse when lizards were denied visual cues during the displacement than when they were not. However when lizards were displaced with their field of view restricted to the sky, their homeward orientation was equally as good as that of lizards displaced with no visual restriction. These experiments suggest that sleepy lizards use celestial cues to determine the compass bearing of the outward journey, and reverse this bearing to orient in the homeward direction (course reversal). In a subsequent experiment, lizards oriented randomly with respect to home when the parietal eye was entirely covered with a patch during the displacement and return, while control lizards fitted with a sham parietal eye patch were well oriented towards home. In both groups, the lateral eyes were unobstructed and had complete access to visual cues including celestial cues and landmarks. These results suggest that the parietal eye plays a highly significant role in sleepy lizard homing, perhaps mediating a sky polarization compass sense.     

Chemical polymorphism in male femoral gland secretions matches polymorphic coloration in common wall lizards (Podarcis muralis)

Previous studies showed that common wall lizards (Podarcis muralis) are polymorphic in colour, both sexes showing three main ventral morphs (white, yellow and red) within the same population and that the three morphs correlate with many life-history traits, including a positive assortative mating according to colour. Chemical communication plays a key role in intra-specific recognition and in social organization of lizards; thus chemical cues might be involved in morph recognition and mate choice. We used gas chromatography–mass spectrometry (GC–MS) to investigate possible differences in the lipophilic fraction of femoral gland secretions between size/age classes and to explore whether chemical secretions match male colour morphs. As expected, most males shared the same compounds, but smaller males showed significantly higher proportions of aldehydes, alcohols and ketones and significantly lower proportions of tocopherols than larger males. Interestingly, inter-morph differences in the proportion of some compounds (especially tocopherols and furanones) matched ventral colour polymorphism. Pairwise comparisons showed that white lizards had significantly different chemical profiles than both the yellow and red ones, whereas differences between yellow and red males were only marginal. A further canonical analysis of principal coordinates correctly classified 67.2 % on average of the chemical profiles according to colour morph (white 85.0 %, red 60.9 %, yellow 57.1 %). We hypothesized that chemical differences associated with colour polymorphism may play a central role in intra-specific communication and even in sexual selection, allowing individuals to choose their partners according to their age, and more interestingly according to their colour morph, in a non-random mating population system.