Male Iberian Rock Lizards Research Articles

Proteins from femoral gland secretions of male rock lizards Iberolacerta cyreni allow self—but not individual—recognition of unfamiliar males

Individual recognition (IR) plays an important role in modulating social interactions of several animal species. IR may work at two fundamental levels: at class-level (CIR), if it allows group membership identification (e.g. familiar/unfamiliar), or at individual-level (true IR; TIR), if it allows uniquely recognizing conspecifics. Direct and indirect evidences suggest that many lizards are able to recognize conspecifics, notably using the secretions from femoral glands, specialized epidermal structures located in the cloacal region. Such secretions are made of a mix of lipids and proteins, the latter having been poorly studied but hypothesised to convey identity-related information. Using male Iberian Rock lizards, we set up bioassays to test the role of the protein fraction in IR, and specifically whether lizards: (1) can detect proteins from femoral glands, (2) can recognize their own proteins from those of an unfamiliar male (CIR) and (3) can distinguish between two unfamiliar protein signals (TIR). We found that femoral proteins can be actually detected, and the protein signal was enough to allow self-recognition, but not to distinguish between two unfamiliar males. These outcomes support the hypothesis that proteins from lizard femoral glands are used in intraspecific communication, at least at CIR level. The lack of TIR detection has three possible explanations: (1) finer IR abilities are actually absent in this species; (2) TIR requires a more complex and complete chemical signal or (3) a more prolonged and complete set of previous interactions among individuals is needed to lead to familiarity and TIR. The ability to individually distinguish conspecifics is at the basis of many social behaviours. While the sensorial channel through which individual recognition is achieved may vary, the structure of the signal is usually complex and it could be expected different components to play different roles, so which part of the signal is actually responsible for individual recognition? Lizards use the secretion of specialized epidermal glands for intraspecific chemical communication, including individual recognition. Being a mixture of lipids and proteins, we wondered if it was the protein fraction of the secretion (i.e. the heritable part) which conveys identity. Using male Iberian Rock lizards, we showed that proteins allow for self but not for true individual recognition, suggesting that a partial signature may be not enough.

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.

Female sensory bias may allow honest chemical signaling by male Iberian rock lizards

Some mate choice theories propose that only male signals that are honest and condition-dependent can be stable, while another hypothesis states that males evolve signals that exploit the sensory system of females. However, sensory traps might evolve into honest signals if they are differentially costly for males. We tested whether a pre-existing sensory bias for food chemicals explained chemosensory preferences of female Iberian rock lizards for male scents. We manipulated hunger levels of females and found that food-deprived females had increased chemosensory responses to chemical stimuli from both invertebrate prey and femoral secretions of males, but not to control water. Further tests suggested that cholesta-5,7-dien-3-ol (provitamin D3), a lipid found in both prey and males’ scent, may be one of the chemicals eliciting these responses. Moreover, hungry females spent more time on scent marks of males that had experimentally increased cholesta-5,7-dien-3-ol than on scent marks of males alone, whereas for control females this effect was not significant. We suggest that preexisting sensory bias for essential nutrients (i.e., provitamin D) may be the origin of similar female responses to male chemicals. However, previous studies have suggested that the allocation of these chemicals to ornaments is costly and only high quality males can afford it. Therefore, preexisting sensory bias for essential nutrients may further allow the evolution and maintenance of honest sexual displays.

Intersexual differences in chemosensory responses to selected lipids reveal different messages conveyed by femoral secretions of male Iberian rock lizards

AbstractThe effects of intrasexual selection (i.e., male-male competition) and intersexual selection (i.e., mate choice) may result on the evolution of different secondary sexual traits. We tested whether chemosensory responses of male and female Iberolacerta cyreni lizards to femoral secretion of conspecific males (a chemical sexual trait used in social behavior) were eliciting by different chemical traits. Tongue-flick essays showed that males and females had similar chemosensory responses to the femoral secretions of males, but males and females differed in the magnitude of their chemosensory responses to the different chemicals found in secretions. Moreover, responses to chemicals related to body size depended on the own body size of the responding male, but did not in females. These results might support that femoral secretions of males convey different messages for male or female I. cyreni lizards.

Status‐signalling chemical badges in male Iberian rock lizards

Summary Male competition for females often results in the evolution of conspicuous male traits that signal fighting ability or dominance status. Most studies examining mechanisms allowing these traits to function as reliable status signals (or badges) have focused on conspicuous visual or acoustic traits. However, many animals communicate chemically, and chemical traits alone may also signal male dominance status. We examined whether chemicals in femoral gland secretions of male Iberian rock lizards (Lacerta monticola monticola Boulenger 1905) may signal dominance status. In staged encounters, larger males were dominant over smaller ones. While controlling for male body size, males of higher dominance status produced femoral secretions with higher proportions of hexadecanol and octadecanol. Tongue‐flick assays showed that males were able to (1) discriminate, by chemosensory cues alone, the different concentrations of hexadecanol from other chemicals presented in femoral secretions; (2) respond aggressively towards hexadecanol while responding neutrally towards other chemicals; and (3) show differential chemosensory and aggressive behaviours towards hexadecanol according to their own dominance status. These results suggest that hexadecanol may be a reliable status badge. Moreover, because hexadecanol elicits male aggressive behaviour, subordinate males signalling high status (‘cheaters’) may end up paying high fighting costs. In addition, males that had higher dominance status, and that allocated higher proportions of hexadecanol to femoral secretions, had greater T‐cell immune responses. This result suggests a possible link between quality of the immune system, dominance status, and chemical signals.

Vitamin D and Sex: Vitamin D Supplementation Increases the Attractiveness of Males' Scent for Female Iberian Rock Lizards. Proc Biol Sci 273: 2619-2624, 2006.

Vitamin D and Sex: Vitamin D Supplementation Increases the Attractiveness of Males' Scent for Female Iberian Rock Lizards. Proc Biol Sci 273: 2619-2624, 2006.

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.

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.

Chemical Compounds from Femoral Gland Secretions of Male Iberian Rock Lizards, Lacerta monticola cyreni

In spite of the importance of chemoreception and chemical signals in the social organization of lizards, there are only a few studies examining the chemical composition of secretions of lizards used for scent marking. The secretion of the femoral glands of male Iberian rock lizards (Lacerta monticola cyreni) contains 44 lipophilic compounds, including several steroids (mainly cholesterol), and n-C6 to n-C22 carboxylic acids, and minor components such as esters of carboxylic acids, alcohols, squalene, and one lactone. These compounds were identified on the basis of mass spectra, obtained by GC-MS. Most lipids were detected in all individuals, although relative proportions of each chemical show a high interindividual variability. This variability might be related to the characteristics or physical and health condition of males and might be the basis of female choice based on chemical cues observed in this lizard species.

The Ontogeny of Spatio‐Temporal Tactics and Social Relationships of Adult Male Iberian Rock Lizards, Lacerta monticola

AbstractBehavioural aspects of many species may change through their ontogenetic trajectory. Mature males of the lizard Lacerta monticola present two types of colour phase, with bright green males being older, larger and more dominant than dull brown males. We hypothesized those ontogenetic differences in males’ competitive ability may lead to differences in spatio‐temporal tactics. In a field study, we did not find differences in the size of the home ranges or core areas of green and brown males. However, after controlling for size, green males had more exclusive areas than brown males. Green males also had higher levels of conspicuous activities than brown males. Green and brown males had different spatio‐temporal tactics within the day; green males used their home ranges more, were more active and had a higher degree of overlap with other males in the morning than in the afternoon. Brown males did not show these variations through the day. Green males participated in, and won more intrasexual agonistic interactions. Also, green males overlapped more extensively with areas of potential mates, and guarded females more often than brown males. These behavioural differences between males showed plasticity through ontogeny in the use of space, time and types of activity.

Sources of individual shy–bold variations in antipredator behaviour of male Iberian rock lizards

Individual animals from the same population, sex, age and reproductive status often respond differently and consistently to predators. One important dimension of this behavioural variation is the shy–bold continuum. Innate differences in boldness might explain why individuals differ in their antipredator behaviour. In a laboratory experiment, we examined the sources of individual variation in antipredator behaviour of adult male lizards Lacerta monticola. We simulated in the laboratory repeated predatory attacks of low or high risk and analysed activity levels and refuge use in both situations. Multivariate analyses suggested the existence of two consistent and independent shy–bold continua. The first described a gradient from bold lizards that spent shorter times in the refuge after predatory approaches to shy lizards with longer emergence times, whereas the other described a gradient from bold lizards with a low propensity to hide when the predator was close but risk was low to shy lizards that hid more often. We analysed whether morphological characteristics, body condition and health (estimated from their T cell immunocompetence) of individuals might account for the differences observed. Bold individuals had smaller absolute body size, but relatively larger heads, better body condition and better health. Bold individuals with a low propensity to hide when risk was low had larger absolute body sizes, whereas relative head size, and body condition and health were not important. We suggest that the position of an individual in the shy–bold continua might reflect its optimal antipredator behaviour, which would be a function of its health, general quality and ability to evade predators.

Copulatory plug displacement and prolonged copulation in the Iberian rock lizard (Lacerta monticola)

Male Iberian rock lizards (Lacerta monticola) produce copulatory plugs that adhere firmly inside the female cloaca and occlude both oviducts. These plugs do not prevent rival male insemination, as they neither re- duce female attractiveness or receptivity to rival males nor do they function as "chastity belts". Prior to copula- tion, males bite various regions of the female body, in- cluding the cloacal region. A previous plug in the female cloaca is expelled only after rival male intromission. We hypothesized that: (1) such male pre-copulatory be- haviours function to loosen plug adherence to the female cloaca, thereby facilitating intromission, and that (2) the hemipenis plays a role in displacing a previous plug prior to the delivery of a new plug. Neither of these hypotheses was supported. Instead, our results indicate that rival males can intromit the hemipenis past a previous plug in the female cloaca and deliver their own plug underneath it. Consequently, previous plugs are pushed away from the oviductal openings and even dislodged from the fe- male cloaca. Copulation duration was determined both by the time used by males to deliver a plug and by the fact that males prolonged copulation beyond plug delivery. There seemed to be sexual conflict over prolonged cop- ulation, which was resolved by the male/female head- length ratio. The adaptive value of Iberian rock lizard copulatory plugs and prolonged copulation in Iberian rock lizards is discussed in the context of sperm competition.

Differential Avoidance Responses to Chemical Cues from Familiar and Unfamiliar Conspecifics by Male Iberian Rock Lizards (Lacerta monticola)

We conducted a field study to analyze spatial relationships among male Iberian Rock Lizards, Lacerta monticola. We then used the same individuals in a laboratory experiment to test whether avoidance responses of a male lizard in a previously unknown area is affected by presence of scents of familiar and unfamiliar resident males. Time spent attempting to escape in presence of unfamiliar odors was significantly higher than in presence of familiar odors suggesting avoidance of unfamiliar scent marks, which may lower the costs of aggressive interactions. Our results are concordant with previous studies in which differential tongue-flick rates showed discrimination between odors of familiar and unfamiliar males of L. monticola.

Chemosensory discrimination of familiar and unfamiliar conspecifics by lizards: implications of field spatial relationships between males

The ability of territorial lizards to discriminate between scents of neighbors and non-neighbors might contribute to decreasing the costs of aggressive interactions. To test this hypothesis, we conducted a field study to analyze the spatial relationships between male Iberian rock-lizards, Lacerta monticola. We then used the same individuals in a laboratory experiment to test whether male lizards can use chemical cues to discriminate between familiar conspecific males (those whose home ranges overlapped) and unfamiliar conspecific males (those whose home ranges did not overlap, and whose home range centers were at least 50 m apart). Differences in tongue-flick rates in the presence of chemical cues suggested that male L. monticola discriminated between odors of familiar and unfamiliar males. The behavioral responses were also dependent on relative differences in body size between the responding male and the unfamiliar male that donated the scent: There was a significant negative correlation between tongue-flick rates emitted in cages of unfamiliar males and the body size differences between males. In contrast, when the donor of the scent was a familiar male, the tongue-flick rate was not dependent on body size differences. These results are compatible with individual discrimination through chemical cues in male L. monticola.

Discrimination of Femoral Gland Secretions from Familiar and Unfamiliar Conspecifics by Male Iberian Rock-Lizards, Lacerta monticola

Discrimination of Femoral Gland Secretions from Familiar and Unfamiliar Conspecifics by Male Iberian Rock-Lizards, Lacerta monticola

Social status of male Iberian rock lizards (Lacerta monticola) influences their activity patterns during the mating season

Not all individual lizards in a population are simultaneously active even when thermal conditions are suitable for activity. We examined inter-individual variability in activity levels of male Iberian rock lizards (Lacerta monticola) in a seminatural enclosure during the mating season, and analyzed whether social status affects their activity levels, time budgets, and body-mass changes. Activity levels of lizards varied significantly with time of day. However, activity levels of individual males were significantly correlated with their rank in the social hierarchy. When the males were active, their status did not influence the time spent basking, resting, or moving, but males with a higher status spent more time in social activities. Higher activity levels were costly, causing males to lose more body mass, although this could have been mainly due to the costs of maintaining a higher social status. We conclude that because attaining a higher status may require a male to be more active and more involved in agonistic encounters, subordinate individuals decrease their activity in order to decrease the costs of social behavior.

Social status of male Iberian rock lizards (<i>Lacerta</i> <i>monticola</i>) influences their activity patterns during the mating season

Social status of male Iberian rock lizards (<i>Lacerta</i> <i>monticola</i>) influences their activity patterns during the mating season

Immunocompetence of nestling great tits in relation to rearing environment and parentage

Theoretical models of host–parasite coevolution assume a partially genetic basis to the variability in susceptibility to parasites among hosts, for instance as a result of genetic variation in immune function. However, few empirical data exist for free–living vertebrate hosts to support this presumption. In a cross–fostering experiment with nestling great tits, by comparing nestlings of the same origin we investigated (i) the variance in host resistance against an ectoparasite due to a common genetic origin, (ii) the effect of ectoparasite infestation on cell–mediated immunity and (iii) the variance in cell–mediated immunity due to a common genetic origin. Ectoparasitic hen fleas can impair the growth of nestling great tits and nestling growth was therefore taken as a measure of host susceptibility. A common origin did not account for a significant part of the variation in host susceptibility to fleas. There was no significant overall effect of fleas on nestling growth or cell–mediated immunity, as assessed by a cutaneous hypersensitivity response. A common rearing environment explained a significant part of the variation in cell–mediated immunity among nestlings, mainly through its effect on nestling body mass. The variation in cell–mediated immunity was also related to a common origin. However, the origin–related variation in body mass did not account for the origin–related differences in cell–mediated immunity. The results of the present study thus suggest heritable variation in cell–mediated immunity among nestling great tits.