Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges

The threat sensitivity hypothesis assumes that multiple cues from a predator should contribute in an additive way to determine the degree of risk-sensitive behaviour. The ability to use multiple cues in assessing the current level of predation risk should be especially important to prey exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds or mammals by hiding inside rock crevices, where they may encounter another predator, the smooth snake, Coronella austriaca. We investigated in the laboratory whether chemical cues may be important to wall lizards for detection of snakes. The greater tongue-flick rate and shorter latency to first tongue-flick in response to predator scents indicated that lizards were able to detect the snakes' chemical cues. We also investigated the use of different predatory cues by lizards when detecting the presence of snakes within refuges. We simulated successive predator attacks and compared the propensity of lizards to enter the refuge and time spent within it for predator-free refuges, refuges containing either only visual or chemical cues of a snake, or a combination of these. The antipredatory response of lizards was greater when they were exposed to both visual and chemical cues than when only one cue was presented, supporting the threat sensitivity hypothesis. This ability may improve the accuracy of assessments of the current level of predation risk inside the refuge. It could be especially important in allowing lizards to cope with threats posed by two types of predators requiring conflicting prey defences.     

Can Wall Lizards Combine Chemical and Visual Cues to Discriminate Predatory from Non‐Predatory Snakes Inside Refuges?

The ability to use multiple cues in assessing predation risk is especially important to prey animals exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds in the open by hiding inside rock crevices, where they may encounter saurophagous ambush smooth snakes. Lizards should avoid refuges with these snakes, but in refuges lizards can also find non‐saurophagous viperine snakes, which lizards do not need to avoid. We investigated in the laboratory whether wall lizards used different predator cues to detect and discriminate between snake species within refuges. We simulated predatory attacks in the open to lizards, and compared their refuge use, and the variation in the responses after a repeated attack, between predator‐free refuges and refuges containing visual, chemical, or visual and chemical cues of saurophagous or non‐saurophagous snakes. Time to enter a refuge was not influenced by potential risk inside the refuge. In contrast, in a successive second attack, lizards sought cover faster and tended to increase time spent hidden in the refuge. This suggests a case of predator facilitation because persistent predators in the open may force lizards to hide faster and for longer in hazardous refuges. However, after hiding, lizards spent less time in refuges with both chemical and visual cues of snakes, or with chemical cues alone, than in predator‐free refuges or in refuges with snake visual cues alone, but there were no differences in response to the two snake species. Therefore, lizards could be overestimating predation risk inside refuges. We discuss which selection pressures might explain this lack of discrimination of predatory from similar non‐predatory snakes.     

Variability in the Assessment of Snake Predation Risk by Liolaemus Lizards

The ability to assess and respond to predation risk is a strong selective force. Detection of predators is carried out by one or more sensory modalities, but the use of chemoreception has significant advantages. This study examines the chemosensorial assessment of snake predation risk and corresponding behaviours in different species and populations of Liolaemus lizards naturally exposed to different levels of snake predation pressure. The species studied were sympatric (Liolaemus lemniscatus), parapatric (L. nigroviridis) and allopatric (L. fitzgeraldi) to the saurophagous snake, Philodryas chamissonis. Additionally, two populations of L. lemniscatus from areas differing in snake densities were compared. Chemo‐assessment of predation risk was determined by comparing the number of tongue‐flicks (TF) and the behavioural responses of lizards submitted to three treatments (with semiochemicals of snake, conspecifics, and without semiochemicals – control). The results suggest that Liolaemus lizards can chemo‐assess snake predation risk, but this was modulated by the predation pressure experienced by lizards in their natural habitats. When exposed to snake semiochemicals, the sympatric prey showed less chemical exploratory behaviour (i.e. lower number of TF), a higher frequency of antipredator behaviours that would reduce its detection by a predator, and did not show the behaviour triggered by conspecific semiochemicals. The parapatric prey showed similar number of TF across different treatments, suggesting an absence of recognition of snake semiochemicals; however, it did show antipredatory behaviours when confronted with snake semiochemicals. The allopatric prey showed similar behaviour in all treatments. Both populations of the sympatric species, L. lemniscatus, showed a similar ability to detect predation risk when confronted with snake semiochemicals (i.e. similar number of TF), but antipredatory behaviours were diminished, and marking behaviours were present in the population subject to lower predation pressure. Relaxed predation pressure from a predator that releases and detects semiochemicals had similar consequences at species and population levels.     

Antipredator behaviour of invasive geckos in response to chemical cues from snakes

Antipredator behaviours and the ability to appropriately assess predation risk contribute to increased fitness. Predator avoidance can be costly; however, so we expect prey to most strongly avoid predators that pose the greatest risk (i.e., prey should show threat sensitivity). For invasive species, effectively assessing the relative risk posed by predators in the new environment may help them establish in new environments. We examined the antipredator behaviour of introduced Asian house geckos, Hemidactylus frenatus (Schlegel), by determining if they avoided shelters scented with the chemical cues of native predatory snakes (spotted pythons, Antaresia maculosa [Peters]; brown tree snakes, Boiga irregularis [Merrem]; common tree snakes, Dendrelaphis punctulata [Grey]; and carpet pythons, Morelia spilota [Lacépède]). We also tested if Asian house geckos collected from vegetation vs. anthropogenic substrates (buildings) responded differently to the chemical cues of predatory snakes. Asian house geckos did not show a generalised antipredator response, that is, they did not respond to the chemical cues of all snakes in the same way. Asian house geckos avoided the chemical cues of carpet pythons more strongly than those of other snake species, providing some support for the threat‐sensitivity hypothesis. There was no difference in the antipredator behaviour of Asian house geckos collected from buildings vs. natural vegetation, suggesting that individuals that have invaded natural habitats have not changed their antipredator behaviour compared to urban individuals. Overall, we found some evidence indicating Asian house geckos are threat‐sensitive to some Australian predacious snakes.     

Systematics of the Southeast Asian mongooses (Herpestidae,Carnivora): solving the mystery of the elusive collared mongoose and Palawan mongoose

Although recent molecular studies have clarified the phylogeny of mongooses, the systematics of the Southeast Asian species was incomplete as the collared mongoose Urva semitorquata and some debatable taxa (Hose's mongoose, Palawan mongoose) were missing in the analyses. We sequenced three mitochondrial (cytochrome b, ND2, control region) and one nuclear (beta‐fibrinogen intron 7) fragments of the Southeast Asian mongooses to clarify the systematic position of the different species and populations occurring in this region. Our results showed that the collared mongoose is closely related to the crab‐eating mongoose Urva urva, these two species forming a sister‐group to the short‐tailed mongoose Urva brachyura. Despite Sumatran collared mongooses having a peculiar orange phenotype, we showed that they exhibited very little genetic divergence to individuals from Borneo. In contrast, the populations of the short‐tailed mongoose from Borneo were strongly divergent to those from Peninsular Malaysia and Sumatra, and these might represent separate species. Within the crab‐eating mongoose, we observed little geographical genetic structure. Our study suggests that Hose's mongoose is not a valid species. The Palawan mongooses did not cluster with the other populations of the short‐tailed mongoose; they were closer to the collared mongoose and should be included in this species. © 2014 The Linnean Society of London     

Olfactory Snake‐Predator Discrimination in the Cape Ground Squirrel

Small mammals have a number of means to detect and avoid predators, including visual, auditory and olfactory cues. Olfactory cues are particularly important for nocturnal or fossorial species where visual cues would not be as reliable. The Cape ground squirrel (Xerus inauris) is a semi‐fossorial, diurnal mammal from southern Africa. Cape ground squirrels encounter multiple species of predatory snake that pursue individuals underground where visual and social cues are limited. We assessed whether Cape ground squirrels use odours to discriminate between snakes by presenting a non‐venomous snake, a venomous snake and a control odour collected on polyethylene cubes to 11 adult female squirrels from 11 different social groups. Cape ground squirrels responded by inspecting the cube, displaying snake harassment–associated behaviours and decreasing time spent in close proximity to snake odours when compared with a control. They also displayed discrimination between two snake species by increasing the frequency of cube inspection and increasing harassment behaviours with venomous snake odours when compared with non‐venomous snake odours. We conclude that Cape ground squirrels respond with snake‐specific antipredator behaviours when presented olfactory cues alone. Olfactory discrimination may be maintained by the decreased utility of other methods of predator detection: sight and group detection, in below‐ground encounters.     

Chemoreceptive and behavioural responses of the common lizard Lacerta vivipara to snake chemical deposits

Behavioural cues were used to assay the capacity of common lizards to detect chemical deposits of snakes. The lizards were observed in cages that had been previously inhabited either by one of two species of snake that feed on lizards (the viper Vipera berus and the smooth snake Coronella austriaca), or the grass snake (Natrix natrix), which does not feed on lizards. As a control, the lizards were tested both in a clean cage and in one sprayed with a pungent odorant. The lizards responded to the snakes' chemicals by increased tongue-flick rates, with the highest rates being given in response to the deposits of their predators. The chemosensory examination of the snakes' odours induced a shift in general behaviour in response to the predator, but not to the non-predator chemical cues. This behavioural response consisted mainly of a disruption of the locomotor patterns. Our findings strongly suggest that lizards detected and distinguished between the chemicals deposited by three species of snake. Behavioural performances were highly variable among individual lizards in all trials, but the relative scores of individuals tended to be similar in response to different stimuli.     

Identification of 2-phenylethanol with a rose-like odor from anal sac secretions of the small Indian mongoose (Herpestes auropunctatus)

The small Indian mongoose (Herpestes auropunctatus) is an invasive species in Okinawa and Amami-Oshima, Japan. Major strategies for their eradication have been the use of baited traps, which suffer from decreasing efficiency with declining populations and the bycatch of native animals. To address these concerns, mongoose-specific lures are required. In this study, we aimed to identify species- and/or sex-specific compounds from anal sac secretions of small Indian mongooses. Volatile compounds emitted from male and female mongoose anal sac secretions were analyzed by thermal desorption-gas chromatography-mass spectrometry. In addition to several fatty acids, 2-phenylethanol was identified as a minor compound, which is uncommon in mammalian secretions but a dominant odorant in roses. Female samples emitted higher levels of 2-phenylethanol than male samples did. These findings indicate that 2-phenylethanol is a female-specific volatile compound of anal sac secretions in small Indian mongooses, and it may be useful as an ingredient of mongoose-specific scent lures.     

Molecular phylogeny of the Herpestidae (Mammalia, Carnivora) with a special emphasis on the Asian Herpestes

Until now, phylogenetic studies of the mongooses (Carnivora, Herpestidae) have not included an exhaustive sampling of the Asian members of this family. In this study, we used mitochondrial (Cytochrome b and ND2), nuclear (β-fibrinogen intron 7 and Transthyretin intron 1) sequences from almost all of the recognized mongoose species to produce a well-resolved phylogeny of the Herpestidae. We also performed molecular dating analyses to infer divergence dates of the different lineages within the Herpestidae. Our results confirmed the paraphyly of the Herpestes genus and other phylogenetic relationships, which previously had only been moderately supported. The Asian herpestid species were found to form a monophyletic group within the Herpestidae. Within the Asian species, a cyto-nuclear conflict was discovered between the small Indian mongoose (Herpestes auropunctatus), the Indian gray mongoose (Herpestes edwardsii) and the Javan mongoose (Herpestes javanicus), which may have occurred through interspecific hybridization. This study inferred an Early Miocene origin for the Herpestidae and a Middle Miocene origin for the Asian mongooses.     

The Relationship Between Foraging Ecology and Lizard Chemoreception: Can a Snake Analogue (Burton’s Legless Lizard,Lialis burtonis) Detect Prey Scent?

In lizards and snakes, foraging mode (active vs. ambush) is highly correlated with the ability to detect prey chemical cues, and the way in which such cues are utilized. Ambush-foraging lizards tend not to recognize prey scent, whereas active foragers do. Prey scent often elicits strikes in actively-foraging snakes, while ambushers use it to select profitable foraging sites. We tested the influence of foraging ecology on the evolution of squamate chemoreception by gauging the response of Burton's legless lizard ( Lialis burtonis Gray, Pygopodidae) to prey chemical cues. Lialis burtonis is the ecological equivalent of an ambush-foraging snake, feeding at infrequent intervals on relatively large prey, which are swallowed whole. Captive L. burtonis did not respond to prey odour in any manner: prey chemical cues did not elicit elevated tongue-flick rates or feeding strikes, nor were they utilized in the selection of ambush sites. Like other ambushing lizards, L. burtonis appears to be a visually oriented predator. In contrast, an active forager in the same family, the common scaly-foot ( Pygopus lepidopodus ), did tongue-flick in response to odours of its preferred prey. These results extend the correlation between lizard foraging mode and chemosensory abilities to a heretofore-unstudied family, the Pygopodidae.     

Conservation implications of small Indian mongoose (<Emphasis Type="Italic">Herpestes auropunctatus</Emphasis>) predation in a hotspot within a hotspot: the Hellshire Hills,Jamaica

This study documents impacts of the small Indian mongoose (Herpestes auropunctatus) on a threatened endemic fauna occurring in a biodiversity hotspot within a hotspot, the Hellshire Hills, Jamaica. We analyzed the stomach contents of 217 mongooses and supplemented this information with behavioural observations. The mongoose’s diet consists primarily of invertebrates and lizards, but bird feathers, mammal hair, and a small number of seeds were also recorded. Invertebrates and lizards accounted for 93% of identified prey items. Of special concern were the remains of threatened species such as the recently re-discovered blue-tailed galliwasp (Celestus duquesneyi), indicating that the mongoose may represent a considerable threat to this poorly known taxon. Dietary analyses did not reveal remains of the Critically Endangered Jamaican iguana (Cyclura collei), yet field observations confirmed that the mongoose is a potent predator of hatchling iguanas. Ignoring issues of sample size, this suggests that the analysis of stomach contents alone may mask important demographic impacts attributable to the mongoose (or other predator species). In other words, rare and endangered species may not be detected in diet samples, but the impact of predation may be of demographic significance for effected prey taxa. This study supports previous arguments concerning the negative impact of the mongoose on endemic insular species, and underscores the utility of employing field observations of mongoose foraging behaviour to provide important insights into the conservation implications of predation by non-native predators.     

Male southern water skinks (Eulamprus heatwolei) use both visual and chemical cues to detect female sexual receptivity

A wide range of organisms use chemical and visual cues in mate attraction and courtship; however, chemical discrimination relevant to reproduction and the interplay between these two types of communication are poorly understood in reptiles. We experimentally tested the ability of male Eulamprus heatwolei, a scincoid lizard, to discriminate between sexually receptive and non-receptive females in two ways. First, we conducted 155 staged encounters between males and females over 29 days to determine the start and the duration of the female receptive period based on the date of copulations. These data suggest that the receptive period lasted for approximately 7 days in late October under controlled laboratory conditions. We also recorded 6,330 individual male and female behaviours during these trials to evaluate the frequency of female courtship and rejection behaviours and the intensity of male courtship behaviour. Female courtship increased sharply during the receptive period and then diminished. The disparity between female courtship behaviours and female rejection behaviours was greatest during the receptive period. Male courtship intensity increased sharply prior to the receptive period, peaked during the receptive period and thereafter declined rapidly. To determine if males were using visual cues, chemical cues or both from females, we conducted an experiment during and after the receptive period wherein male lizards were presented with a choice of two retreat sites treated either with the odour of large sexually receptive females, odour of small sexually non-receptive females or no odour (control). Males preferred the scent of females over the odourless control, and analysis using a special form of a generalized linear model, the Bradley–Terry model, showed a clear order of retreat site preferences, with large sexually receptive females favoured over small non-receptive females over the odourless control. We speculate that males use vision to find females and then use their chemosensory ability to chemically evaluate female sexual receptivity once the pair are in close proximity.     

Fixed prey cue preferences among Dusky Pigmy Rattlesnakes (<Emphasis Type="Italic">Sistrurus miliarius barbouri</Emphasis>) raised on different long-term diets

Chemoreception is often crucial to the interaction between predators and their prey. Investigating the mechanisms controlling predator chemical preference gives insight into how selection molds traits directly involved in ecological interactions between species. In snakes, prey cue preferences are influenced by both direct genetic control and experience-based plasticity. We assessed prey preference in a group of Dusky Pigmy Rattlesnakes that had eaten only mice or lizards over a 5 year period to test whether genetics or plasticity primarily determine the preference phenotype. Our results provide evidence for genetic determination of preference for lizard chemical cues in pigmy rattlesnakes. Snakes preferred the scent of lizards, regardless of their initial diet, and the response to mouse scent did not differ from the water-only control. We discuss these findings in light of previous studies that manipulated snake diets over shorter timescales.     

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.     

Experimental analysis of retreat‐site selection by thick‐tailed geckos Nephrurus milii

Abstract Although animals use habitats non‐randomly in the wild, complex correlations among environmental features mean that proximate influences on habitat selection can be identified only by experimental manipulation of potential cues. Thick‐tailed geckos Nephrurus milii are large lizards that are widely distributed through southern Australia. These nocturnally active animals typically spend daylight hours under surface rocks. We presented captive geckos with alternative retreat‐sites (rock crevices) differing in attributes potentially relevant to habitat selection. The lizards showed strong preference for shelter‐sites that enhanced thermoregulation (warm rather than cool) and that reduced the animal's vulnerability to predators (narrow crevices with small openings and not containing the scent of a predatory snake). Horizontal rather than sloping crevices were also preferred. Overall crevice size and thickness of the overlying rock did not influence retreat‐site selection in the laboratory, but could be important in the field because of their influence on thermal regimes under rocks. The present study supports the idea that nocturnal reptiles base their selection of diurnal shelters on multiple aspects related to the fitness consequences of occupancy of alternative available retreat‐sites.     

Does human scent bias the survival of bird nests?

Human-scent contamination of bird nests and the human-made trails leading to them is suspected to influence nest survival by attracting or deterring predatory mammals. This paper (1) reviews studies in which human-scent contamination was suspected to have biased the survival of real and artificial nests by influencing the behaviour of predatory mammals, (2) summarizes the procedures used in attempts to mitigate human-scent contamination in nest-survival studies, and (3) describes procedures to enhance the design and interpretation of nest-survival experiments. The behaviour of various non-domesticated mammals is confirmed or suspected to be affected by human scent, so similar effects on nest predators are plausible. However, suggestions that human scent affects nest survival by influencing the behaviour of predatory mammals are poorly supported, due to a dearth of appropriately designed experiments. Some studies failed to include measures to reduce human-scent contamination, and the effectiveness of scent-mitigation methods used in other studies has seldom been verified. In addition, volatile compounds arising from soil and vegetation disturbed underfoot by field researchers may have confounded many nest-survival studies. Investigators have routinely inferred human-scent effects from post hoc predation patterns or have simply acknowledged possible human-scent effects among other potential influences of nest fate. Studies are needed of the effects of human scent using uniform methods of scent application and verified methods of scent mitigation, where the fates of different types of nests are examined under a range of field conditions. More fundamentally, studies of naïve and experienced mammals are needed to assess their responses to human scent and clarify its salience in wildlife disturbance.     

Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca

We exposed females of a highly placentotrophic viviparous scincid lizard (Pseudemoia pagenstecheri) to various environmental factors during pregnancy, and quantified the effects of these treatments on their offspring. The clear result was that the phenotypes of neonatal lizards can be substantially modified by the environment that their mother experiences during gestation. Restricting prey availability to the females reduced the size of their offspring. Limiting the females' basking opportunities delayed their seasonal timing of parturition, and modified body proportions (tail length relative to snout-vent length) of the neonates. More surprisingly, female lizards that were regularly exposed to the scent of sympatric lizard-eating snakes gave birth to offspring that were heavier, had unusually long tails relative to body length, and were highly sensitive to the odour of those snakes (as measured by tongue-flick responses). The neonates' antipredator responses were also modified by the experimental treatment to which their mother was exposed. The modifications in body mass, tail length and response to snake scent plausibly reduce the offspring's vulnerability to predatory snakes, and hence may constitute adaptive maternal manipulations of the neonatal phenotype. Received: 6 July 1998 / Accepted: 5 December 1998     

Floral visitors and ant scent marks: noticed but not used?

1. Bee behaviour when visiting flowers is mediated by diverse chemical cues and signals, from the flower itself and from previous visitors to the flower. Flowers recently visited by bees and hoverflies may be rejected for a period of time by subsequent bee visitors. 2. Nectar‐thieving ants also commonly visit flowers and could potentially influence the foraging decisions of bees, through the detection of ant trail pheromones or footprint hydrocarbons. 3. Here we demonstrate that, while naÏve bumblebees in laboratory trials are not inherently repelled by ant scent marks, they can learn to use them as informative signals while foraging on artificial flowers. 4. To test for similar activity in the wild, visitor behaviours at the flowers of Digitalis purpurea Linnaeus, Bupleurum fruticosum Linnaeus, and Brassica juncea (Linnaeus) Czernajew were compared between flowers that had been in contact with ants and those that had not. No differences were found between the two treatments. 5. The use of chemical foraging cues by bees would appear to be strongly dependent on previous experience and in the context of these plant species bees did not associate ant scent mark cues with foraging costs.     

Differential Avoidance of Snake Odours by a Lizard: Evidence for Prioritized Avoidance Based on Risk

Most studies of predator avoidance behaviours have focussed on single‐predator systems, despite the fact that prey often are confronted with predator rich environments. In the presence of more than one predator, prey may have to choose between avoiding one predator over another. How prey cope with exposure to several enemies simultaneously remains largely untested. In this study I set out to investigate if skinks showed preferential avoidance of snake odours based on the relative predation risk posed by different snake species. This relative predation risk was estimated using information on density, diet specificity and foraging habit of each snake species. I tested retreat‐site selection in two‐choice tests, where lizards chose between different combinations of control and snake treated retreat‐sites as well as two retreat‐sites treated with different snake species odours. Lizards preferred control–treated retreat‐sites to those treated with snake odours and showed a differential avoidance response to refuges treated with odours from different snake species. There was strong evidence to suggest that lizards preferentially avoided refuges with the odours of the snake that posed the greatest predation risk, the white‐lipped snake (Drysdalia coronoides). Naïve juvenile lizards were also tested and their response was similar to the adults demonstrating that the behaviour is innate and not the result of higher encounter rates of more common snake odours. To my knowledge this is one of the first studies to demonstrate that prey can prioritize avoidance to a single most dangerous predator in the face of several predators and conflicting avoidance responses.     

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.