Blind date: female fossorial amphisbaenians prefer scent marks of large and healthy males.

Selecting a good mate is a decision with important fitness consequences. For this reason, mate choice has promoted the evolution of sexual ornaments signaling the quality of an individual. In fossorial animals, inhabiting visually restricted underground environments, chemical senses should be very important for mate choice. We examined whether sexual chemical signals (substrate scent marks) produced by males of the Iberian worm lizard, Blanus cinereus, a strictly fossorial blind amphisbaenian, provide information to females on morphological traits and health state. We administered corticosterone (CORT) to males simulating a continuous stressor affecting their health. Females preferred settling at sites scent-marked by males in comparison with similar sites with female scent or unmarked sites, but the attractiveness of males' scent differed between individuals. Females preferred scent marks of larger/older males and with a higher immune response, while their body condition and CORT treatment were unrelated to female preferences. Chemical analyses showed that proportions of some compounds in precloacal secretions of males (used to produce scent marks) were correlated with the morphological (body size) and health state (immune response and body condition, but not CORT treatment) of these males. These results suggest that females may make site-selection decisions based on assessing the chemical characteristics of males' scent marks, which were reliably related to some of the traits of the male that produced the scent. Therefore, females might use chemical senses to increase the opportunities to find and mate with males of high quality, coping with the restrictions of the subterranean environment.

Coping with drought? Effects of extended drought conditions on soil invertebrate prey and diet selection by a fossorial amphisbaenian reptile.

Arid climates are characterized by a summer drought period to which animals seem adapted. However, in some years, the drought can extend for unusually longer periods. Examining the effects of these current extreme weather events on biodiversity can help to understand the effects of climate change, as models predict an increase in drought severity. Here, we examined the effects of "unusual" extended drought on soil invertebrate prey availability and on diet composition (based on fecal contents) and diet selection of a fossorial amphisbaenian, the checkerboard worm lizard Trogonophis wiegmanni. Weather data show interannual variations in summer drought duration. The abundance and diversity of soil invertebrates in spring were high, and similar to those found in a "normal" early autumn, after some rain had ended with the summer drought. In contrast, in years with "unusual" extended drought, abundance, and diversity of soil invertebrates in early autumn were very low. Also, there were seasonal changes in amphisbaenians' diet; in autumn with drought, prey diversity, and niche breadth decreased with respect to spring and autumns after some rain had fallen. Amphisbaenians did not eat prey at random in any season, but made some changes in prey selection that may result from drought-related restrictions in prey availability. Finally, in spite that amphisbaenians showed some feeding flexibility, their body condition was lower in autumn than in spring, and much lower in autumn with drought. If extended drought became the norm in the future, amphisbaenians might suffer important negative effects for their health state.

Effects of Anthropogenic Disturbance of Natural Habitats on the Feeding Ecology of Moorish Geckos.

Urbanization and anthropic influences can drastically modify a natural habitat and transform it into an easily recognizable "urban habitat". Human activities can also induce less severe modifications of what apparently might still look like natural habitats. Therefore, these subtle alterations may be hidden but can still cause important negative effects on plant and animals. In contrast, some species seem able to take advantage of these anthropic alterations. Here, we examined the possible effects of the anthropogenic disturbance of an apparent natural habitat on the feeding ecology and body condition of Moorish geckos, Tarentola mauritanica. For this, we compared microhabitat structure, invertebrate availability, the diet composition (estimated from fecal contents), diet selection patterns and body condition of the two populations of geckos inhabiting two contiguous small islands. These islands have similar environmental characteristics, but highly contrasting differences in urbanization and anthropogenic influence. We found that, although the abundance of potential invertebrate prey was similar on both habitats, the diversity of invertebrate prey was lower in the altered habitat. As a consequence, although composition of the diet of geckos was similar on both islands, the diversity of prey and food niche breadth were lower in the altered habitat, and patterns of diet selection changed. However, these inter-habitat differences did not seem to affect the body size and body condition of geckos. We discuss how flexibility in feeding ecology may allow some species to cope with small anthropic disturbances of the habitat.

Intersexual and body size-related variation in chemical constituents from feces and cloacal products involved in intraspecific communication of a fossorial amphisbaenian.

Background: Many animals rely on chemical cues for intraspecific communication. This is especially important in fossorial animals because visual restrictions of the underground environment limit the opportunities for visual communication. Previous experiments showed the ability of the amphisbaenian Trogonophis wiegmanni to discriminate between several categories of conspecifics based on chemical cues alone. However, in contrast with many other reptile species, T. wiegmanni does not have external secretory glands, but uses uncharacterized secretions from the cloaca in intraspecific chemosensory communication. Methods: Using gas chromatography-mass spectrometry (GC-MS), we analyzed the lipophilic compounds from feces and cloacal products freshly extracted from the cloaca of male and female T. wiegmanni. We identified and estimated relative proportions of the compounds found, and tested for intersexual and body-size related differences. Results: We found a total of 103 compounds, being some steroids (mainly cholesterol and cholestanol), some alkanes and squalene the most abundant and frequent. Further, we found intersexual differences, with males, especially larger ones, having higher proportions of several alkanes between C13 and C24 and of squalene than females, which had higher proportions of several steroids and also of nonacosane and methylnonacosane than males. We compared these findings with secretions of other animals and discuss the potential role of these compounds and their variations in intraspecific communication of amphisbaenians.

Relationships between soil pollution by heavy metals and melanin-dependent coloration of a fossorial amphisbaenian reptile.

Melanin is the basis of coloration in many animals, and although it is often used in communication, thermoregulation, or camouflage, melanin has many other physiological functions. For example, in polluted habitats, melanin can have a detoxifying function. Melanic coloration would help to sequester in the skin the heavy metal contaminants from inside the body, which will be expelled to the exterior when the skin is sloughed. Moreover, animals should have evolved more melanic colorations in more polluted habitats ("industrial melanism" hypothesis). We examined whether the fossorial amphisbaenian reptile, Trogonophis wiegmanni, is able to eliminate heavy metals, derived from soil pollution by seagull depositions, through sloughing its skin. Our results suggest a covariation between levels of soil pollution by heavy metals and the concentration of heavy metals in the sloughed skins of amphisbaenians. This suggests that amphisbaenians may expel heavy metals from their bodies when they slough the skins. We also tested whether amphisbaenians inhabiting soils with higher levels of heavy metal pollution had darker (melanin-dependent) body colorations. However, contrary to predictions from the "industrial melanization" hypothesis, we found a negative relationship between soil pollution and proportions of melanic coloration. This contradictory result could, however, be explained because heavy metals have endocrine disruption effects that increase physiological stress, and higher stress levels could result in decreased melanogenesis. We suggest that although amphisbaenians might have some detoxifying mechanism linked to melanin in the skin, this process might be negatively affected by stress and result ineffective under conditions of high soil pollution.

Hidden but Potentially Stressed: A Non-Invasive Technique to Quantify Fecal Glucocorticoid Levels in a Fossorial Amphisbaenian Reptile.

To understand wildlife responses to the changing environment, it is useful to examine their physiological responses and particularly their endocrine status. Here, we validated an enzyme immunoassay (EIA) to non-invasively quantify fecal corticosterone metabolites (FCM) in the fossorial amphisbaenian reptile Trogonophis wiegmanni from North Africa. We supplemented animals assigned to the treatment group with corticosterone dissolved in oil applied non-invasively on the skin for several days, while control groups received the oil-alone solution. Fresh feces were collected at the end of the supplementation period, and FCM levels were quantified by an EIA. Basal FCM levels were similar for both treatments and increased at the end of the test, but FCM increased significantly more in corticosterone-treated animals. A further examination of FCM levels in a wild population of this amphisbaenian did not find overall sexual, size or seasonal differences but showed a high range of variation among individuals. This suggests that different uncontrolled intrinsic or local environmental variables might increase the circulating glucocorticoid levels of different individuals. Our results confirmed the suitability of EIA for analyzing physiological changes in FCM in this amphisbaenian species. This technique may be useful for understanding and remediating the little-explored potential stressors of the soil environment that may negatively affect the health state of fossorial reptiles.

Soil pollution by heavy metals correlates with levels of faecal glucocorticoid metabolites of a fossorial amphisbaenian reptile.

Soil degradation may have strong negative consequences for soil biodiversity, but these potential effects are understudied and poorly understood. Concentration of nesting seabirds may be a source of soil pollution by heavy metals, which are incorporated into the food chain and may have toxicological effects in vertebrates, especially in fossorial animals with low dispersal ability. We examined whether contamination by heavy metals, derived from seagull depositions, and other soil characteristics, may affect the levels of faecal glucocorticoid metabolites (as a potential indicator of physiological stress) of the fossorial amphisbaenian reptile Trogonophis wiegmanni. We found a relationship between soil pollution by heavy metals and increased levels of faecal corticosterone metabolite of the amphisbaenians that live buried in those soils. This can be due to the strong endocrine disruption effect of heavy metals. In addition, there was an independent effect of the soil texture, with amphisbaenians showing higher levels of faecal corticosterone metabolite in soils with less sand and more silt and clay, which are more energetically costly to dig. Long-term exposure to high glucocorticoid levels might have serious effects on health state and fitness of fossorial animals that may be unnoticed. Our study emphasizes that, to prevent future conservation problems, we need to perform periodic surveys on the physiological health state of the little-known subterranean biodiversity.

Foraging decisions of rock lizards may be dependent both on current rival assessment and dear enemy recognition.

Foraging strategies aim to maximize the amount of food obtained while minimizing searching costs. To reduce these costs, animals use different strategies based on the use of personal or social information to exploit food patches. At the same time, the social attraction for food resources could increase competition intensity for them. Prior experiences of animals regarding social risk and the foreknowledge of the competitors might drive the foraging strategies. In this paper, we examined experimentally whether rock lizards used behavioural strategies to reduce the risks of foraging in presence of potential competitors. We measured the foraging behaviour of a lizard resident to a territory (i.e. terrarium), in the presence of both familiar and unfamiliar conspecifics (potential competitors). We considered whether foraging choices between two food sources of different value (i.e. quantity) are influenced by familiarity with the intruder and the evaluation of its competitive ability based on body size differences between lizards. We found differences in the number of attacks performed to the best food source, with more attacks when the intruder was unfamiliar. The results suggest evidence of both dear enemy recognition and current rival assessment modulate the foraging choices depending on the identity and the social relationship with the intruder.

Going underground: short- and long-term movements may reveal the fossorial spatial ecology of an amphisbaenian.

BACKGROUND: The movement and spatial ecology of an animal depends on its morphological and functional adaptations to its environment. In fossorial animals, adaptations to the underground life help to face peculiar ecological challenges, very different from those of epigeal species, but may constrain their movement ability. METHODS: We made a long-term capture-recapture study of the strictly fossorial amphisbaenian reptile Trogonophis wiegmanni to analyze its long-term movement patterns. We also used passive integrated transponder (PIT) telemetry to detect and follow undisturbed individuals underground, obtaining data of their short-term movement patterns. RESULTS: Amphisbaenians showed a high site fidelity, moving short distances and over small areas, and spending some days without any noticeable movement, even under favorable conditions. We also found differences in movements between sexes and age classes. CONCLUSIONS: This movement and spatial strategy can be related to the energetic constrains of underground burrowing, or to the low metabolic requirements of fossorial reptiles, as distances and areas covered were much smaller than for epigeal reptiles of similar size. Individual differences probably reflect differential reproductive and social requirements of males and females, and that younger individuals might show more floating behavior until they can settle in a territory. This study is a rare example describing the movement ecology of a fossorial species and may contribute to the general understanding of the factors that affect space use and movement decisions in animals.

Maternal diet affects juvenile Carpetan rock lizard performance and personality.

Differences in both stable and labile state variables are known to affect the emergence and maintenance of consistent interindividual behavioral variation (animal personality or behavioral syndrome), especially when experienced early in life. Variation in environmental conditions experienced by gestating mothers (viz. nongenetic maternal effects) is known to have significant impact on offspring condition and behavior; yet, their effect on behavioral consistency is not clear. Here, by applying an orthogonal experimental design, we aimed to study whether increased vitamin D3 content in maternal diet during gestation (vitamin-supplemented vs. vitamin control treatments) combined with corticosterone treatment (corticosterone-treated vs. corticosterone control treatments) applied on freshly hatched juveniles had an effect on individual state and behavioral consistency of juvenile Carpetan rock lizards (Iberolacerta cyreni). We tested the effect of our treatments on (a) climbing speed and the following levels of behavioral variation, (b) strength of animal personality (behavioral repeatability), (c) behavioral type (individual mean behavior), and (d) behavioral predictability (within-individual behavioral variation unrelated to environmental change). We found higher locomotor performance of juveniles from the vitamin-supplemented group (42.4% increase), irrespective of corticosterone treatment. While activity personality was present in all treatments, shelter use personality was present only in the vitamin-supplemented × corticosterone-treated treatment and risk-taking personality was present in corticosterone control treatments. Contrary to our expectations, behavioral type was not affected by our treatments, indicating that individual quality can affect behavioral strategies without affecting group-level mean behavior. Behavioral predictability decreased in individuals with low climbing speed, which could be interpreted as a form of antipredator strategy. Our results clearly demonstrate that maternal diet and corticosterone treatment have the potential to induce or hamper between-individual variation in different components of boldness, often in interactions.

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.

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.