Alejandro Ibáñez

Sexually dichromatic coloration reflects size and immunocompetence in female Spanish terrapins, Mauremys leprosa

Many studies have shown the importance of colorful ornamentation in mate choosiness or intrasexual conflict. However, research on color ornaments has focused mainly on birds, lizards or fish, but remains practically unknown in other animal groups such as turtles. In addition, female ornaments and their relation with sexual selection also remain almost unknown. Here, we measured the coloration of the shell and the limb stripes of male and female Spanish terrapins Mauremys leprosa and explored the existence of sexual dichromatism and the relation of color characteristics with body size and health state estimated from the immune response to the injection of an antigen (phytohaemagglutinin test). Our results showed that shell coloration, which could be constrained by natural selection to be cryptic, changed with body size, but did not differ between sexes. In contrast, females had brighter and less ultraviolet-saturated and more orange-saturated limb stripes than males. In females, interindividual variation in limb stripe coloration was related with body size and immune response suggesting that this coloration may inform honestly about multiple traits that could be important in sexual selection. In contrast, coloration of limb stripes of males was duller than in females, and was not related with any trait suggesting that coloration is not important in sexual selection for males.

Reproductive state affects hiding behaviour under risk of predation but not exploratory activity of female Spanish terrapins

Female investment during reproduction may reduce survivorship due to increased predation risk. During pregnancy, the locomotor performance of gravid females might be diminished due to the additional weight acquired. In addition, egg production may also increase thermoregulatory, metabolic and physiological costs. Also, pregnant females have greater potential fitness and should take fewer risks. Thus, females should ponder their reproductive state when considering their behavioural responses under risky situations. Here, we examine how reproductive state influence risk-taking behaviour in different contexts in female Spanish terrapins (Mauremys leprosa). We simulated predator attacks of different risk levels and measured the time that the turtles spent hiding entirely inside their own shells (i.e. appearance times). We also assessed the subsequent time after emergence from the shell that the turtles spent immobile monitoring for predators before starting to escape actively (i.e. waiting times). Likewise, we performed a novel-environment test and measured the exploratory activity of turtles. We found no correlations between appearance time, waiting time or exploratory activity, but appearance times were correlated across different risk levels. Only appearance time was affected by the reproductive state, where gravid females reappeared relatively later from their shells after a predator attack than non-gravid ones. Moreover, among gravid females, those carrying greater clutches tended to have longer appearance times. This suggests that only larger clutches could affect hiding behaviour in risky contexts. In contrast, waiting time spent scanning for predators and exploratory activity were not affected by the reproductive state. These differences between gravid and non-gravid females might be explained by the metabolic-physiological costs associated with egg production and embryo maintenance, as well as by the relatively higher potential fitness of gravid females.

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.

Chemosensory discrimination of conspecifics in the juvenile yellow-spotted river turtle Podocnemis unifilis

Chelonians are very promising models to explore the role of chemical communication in social contexts. However, it still remains unknown how chemical signals may influence most behavioural patterns in turtles. In this study, we examined whether juvenile yellow-spotted river turtles (Podocnemis unifilis) use chemical cues released into water by other conspecifics to orientate towards them. To test our hypothesis, we compared the behavioural response (i.e., activity level and latency time) of juveniles when exposed to chemical stimuli obtained from other conspecifics (i.e., other juveniles and adult females), as compared to their response in clean water (i.e., the baseline). The results obtained in the study showed that juvenile P. unifilis increased their activity in response to chemical cues of female adult conspecifics. These findings suggest that juvenile turtles may chemically orientate themselves towards adult females during migratory processes. Efficient detection of conspecific chemical cues by juveniles is necessary for particular individuals to aggregate before migrating to habitats with more abundant food resources. Our study provides a framework for future research that should disentangle the role of chemical cues in mass migration of freshwater turtles.

Absence of haemoparasite infection in the fossorial amphisbaenian Trogonophis wiegmanni

Blood parasites such as haemogregarines and haemosporidians have been identified in almost all groups of vertebrates. However, very little is known about biodiversity of these parasites and their effects on some major groups of reptiles such as amphisbaenians, a distinctive group with many morphological and ecological adaptations to fossorial life. Conditions of the fossorial environment might also affect host-parasite relationships. We investigated the presence and the potential prevalence of three genera of haemoparasitic aplicomplexan blood parasites (Hepatozoon, Plasmodium and Haemoproteus) in the amphisbaenian Trogonophis wiegmanni, a fossorial worm lizard species from North West Africa. Blood parasite infection was not detected in T. wiegmanni, both in visual surveys of blood smears and using molecular methods to detect DNA of such parasites in the blood of the potential amphisbaenian hosts. We discuss how conditions of the fossorial environment might affect blood parasitaemias in amphisbaenians as well as in other fossorial reptiles.

Prevalence and genetic diversity of blood parasite mixed infections in Spanish terrapins, Mauremys leprosa

Blood parasites such as haemogregarines and haemosporidians have been identified in almost all groups of vertebrates and may cause serious damages to their hosts. However, very little is known about biodiversity of these parasites and their effects on some groups of reptiles such as terrapins. Moreover, the information on virulence from blood parasites mixed infection is largely unknown in reptiles. With this aim, we investigated for the first time the prevalence and genetic diversity of blood parasites from one genus of haemoparasitic aplicomplexan (Hepatozoon) in two populations of Spanish terrapins (Mauremys leprosa), a semi-aquatic turtle from southwestern Europe with a vulnerable conservation status. We also examined the association between mixed blood parasite infection and indicators of health of terrapins (body condition, haematocrit values and immune response). Blood parasite infection with Hepatozoon spp was detected in 46·4% of 140 examined terrapins. The prevalence of blood parasites infection differed between populations. We found two different lineages of blood parasite, which have not been found in previous studies. Of the turtles with infection, 5·7% harboured mixed infection by the two lineages. There was no difference in body condition between uninfected, single-infected and mixed-infected turtles, but mixed-infected individuals had the lowest values of haematocrit, thus revealing the negative effects of blood parasite mixed infections. Immune response varied among terrapins with different infection status, where mixed infected individuals had higher immune response than uninfected or single-infected terrapins.