Mauremys Leprosa Research Articles

The Mediterranean Pond Turtle shows resilience to extreme flood events

The Mediterranean Pond Turtle shows resilience to extreme flood events

Morphological and genetic evidence of hybridisation between Mauremys mutica (Cantor, 1842) and Mauremys leprosa (Schweigger, 1812) in northeast Spain

Morphological and genetic evidence of hybridisation between Mauremys mutica (Cantor, 1842) and Mauremys leprosa (Schweigger, 1812) in northeast Spain

Species-specific variation in mental gland secretions of turtles revealed by proteomic and lipidomic profiling

Chemical signaling through pheromones is an ancient and widespread mode of communication. Turtles and tortoises (chelonians) secrete pheromones via mental (chin) glands and have superior olfactory capacities rendering them a promising group to study the evolution and function of chemical communication in vertebrates. Here, we use state-of-the art proteomics and lipidomics techniques to identify and explore the possible functions of proteins and lipids secreted by mental glands in turtles. We examined four turtle species all from the family Geoemydidae, to understand among-species as well as sexual variation in the composition of mental gland secretions. Differential expression of a relatively small number (ca. 65) of proteins explained a large portion of the proteome variation across species, highlighting the existence of specific signals evolving even in closely related species. Lipidomic analysis revealed high inter-individual variation, but species differences could be attributed to five different lipid classes. The lipids found in mental glands could have a dietary origin or be related to individual condition, but may nonetheless be used in communication. We also examined sex-specific differences in the proteome of a single species (Mauremys leprosa) and found that males expressed a much larger array of proteins than females. Our findings establish a group of candidate proteins potentially involved in chemical signaling in freshwater geoemydid turtles. Alternatively, differently expressed proteins in mental glands could have an indirect link to chemical communication, being involved in pheromone transport and/or antioxidant protection.

Morphological variations and demographic responses of the Mediterranean pond turtle Mauremys leprosa to heterogeneous aquatic habitats

Human activities affect terrestrial and aquatic habitats leading to changes at both individual and population levels in wild animal species. In this study, we investigated the phenotype and demographics of the Mediterranean pond turtle Mauremys leprosa (Schweigger, 1812) in contrasted environments of Southern France: two peri-urban rivers receiving effluents from wastewater treatment plants (WWTP), and another one without sewage treatment plant. Our findings revealed the presence of pesticides and pharmaceuticals in the three rivers of investigation, the highest diversities and concentrations of pollutants being found in the river subsections impacted by WWTP effluents. Principal component analysis and hierarchical clustering identified three levels of habitat quality, with different pollutant concentrations, thermal conditions, nutrient, and organic matter levels. The highest turtle densities, growth rates, and body sizes were estimated in the most disturbed habitats, suggesting potential adult benefits derived from harsh environmental conditions induced by pollution and eutrophication. Conversely, juveniles were the most abundant in the least polluted habitats, suggesting adverse effects of pollution on juvenile survival or adult reproduction. This study suggests that turtles living in polluted habitats may benefit from enhanced growth and body size, at the expense of reproductive success.

Enteric parasites in free-living Mediterranean pond turtle (Mauremys leprosa leprosa) in contrasted areas (natural vs polluted) from central-western of Morocco.

The objective of this study is to assess the occurrence of intestinal parasites in Mediterranean pond turtle Mauremys leprosa leprosa collected from three contrasting environments in Morocco. Stool samples from 92 turtles were examined for parasite detection and enumeration. The identified intestinal parasites belong to helminths (oxyurids and ascarid) and protozoa (Entamoebidae). A total of 25 turtles (27.17%) were found to be infected by helminths and/or protozoan parasites. No adult form of these parasites was detected. Eggs of oxyurid and ascarid were detected in individuals of populations studied from Oued Ksob (23.07% and 30.76% of n = 13 turtles) and Oued Zat (34.14% and 24.39% of n = 41 turtles), respectively. For protozoa, Entamoeba cysts were present in turtles in Oued Ksob (15.38% of n = 13turtles), Oued Zat (12.19% of n = 41turtles), and Oued Tensift (5.26% of n = 38turtles) localities. Oxyurid eggs showed the highest intensity at Oued Zat reaching 29.30 ± 59.59 eggs per gram (EPG), versus 12 ± 0.38 EPG for ascaris eggs in Oued Ksob. Entamoeba cysts were detected in lower levels with a maximum of 1.66 ± 1.50 cysts per gram (CPG), in Oued Zat. The prevalence of turtles eliminating eggs was statistically significant between localities for different parasite groups. This study reports for the first time a parasitological characterization of gastrointestinal parasites in wild populations of M. leprosa leprosa from contrasting environments, suggesting a relationship between turtles' infestation and the quality of their habitat.

Sexual Cycle of the Mediterranean Pond Turtle, <i>Mauremys leprosa</i> (Testudines: Geoemydidae) in West Central Morocco

We studied the reproductive cycle of male and female Mauremys leprosa in central Morocco. The cycle for males starts in the spring with warming temperatures and the beginning of the dry-season with testicular enlargement and a decrease in epididimydes size accompanied by sperm production. The epididymis contains sperm mainly in winter, spring and summer. Females exhibited follicular enlargement from November reaching a peak in February when a maximum follicle size of 38.5 mm was observed. Ovulation appears to begin in April or May and oviductal eggs were present in our samples from April – July. Suspected mating activity occurred from January – March when environmental temperatures were lowest and the wet-season peaked. Sexual activity was coincident with the onset of maximum storage of sperm in the epididymis. The overall reproductive cycle of this species is similar to that of other Temperate Zone turtles with the exception that mating occurs in the winter, not in the spring and fall. Winter mating may be a response to the wet-season Mediterranean climates. Rain connects isolated pools in ephemeral rivers and streams in Morocco that form during the dry season, thus providing greater opportunities for access to mates.

Body Size and Ectoparasitic Infestations in the Mediterranean Pond Turtle Mauremys leprosa (Testudines, Geoemydidae) in Majen Belahriti Pond (North-Eastern Algeria)

Morphological parameters were measured on a population of the Mediterranean pond turtle Mauremys leprosa (Schweigger, 1812) in Majen Belahriti pond in the region of Guelma (North-east of Algeria). Females exhibited a longer carapace length (CL) at 177 ± 23.85 mm, surpassing that of males (151.45 ± 31.12 mm), and they also displayed a higher body weight (BW) at 756.52 ± 243.91 g, which was notably greater than that of males (453.09 ± 224.42 g). Placobdella nabeulensis Ben Ahmed, Gajda, Utevsky, Kwist & Świątek, 2023 (Hirudinida, Glossiphoniidae) was identified as the only ectoparasite affecting M. leprosa, with an average body length and width of 11 ± 5.83 mm and 5.1 ± 2.89 mm respectively. The intensity, represented by the average number of leeches per turtle, was calculated to be 2.21 ± 1.31 for this specific population and a prevalence rate of 21.17 %. The tail region showed the highest parasite load, indicating its increased susceptibility compared to other body parts.

Intra- and inter-drainage variation in population structure, body condition, shape morphology and sexual dimorphism in Mauremys leprosa saharica from southern Morocco

The Mediterranean pond turtle Mauremys leprosa is widely distributed in Morocco. Significant variations could be observed in this species due to the fact that it occupies a vast and environmentally diverse area. Thus, the analysis of population parameters is crucial in elucidating the differences between populations. Differences between individuals may be linked to environmental factors, including many habitat characteristics. In the present study, variation in population structure, body condition, morphology and sexual dimorphism, were examined for the Sahara Desert blue-eyed turtle M. l. saharica in southern Morocco from seven distinct localities distributed in four different drainages in southern Morocco. A total of 224 turtles were captured, sexed, weighed and then measured for their carapace and tail dimensions before being released. Among the studied populations, four were dominated by adult individuals (Taakilt: 96%, Oued Guir: 87%, Oued Ziz: 75%, Sidi ElMehdaoui: 70%), two comprised 100% of adults (Oued Noun and Tarmigt) and one population consisted of 50% adults (Lower Draa). The sex ratio was significantly different between populations, being balanced in two populations (Tarmigt and Sidi El Mehdaoui), male-biased in three populations (Oued Zizi, Oued Noun, Lower Draa) and female-biased in the two remaining populations (Oued Guir and Taakilt). Body Condition Index (BCI, g/cm3) was significantly different among populations but not between sexes, or for the Sex × Locality interaction. The Sexual Size Dimorphism (SSD), females being larger than males, varies among population with the greatest degree observed in Oued Guir population (SSD = 0.41) and the lowest in Sidi El Mehdaoui population (SSD = -0.14). Length-Weight Relation (LWR) shows that M. l. saharica has isometric growth for both male and female of Oued Guir and Tarmigt, for female of Oued Ziz, Taakilt, Oued Noun and lower Draa and hypo-allometric for male of Oued Ziz, Taakilt, Oued Noun, Lower Draa and for both male and female of Sidi El Mehdaoui. Morphological variation of carapace is shown in this species associated with population variation among basins. Increased understanding of population characteristics and their fitness status must be considered in conservation and management action plans for the species and its habitat.

Molecular Phylogenies of Leeches and Haemoparasites Infecting Freshwater Turtles in Aquatic Ecosystems of Northern Africa Suggest Phylogenetic Congruence between Placobdella costata Sensu Lato and Haemogregarina stepanowi Sensu Lato.

Haemogregarines are blood parasites with a life-cycle involving a vertebrate as the intermediate host and an invertebrate as the definitive host and vector. Extensive phylogenetic investigations based on 18S-rRNA gene sequences have shown that Haemogregarina stepanowi (Apicomplexa: Haemogregarinidae) is able to infest a large diversity of freshwater turtle species, including the European pond turtle Emys orbicularis, the Sicilian pond turtle Emys trinacris, the Caspian turtle Mauremys caspica, the Mediterranean pond turtle Mauremys leprosa, and the Western Caspian turtle Mauremys rivulata, among others. From the same molecular markers, H. stepanowi is further considered to be a complex of cryptic species predisposed to infect the same host species. While Placobdella costata is known to be the unique vector of H. stepanowi, it is only recently that independent lineages within P. costata have been illustrated-suggesting the presence of at least five unique leech species across Western Europe. The aims of our study were therefore to investigate from mitochondrial markers (COI) the genetic diversity within haemogregarines and leeches infecting freshwater turtles of the Maghreb, in order to identify processes of parasite speciation. We showed that H. stepanowi consists of at least five cryptic species in the Maghreb, while two Placobella species were identified in the same area. Although an Eastern-Western speciation pattern was apparent for both leeches and haemogregarines, we cannot make definitive conclusions regarding co-speciation patterns between parasites and vectors. However, we cannot reject the hypothesis of a very strict host-parasite specificity within leeches.

Population structure and dynamics of the Mediterranean Pond Turtle Mauremys leprosa (Schweigger, 1812) in contrasted polluted aquatic environments

Pollution contributes to the degraded state of continental aquatic ecosystems and biodiversity. Some species appear to be tolerant to aquatic pollution, yet little is known about the effects of such pollution on population structure and dynamics. Here, we investigated how wastewater treatment plant (WWTP) effluents of the Cabestany City, in southern France, contribute to the pollution levels of the Fosseille River, and we tested how they could affect population structure and medium-term dynamics of the native freshwater turtle, the Mediterranean Pond Turtle Mauremys leprosa (Schweigger, 1812). Amongst the 68 pesticides surveyed from water samples collected along the river in 2018 and 2021, a total of 16 pesticides were detected, among which eight were found in the upstream section of the river, 15 in the river section located downstream of the WWTP, and 14 in the outfall of the WWTP, exhibiting the contribution of effluents to the river pollution. From 2013 to 2018 and in 2021, capture-mark-recapture protocols were carried out on the freshwater turtle population living in the river. Using robust design and multi-state models, we showed a stable population throughout the study period, with high year-dependent seniority, and a bidirectional transition occurring primarily from the upstream to the downstream river sections of the WWTP. The freshwater turtle population consisted mostly of adults, with a male biased sex ratio detected downstream of the WWTP neither related to sex-dependent survival, recruitment, nor transition, suggesting a male bias in the hatchlings or primary sex ratio. Also, the largest immatures and females were captured downstream of the WWTP, with females having the highest body condition, whereas no such differences were observed in males. This study highlights that population functioning of M. leprosa is driven primarily by effluents induced resources, at least over the medium-term.

Growth rates and age at maturity of Mediterranean loggerhead sea turtles estimated from a single-population foraging ground

In sea turtles, somatic growth rates and Age at Sexual Maturity (ASM) are important parameters for investigating population dynamics. Moreover, ASM informs on the time lag needed to observe the effects of past environmental variables, threats and conservation measures acting at nesting beaches on future numbers of clutches or nesting females, that are the most monitored indices. Assessing ASM of mixed populations that share the same foraging areas is difficult, as in the case of the Mediterranean Sea that is frequented by turtles originating from both the Mediterranean and the Atlantic. Here we investigated growth rates of loggerhead sea turtles (Caretta caretta) foraging in the Adriatic Sea, known to be frequented only by individuals of Mediterranean origin. Capture–mark–recapture records of 79 turtles provided growth rates ranging from – 1.1 to 9.6 cm yr−1 which were analyzed through Generalized Additive Models. When integrated with previous data on growth rates in the first years of life, results indicate a non-monotonic growth curve, likely due to an ontogenetic shift from oceanic to neritic areas. Using an integration equation, we estimated mean ASM to be 29.5 or 25.0 year based on mean nester size in Greece (83.4 cm curved carapace length, CCL) or across the Mediterranean (79.7 cm CCL), respectively. Growth rates and size-at-age are similar to the Atlantic population, but Mediterranean turtles mature earlier at a smaller size. The heterogenous growth rates and ASM reported so far in the Mediterranean are probably due, at least in part, to different foraging areas.

Chelonians from the Middle Palaeolithic Site of Mealhada (Coimbra, Portugal): An Update

The results of a review of the chelonian remains retrieved in the excavations carried out in Mealhada (Coimbra, central Portugal) are presented here. Mealhada is a Portuguese Middle Palaeolithic classical site, discovered at the end of the 19th century, and chronologically ascribed to the interglacial Riss-Würm (ca. 120 ka BP). This study has allowed the identification, justification, and figuration of remains attributed to three Iberian chelonian taxa, Testudinidae indet., Mauremys leprosa, and Emys orbicularis, the last one being recognized for the first time in this site. Thus, an update on the data concerning the chelonian record from Mealhada has been achieved, offering new justified taxonomic evidence regarding Iberian chelonian taxa distribution during the Upper Pleistocene. Furthermore, chelonian consumption amongst pre-Upper Palaeolithic hunter-gatherer groups has been documented worldwide. Frequently a locally captured resource, archaeological turtle remains offer relevant information concerning the role that small prey has played in hominid nutritional choices. The potential presence of anthropic alterations (e.g., cutmarks) in some of the chelonian remains from Mealhada is here analysed and the human consumption hypothesis assessed.

Reproductive Traits Demonstrate How Well the Mediterranean Stripe-Necked Turtle Mauremys leprosa Can Flourish under Highly Degraded-Polluted Conditions.

We measured and compared the reproductive traits of the Mediterranean stripe-necked turtles Mauremys leprosa living in highly degraded-polluted vs. intact natural habitats in Algeria. Data on reproduction were obtained by using X-ray examination of gravid females and examination of nests. The results were opposite to the negative trend confirmed in most freshwater turtles exposed to pollution and suggested the ability of this species to flourish instead in highly degraded-polluted habitats. An optimum development was recorded for several reproductive patterns of the studied freshwater turtle under conditions considered uninhabitable for other vertebrates. Females exhibited record body sizes among conspecifics, which allowed them to carry significantly larger clutches, exceeding by up to 3 eggs the previously largest reported clutch. The mean clutch size (8.79 ± 2.70 eggs) was also higher than findings from previous studies, except for in some other polluted habitats. Furthermore, large females even with large clutches carried large eggs. Egg measurements in the disturbed habitat revealed new records exceeding those previously noted; in egg length (by 3.0 mm), egg width (by 2.8 mm), egg mass (by 1.8 g), and clutch mass (by 18.6 g). In comparison, the usual reproductive performances were observed in the intact natural habitat; female body sizes were significantly smaller and carried fewer eggs of smaller size.

Coexistence of Native and Invasive Freshwater Turtles: The Llobregat Delta (NE Iberian Peninsula) as a Case Study

The global degradation of wetlands is increasing their susceptibility to invasions, which is greatly determined by a niche overlap between native and invasive species. We analyze its role in regulating the coexistence of the native Mediterranean stripe-necked terrapin Mauremys leprosa and the invasive Red-eared Slider Trachemys scripta elegans in a coastal wetland. We analyzed both water chemistry and landscape attributes, using variance-partitioning analysis to isolate the variance explained by each set of variables. Then, the influence of environmental variables on species co-occurrence patterns was assessed by using latent variable models (LVM), which account for correlation between species that may be attributable to biotic interactions or missing environmental covariates. The species showed a very low niche overlap, with clear differences in their response to environmental and landscape filters. The distribution of T. s. elegans was largely explained by landscape variables, preferring uniform landscapes within the daily movement buffer, whereas at larger scales, it was associated with a high diversity of habitats of small and uniform relative sizes. A high percentage of the distribution of M. leprosa was unexplained by the measured variables and may be related to the competitive exclusion processes with T. s. elegans. The species was positively related with large patches with high perimeter values or ecotone area at medium spatial scales, and it was benefited from a marked heterogeneity in the patches’ size at larger scale. According to latent variable models, both species had wide eutrophication and salinity tolerance ranges, but they showed different environmental preferences. T. s. elegans was related to eutrophic freshwater environments, whereas M. leprosa was related to more saline and less eutrophic waters. Our results suggest that M. leprosa modifies its habitat use in order to avoid interaction with the T. s. elegans. Thus, management actions aimed at removing the invasive species from the territory and promoting habitat heterogeneity might be needed to protect M. leprosa and avoid local extinctions.

Blood parasite diversity (Apicomplexa: Haemogregarinidae) within the western populations of the European pond turtle Emys orbicularis.

Molecular tools have revolutionized assessments of blood parasites in freshwater turtles. In the Iberian Peninsula and North Africa, two native species of terrapins occur, Emys orbicularis (Linnaeus) and Mauremys leprosa (Schweigger). Both have been identified as hosts for the blood parasite Haemogregarina stepanowi Danilewsky, 1885, which has also been found in related species. However, recent assessments of M. leprosa have identified several distinct genetic lineages of these parasites in this host, while only three haemogregarine lineages were identified in E. orbicularis in Tunisia. Here, we screened 215 individuals of E. orbicularis from the Iberian Peninsula, Menorca Island and Morocco for haemogregarine parasites using partial 18S rRNA gene sequences to estimate relationships. Three unrelated lineages of parasites were detected, one presumed H. stepanowi and two lineages previously known from M. leprosa. A considerable undescribed diversity of parasites exists within these vertebrate host species, while mixed infection and host-sharing is also widespread. Considering that E. orbicularis is near threatened in this region, it is of great importance to identify the parasites infecting it, and to further assess the potential deleterious impact of these diverse parasites on their hosts.

Former des scientifiques engagés et actifs pour concilier biodiversité et sociétés humaines. De l’état de l’art à la médiation scientifique / Train committed and active scientists to reconcile biodiversity and human societies. From scientific review to mediation

The rapid deterioration of the state of biodiversity on a Mediterranean and planetary scale calls for a global response of ecological transition from our societies. One of the levers identified is to mobilize the higher education community in raising awareness and educating on ecological transition. Scientific mediation is a mean to allow dissemination and appropriation of such scientific issues within society. Moreover, it constitutes a participatory and creative approach, placing the learner at the center of the educational process. To reconcile biodiversity and human societies, and to promote the conservation of emblematic marine and terrestrial vertebrate species, two different scientific mediation actions are presented. In a first case, a board game was designed to better understand the biology and ecology of Mediterranean turtle, shark and cetacean species, to better identify the threats to these populations, and to raise awareness on conservation actions and on scientific studies and monitoring of this threatened fauna. In a second case, a short video was developed to decipher the issues of coexistence of human activities with three predators : the harrier, the fox, and the wolf. In addition to the knowledge of these species, the mediation emphasizes the questions of occupation of territories, zoonosis, and competition for resources to shed light on the conflicts between humans and predators. The development of such a scientific mediation approach constitutes a new challenge for higher education, which finds itself immersed in an unprecedented framework : the ecological emergency that our society is facing.

Habitat occupancy by semi‐aquatic reptiles on an aridity gradient in the western Mediterranean

AbstractThe influence of aquatic and riparian habitats on the composition of the local herpetofauna has not been studied extensively. We used redundancy analysis and multivariate ordination methods to evaluate the occurrence of semi‐aquatic reptiles in south‐eastern France, the Iberian Peninsula, and Morocco where the climate transitions from humid temperate to subtropical desert. All the semi‐aquatic reptile species present in this region were studied, including two native turtles (Emys orbicularis and Mauremys leprosa), three native snakes (Natrix astreptophora, N. helvetica, and N. maura), and one introduced turtle (Trachemys scripta). We hypothesized that these species will vary in their responses to differences in the composition of riparian habitats (vegetative community and relative proportion of trees, shrubs, grasses, water and bare ground surface) along the aridity gradient in the region. We found that the habitat niche marginality and niche breadth varied widely across species and climatic regions, although most of the species display a greater habitat niche breadth in the transitional semi‐arid belt. Mauremys leprosa and N. maura were the more generalist species, occupying a wide range of freshwater habitats, including streams associated with impoverished vegetation communities, characteristic of the arid southern Mediterranean region.

Niche differentiation among genetic lineages in the Mediterranean Pond turtle, Mauremys leprosa, across its geographical range

Abstract Ecological niche modelling provides a useful tool to measure niche properties such as niche breadth, niche overlap and niche conservatism among genetic lineages, with relevant implications for conservation. The Mediterranean pond turtle Mauremys leprosa occurs on both sides of the Strait of Gibraltar over most Iberia and the Maghreb Region of north-western Africa, where it shows a complex genetic structure as the result of Pleistocene climatic oscillations and the particular geographical features of this region. We analyzed the overlap of the climate niche of genetic lineages and sublineages of Mauremys leprosa, based on confirmed records across the known geographical range of the species. We also compared the accuracy of environmental niche models obtained by splitting the two lineages into subunits and lumping across lineages. Results revealed an overall niche overlap between the two main lineages and among most sublineages, indicating no relationship between genetic variation and niche divergence. Likewise, the environmental niche modelling revealed an extensive geographical overlap of climatic suitability between the two lineages. However, some ecological differentiation occurs for some sublineage pairs, in particular involving a sublineage whose occurrence corresponds to a particular morphotype – the Sahara blue-eyed pond turtle – which occupies very isolated habitats along the Draa basin in Morocco. These populations are currently threatened by fragmentation of habitats, drought and water salinization. This study will help assessing more effectively the impacts of ongoing climate change on Mauremys leprosa that along with local human activities are likely to increase in the southernmost limit of its distribution.

THE ANTHROPOGENIC ADAPTATION INDEX OF REPTILES IN URBANIZED AREAS OF THE ASHBERON PENINSULA

The strong urbanization of Absheron peninsula highlights the urgency of studying the level of adaptation of reptiles that characterize these areas. Therefore, we have aimed to study the degree of anthropogenic adaptation of each reptile species inhabiting the peninsula. The anthropogenic adaptation index of separate reptiles in the Absheron Peninsula is different in terms of reproductive strategy. Thus, relatively high adaptive anthropogenic intensity is observed in the Caspian bent-toed geckoes (24.5) which are habitats of single-storey buildings, moderately adapted water snakes (17.2), and poorly adapted Mediterranean turtles (10.4). In the mixed-storey residential area, the anthropogenic adaptation were 21.4, 12.8 and 3.7 respectively in geckoes, water snakes and turtles. The anthropogenic adaptation was 0 due to the absence of water snakes and Mediterranean turtles in the residential area with multi-storey buildings, but the Caspian bent-toed gecko was rarely found (1,3). In the area of industrial facilities, the Caspian bent-toed gecko predominates over the reptile species studied, but the level of anthropogenic adaptation in woodlands and control area was much lower.

Tracking turtles in the past: zooarchaeological evidence for human-turtle interactions in the ancient Eastern Mediterranean

Abstract