Mauremys Leprosa Research Articles

Interspecific differences in chemosensory responses of freshwater turtles: consequences for competition between native and invasive species

The red-eared slider (Trachemys scripta elegans) is an introduced invasive species in many Mediterranean countries that is displacing the populations of native endangered Spanish terrapins (Mauremys leprosa). However, it is relatively unknown how potential competitive interactions could be taking place. In many freshwater turtles, semiochemicals from different glands might facilitate species and sex recognition. We hypothesized that chemosensory detection of competitor species might affect space use and habitat selection by freshwater turtles. We analyzed whether T. scripta and M. leprosa turtles recognized chemical cues from male and female conspecifics and heterospecifics in water. We compared time spent by turtles in clean water pools vs. water pools containing the different chemical stimuli. Introduced T. scripta did not avoid nor prefer water pools with chemical stimuli of native M. leprosa terrapins, which might favor the expansion of the invasive species. In contrast, M. leprosa preferred water with chemical stimuli of conspecifics and avoided water with chemical cues of T. scripta, which suggests that chemical cues could be used by native M. leprosa to avoid water pools occupied by introduced T. scripta. We suggest that this avoidance behavior of native M. leprosa may be one of the causes that contribute to the observed displacement of their populations by invasive T. scripta.

Interspecific Differences in Responses to Predation Risk May Confer Competitive Advantages to Invasive Freshwater Turtle Species

AbstractThe nature of competitive interactions between native and introduced invasive species is unclear. In the Iberian Peninsula, the introduced red‐eared slider (Trachemys scripta elegans) is an invasive species that is competing and displacing the endangered native Spanish terrapin (Mauremys leprosa). We hypothesized that interspecific differences in antipredatory behavior might confer competitive advantages to introduced T. scripta. We examined whether interspecific differences in responses to predation risk affect the time that turtles remained hidden in the shell before using an active escape to water. Both turtle species adjusted hiding times by balancing predation threat, microhabitat conditions and the costs of remaining hidden. However, introduced T. scripta showed longer hiding times before escaping than native M. Leprosa, which, in contrast, switched from waiting hidden in the shell to escape to deep water as soon as possible. These interspecific differences might result from the risk of facing different types of predators in different microhabitats (land vs. water) in their original habitats. However, in anthropogenically altered habitats where predators have been greatly reduced, T. scripta may avoid potential costs of unnecessary repeated escape responses to water (e.g. interruption of basking). These behavioral asymmetries could contribute to the greater competitive ability of introduced T. scripta within anthropogenically disturbed environments.

Satellite tracking of a Green Turtle, Chelonia mydas, from Syria further highlights importance of North Africa for Mediterranean turtles

In 2006, we tracked a single Green Turtle after nesting Latakia, providing the first evidence of foraging grounds and migratory routes from this rookery which is one of the most important nesting areas in the Mediterranean. Tracking lasted 95 days during which time the turtle migrated southward (minimum average speed=0.9 km/h) and then westward (minimum average speed=1.6 km/h), following the coast. The turtle settled in the Bay of As Sallum, western Egypt where it remained in neritic, coastal waters for the final 26 days of transmissions. These results, when combined with findings from Cyprus, Turkey and Greece, further highlight the importance of the North African coast for foraging adult turtles and the need for effective conservation measures to be adopted there.

Changes in fiber arrangement in the retinofugal pathway of the turtle Mauremys leprosa: An evolutionarily conserved mechanism

In spite of the numerous reports on the optic fiber distribution in the optic nerve and tract of vertebrates, there have been few studies of the visual pathway in reptiles. The arrangement of fibers in the optic nerve and tract of the turtle Mauremys leprosa was studied by placing a small granule of carbocyanine dye (DiI or DiA) in one of the four quadrants of the retina. The labeled fibers were traced through transverse sections of the retinofugal pathway with confocal microscopy. Retinal axons displayed a quadrant-specific order along the optic nerve. However, retinal ganglion cell axons were re-organized as they passed through the chiasmatic region of the optic pathway. In the optic tract, the nasal and temporal fibers remained intermingled, but there was segregation of dorsal from ventral fibers. This re-ordering is similar to that described in other vertebrates, suggesting the existence of an evolutionarily conserved mechanism.

Hematologic and Biochemical Reference Intervals of Free-Living Mediterranean Pond Turtles (Mauremys leprosa)

Reference intervals of hematologic and biochemical blood profiles were obtained from 56 male and 58 female Mediterranean pond turtles (Mauremys leprosa) captured from the wild in different periods of their annual cycle. Mean (or median in nonnormal distributions) values of leukocyte differential were 53.8% and 58.5% heterophils, 35.3% and 32.6% eosinophils, 6.3% and 5.8% lymphocytes, 4.3% and 2% monocytes, and 0% and 0% basophils in males and females, respectively. Biochemical values did not differ from other chelonians, but values were generally higher in females than in males.

Evidence for an asymmetrical size exchange of loggerhead sea turtles between the Mediterranean and the Atlantic through the Straits of Gibraltar

The permanent eastward current at the Straits of Gibraltar may trap small Atlantic loggerhead sea turtles ( Caretta caretta) inside the western Mediterranean until their swimming and diving skills improve enough to allow them counter-current swimming abilities through the current. A captivity experiment with twelve loggerhead sea turtles (straight carapace length or SCL range: 25.3–48.0 cm) revealed that the average critical velocity of this species within the considered length range was 0.38 ± 0.16 m s − 1 or 1.01 ± 0.24 bl s − 1 . As a consequence, loggerhead sea turtles are predicted to require a minimum SCL of 36.0 cm to swim counter-current through the Straits of Gibraltar, where the water velocity ranges 0.31–0.37 m s − 1 . Genetic analysis of 105 specimens using one mitochondrial marker and seven microsatellites, as well as the recapture of three tagged individuals, support this conclusion; all Mediterranean individuals found in the Atlantic side of the Straits were not smaller than 36.0 cm SCL and the average length (47.3 cm SCL) was significantly higher than that of the Mediterranean turtles in the Mediterranean side of the Straits (31.6 cm SCL). Furthermore, the average length of the turtles of any origin moving from the Mediterranean to the Atlantic was much larger than 36.0 cm (SCL: 54.5 cm SCL), which may indicate the intervention of a different, yet unidentified mechanism restricting east–westward movement. The Algerian current, running along northern Africa, may at least partially explain the delayed departure of loggerhead sea turtles from the Mediterranean Sea to the Atlantic Ocean, as it would force the eastward drift of loggerheads occupying the southwestern Mediterranean. Exchange through the Straits is asymmetrical, and Atlantic turtles are found to enter the Mediterranean at a length of about 20.5 cm. However, once in the Mediterranean they would be retained there for up to 7.9 years, due to the surface circulation pattern. This increases the time span at which turtles are exposed to a high mortality rate, caused by fishing.

Coexistence of two freshwater turtle species along a Mediterranean stream: The role of spatial and temporal heterogeneity

In the Iberian Peninsula the European pond turtle (Emys orbicularis) and the Mediterranean pond turtle (Mauremys leprosa) share many freshwater habitats, in particular Mediterranean streams. Whether and how these two species divide space within those habitats is poorly known in part due to the very low abundance of E. orbicularis at most syntopic sites. The spatial coexistence of these two species was studied along a 1.3 km reach of a typical Mediterranean stream based on data from trapping sessions and basking counts. The effect of the hydrological regime on differences in space use between species was also assessed. Spatial associations between species and between each species and microhabitat descriptors were estimated using a permutation procedure to account for spatial autocorrelation. Differences in the use of space were also estimated using a resample technique to account for the small sample sizes of E. orbicularis. Results indicate that E. orbicularis shows a preference for temporary, shallow, well vegetated and sandy reaches, while M. leprosa is less selective regarding microhabitat. Differences between E. orbicularis and juveniles of M. leprosa were less obvious. The high spatial heterogeneity of Mediterranean streams may be responsible for the persistence of viable populations of E. orbicularis as well as favouring the coexistence of the two turtle species. Therefore, stream habitat management and conservation plans for E. orbicularis should give priority to the maintenance of high levels of heterogeneity along Mediterranean streams.

Early development of the optic nerve in the turtle Mauremys leprosa

We show the distribution of the neural and non-neural elements in the early development of the optic nerve in the freshwater turtle, Mauremys leprosa, using light and electron microscopy. The first optic axons invaded the ventral periphery of the optic stalk in close relationship to the radial neuroepithelial processes. Growth cones were thus exclusively located in the ventral margin. As development progressed, growth cones were present in ventral and dorsal regions, including the dorsal periphery, where they intermingled with mature axons. However, growth cones predominated in the ventral part and axonal profiles dorsally, reflecting a dorsal to ventral gradient of maturation. The size and morphology of growth cones depended on the developmental stage and the region of the optic nerve. At early stages, most growth cones were of irregular shape, showing abundant lamellipodia. At the following stages, they tended to be larger and more complex in the ventral third than in intermediate and dorsal portions, suggesting a differential behavior of the growth cones along the ventro-dorsal axis. The arrival of optic axons at the optic stalk involved the progressive transformation of neuroepithelial cells into glial cells. Simultaneously with the fiber invasion, an important number of cells died by apoptosis in the dorsal wall of the optic nerve. These findings are discussed in relation to the results described in the developing optic nerve of other vertebrates.

Developmental changes in the fibre population of the optic nerve follow an avian/mammalian-like pattern in the turtle Mauremys leprosa

The changes in the axon and growth cone numbers in the optic nerve of the freshwater turtle Mauremys leprosa were studied by electron microscopy from the embryonic day 14 (E14) to E80, when the animals normally hatch, and from the first postnatal day (P0) to adulthood (5 years on). At E16, the first axons appeared in the optic nerve and were added slowly until E21. From E21, the fibre number increased rapidly, peaking at E34 (570,000 fibres). Thereafter, the axon number decreased sharply, and from E47 declined steadily until reaching the mature number (about 330,000). These observations indicated that during development of the retina there was an overproduction and later elimination of retinal ganglion cells. Growth cones were first observed in the optic nerve at as early as E16. Their number increased rapidly until E21 and continued to be high through E23 and E26. After E26, the number declined steeply and by E40 the optic nerve was devoid of growth cones. These results indicated that differentiation of the retinal ganglion cells occurred during the first half of the embryonic life. To examine the correlation between the loss of the fibres from the optic nerve and loss of the parent retinal ganglion cells, retinal sections were processed with the TUNEL technique. Apoptotic nuclei were detected in the ganglion cell layer throughout the period of loss of the optic fibres. Our results showed that the time course of the numbers of the fibres in the developing turtle optic nerve was similar to those found in birds and mammals.

Salmonella in free living terrestrial and aquatic turtles

Detection of Salmonella in pet turtles has been the focus of extensive research, but its incidence in free living turtles is not well known. The aim of this study was to evaluate the incidence of Salmonella in terrestrial and aquatic species of chelonians inhabiting a National Park in southwestern Spain. Individuals of the terrestrial tortoise Testudo graeca ( n = 16) and the aquatic turtles Emys orbicularis ( n = 26) and Mauremys leprosa ( n = 50) were investigated. Maximum incidence of Salmonella was recorded in the terrestrial species (100%). In contrast, the incidence of infected animals was low in the aquatic species, 12% in M. leprosa and 15.4% in E. orbicularis. Five serotypes of Salmonella belonging to subspecies enterica (I) and salamae (II) were identified. All serotypes were found in the terrestrial species, and three in the aquatic ones, suggesting that wild terrestrial chelonians are important reservoirs of Salmonella in our study area. Cloacal transmission during mating is the most probable mode of transmission among individuals.

Falcaustra donanaensis sp. nov. (Nematoda: Kathlaniidae) a parasite of Mauremys leprosa (Testudines, Bataguridae) in Spain

Falcaustra donanaensis sp. nov. (Nematoda, Kathlaniidae) from the large intestine of Mauremys leprosa (Testudines, Bataguridae) is described. By the absence of pseudosucker, arrangement of the male caudal papillae and the size of the spicules Falcaustra donanaensis sp. nov. resembles only to Falcaustra washingtonensis [Bursey and Aker (2001) J Parasitol 87:1082-1084], a species from Ambistoma tigrinum melanostictum in the Nearctic Region. Papillae pattern in the male of F. washingtonensis is similar to F. donanaensis, but differs by the presence of a median papilla in the American species, length of pharynx, spicule, and gubernacle in males, size of eggs, and number of eggs in female. This is the first species of Falcaustra reported in freshwater turtles in the Iberian Peninsula.

Impact of mountain chains, sea straits and peripheral populations on genetic and taxonomic structure of a freshwater turtle, Mauremys leprosa (Reptilia, Testudines, Geoemydidae)

Mauremys leprosa, distributed in Iberia and North‐west Africa, contains two major clades of mtDNA haplotypes. Clade A occurs in Portugal, Spain and Morocco north of the Atlas Mountains. Clade B occurs south of the Atlas Mountains in Morocco and north of the Atlas Mountains in eastern Algeria and Tunisia. However, we recorded a single individual containing a clade B haplotype in Morocco from north of the Atlas Mountains. This could indicate gene flow between both clades. The phylogenetically most distinct clade A haplotypes are confined to Morocco, suggesting both clades originated in North Africa. Extensive diversity within clade A in south‐western Iberia argues for a glacial refuge located there. Other regions of the Iberian Peninsula, displaying distinctly lower haplotype diversities, were recolonized from within south‐western Iberia. Most populations in Portugal, Spain and northern Morocco contain the most common clade A haplotype, indicating dispersal from the south‐western Iberian refuge, gene flow across the Strait of Gibraltar, and reinvasion of Morocco by terrapins originating in south‐western Iberia. This hypothesis is consistent with demographic analyses, suggesting rapid clade A population increase while clade B is represented by stationary, fragmented populations. We recommend the eight, morphologically weakly diagnosable, subspecies of M. leprosa be reduced to two, reflecting major mtDNA clades: Mauremys l. leprosa (Iberian Peninsula and northern Morocco) and M. l. saharica (southern Morocco, eastern Algeria and Tunisia). Peripheral populations could play an important role in evolution of M. leprosa because we found endemic haplotypes in populations along the northern and southern range borders. Previous investigations in another western Palearctic freshwater turtle (Emys orbicularis) discovered similar differentiation of peripheral populations, and phylogeographies of Emys orbicularis and Mauremys rivulata underline the barrier status of mountain chains, in contrast to sea straits, suggesting common patterns for western Palearctic freshwater turtles.

Sexual Dimorphism and Allometry in the Stripe-Necked Terrapin, Mauremys leprosa, in Spain

ABSTRACT We measured 140 stripe-necked terrapins (Mauremys leprosa) from the center of the Iberian Peninsula, Spain. Female body size exceeded that of males, and female shells were wider and more domed than those of males in relation to carapace length. Plastron length was also greater in females, but preanal tail length was greater in males. Tail length showed similar values in both sexes. Morphological aspects related to sexual selection processes and those related to the fecundity of females are discussed as possible explanations of the sexually dimorphic traits in this species.

Effects of habitat-related visibility on escape decisions of the Spanish Terrapin Mauremys leprosa

Effects of habitat-related visibility on escape decisions of the Spanish Terrapin Mauremys leprosa

Thermostable lichenase as a translational reporter

The polymerase chain reaction with arbitrary primers (RAPD-PCR) was used to study intraspecific variation in Mediterranean turtle Testudo graeca, which is represented by the Dagestan (T. g. pallasi) and Nikolskii (T. g. nikolskii) subspecies in Russia. To study the phylogenetic relationships, the RAPD variation was also compared in two other T. graeca subspecies (T. g. ibera and T. g. terrestris), two closely related Testudo species (T. kleinmanni and T. marginata), and Central Asian turtle Agrionemys horsfieldii. Parameters of RAPD variation showed that the sample from different geographical regions of Dagestan was more polymorphic and heterogeneous than that from Central Asia. The two samples differed in the mean number of RAPD fragments N (48.761 vs. 40.400), number of polymorphic fragments P (78.7 vs. 32.3), and within-group similarity index APS (0.607 vs. 0.784). In T. g. pallasi, no significant difference in N, P, or APS was observed between samples from different localities of Dagestan or between groups of turtles with four- or five-clawed forelegs. A dendrogram of genetic similarity between the species and subspecies under study contained two clusters, one comprising all A. horsfieldii individuals and the other, all turtles of the genus Testudo. In the latter, T. marginata and T. kleinmanni showed higher similarity to each other than to T. graeca. The four T. graeca subspecies clustered separately from each other with a high reliability, T. g. nikolskii and T. g. ibera (Turkey) being more similar to each other than to T. g. terrestris or T. g. pallasi. The possible causes of the presence of four claws on a foreleg and the relationships among members of the genus Testudo were discussed.

When to come out from your own shell: risk-sensitive hiding decisions in terrapins

Animals should optimize the decision of when to come out from a refuge after a predator’s unsuccessful attack because hiding may be costly. Many prey run to hide in refuges in their habitat, whereas others are sessile and take refuge in a protective structure surrounding their body. An intermediate situation is when animals, such as turtles, have morphological structures that provide some partial protection, but they are also able to escape actively to safer refuges. This might complicate hiding decisions predicted by the theory of optimal-refuge use. We studied antipredatory tactics of Spanish terrapins (Mauremys leprosa) in response to simulated predatory attacks with different characteristics (i.e. combinations of several risk factors) and under different conditions (i.e. proximity to safe refuges), which should contribute to overall risk-level estimation. We specifically examined how risk level affected time spent withdrawn into the shell and time until turtles switched to an active escape tactic. The results showed that turtles were able to adjust their hiding behavior by assessing the risk of emerging before the predator had left the area. However, increasing hiding time may also increase the risk that the predator was able to injure or kill the turtle. Thus, the possibility of switching the antipredatory tactic to an alternative active escape to safer refuges (i.e. water) also influenced hiding times.

The freshwater turtle genus Mauremys (Testudines, Geoemydidae) — a textbook example of an east–west disjunction or a taxonomic misconcept?

Barth, D. Bernhard, D. Fritzsch, G. & Fritz, U. (2004): The freshwater turtle genus Mauremys— a textbook example of an east–west disjunction or a taxonomic misconcept? —Zoologica Scripta, 33, 213–221.We compare 1036 bp of the mitochondrial cytochrome b gene (cyt b) from all six Mauremys species with 16 other taxa, representing both currently recognized subfamilies of the Geoemydidae (Geoemydinae and Batagurinae) to contribute a comprehensive dataset towards resolving the conflicting Mauremys taxonomy and phylogeography. Mauremys, a representative of the Geoemydinae, is thought to be an example of a taxon with an east–west disjunction due to Pleistocene glacial extinction, with species occurring in the western Palearctic and species in the eastern Palearctic and Oriental regions. Our results contradict this traditional zoogeographical scheme and the current taxonomy of the Geoemydidae. Mauremys is paraphyletic with respect to two East Asian genera belonging to the Batagurinae: Chinemys and Ocadia. Therefore, Mauremys, as currently understood, clearly represents a taxonomic misconcept. Mauremys+Chinemys+Ocadia contains four well supported clades, two of which —M. japonica+Chinemys+Ocadia and M. annamensis+M. mutica— are confined to eastern Asia. The other two —M. caspica+M. rivulata and M. leprosa— occur in the western Palearctic. Mauremys leprosa may represent an ancient lineage which differentiated before the split between the other western and eastern species occurred. The patchy distribution of the four clades is likely the result of several ancient radiations rather than of a Pleistocene extinction. The sister‐group of Mauremys+Chinemys+Ocadia is Cuora, a morphologically highly specialized genus with a complicated shell hinging mechanism.

Formation of cartilage in the heart of the Spanish terrapin, Mauremys leprosa (Reptilia, Chelonia).

Cartilaginous deposits are regularly present in the heart of several reptilian, avian, and mammalian species. The formation of these extraskeletal cartilages has been studied in birds and mammals, but not in reptiles. The aim here was to elucidate this question in the Spanish terrapin. Hearts from 23 embryos belonging to Yntema (1968) developmental stages 17 to 26 and eight terrapins age 3 months to 10 years were examined using histological, histochemical, and immunohistochemical techniques. In the heart of the Spanish terrapin (Mauremys leprosa), chondrogenesis can start during embryonic life. Cartilaginous tissue develops from a mesenchymal cellular condensation that extends along the aorticopulmonary septum and the incipient pars fibrosa of the ventricular horizontal septum. This cellular condensation, which is smooth muscle alpha-actin (SMalpha-actin)-negative and type II collagen-negative during stages 17 to 22, acts as a prechondrogenic condensation. In stage 23, production of type II collagen begins in the central core of the condensation and gradually spreads toward its periphery. The type II collagen-positive (chondrogenic) cellular condensation remains devoid of perichondrium prior to birth. Thereafter, it converts into hyaline cartilage that extends along the proximal part of the aorticopulmonary septum and the pars fibrosa of the horizontal septum. Our findings are consistent with the assumption that, as in birds and mammals, the precursors of the cardiac chondrocytes in chelonians are neural crest-derived cells of nonmuscular nature. In addition, they point to the possibility that cells from the neural crest populate the embryonic pars fibrosa of the horizontal septum, thereby contributing to its alignment with the aorticopulmonary septum. In the present species, a second cartilaginous deposit of a hyaline nature extends along the sinus wall of the right semilunar valve of the right aorta, penetrating the fibrous cushion that constitutes the proximal support of the corresponding valve leaflet. This cartilage develops after birth, between the third and eighteenth month of life; its morphogenetic origin is unclear. The cartilaginous foci occurring in hearts of Spanish terrapin appear to act as pivots resisting mechanical tensions generated during the cardiac cycle. In the specimens examined there was no sign of replacement of the cardiac cartilages by bone tissue.

Experimental Assessment of Turtle Predation on Larval Anurans

The effect of predation by large non–gape-limited vertebrates on the survivorship and size distribution of larvae of four anuran species was assessed using two syntopic freshwater turtle species, Emys orbicularis and Mauremys leprosa. Predator species and predator sex within species were used as treatments in replicated, factorial experiments for predation trials on tadpoles of Bufo calamita, Hyla meridionalis, Rana perezi, and Pelobates cultripes. Tadpole consumption rates were significantly higher for the carnivorous E. orbicularis than for M. leprosa. Rana perezi tadpoles were the least consumed, whereas P. cultripes and H. meridionalis had the lowest survivorship rates, being relatively easier to catch than R. perezi. Significant size selection occured for larger tadpoles of P. cultripes, whereas predation upon R. perezi tended to concentrate on the smaller size classes. The results point to an overall tendency of turtles to predate upon large tadpoles, yet the outcome of size selection by large vertebrates may depend on phenotypic traits that enhance the escape potential of tadoles. Mauremys leprosa had a high rejection rate of tadpoles, suggesting a higher sensitivity to unpalatability as compared to E. orbicularis, especially with relation to R. perezi. The results indicate that the effect of unpalatability as a predation deterrent may vary even among taxonomically close predator species.

Assessment of reproductive state in the turtle Mauremys leprosa: a comparison between inguinal palpation and radiography

Inguinal palpation and radiography were carried out simultaneously on a sample of 387 adult female Mediterranean turtles, Mauremys leprosa, to assess the presence of calcified oviductal eggs. A significantly higher frequency of pregnant females was obtained through radiography. Egg-bearing females (as shown on radiographs) with positive palpation tended to have significantly larger clutches than did females with negative palpation. Clutches in the earlier calcification stages were less likely to be detected by palpation than were more calcified eggs. The frequency of positive palpations of egg-bearing females varied significantly throughout the nesting season, as a function of variations in both clutch size and average calcification level.