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.

CEITEC Central European Institute of Technology University of Veterinary Sciences Brno Palackého 1946 1 612 42 Brno Czech Republic

Department of Biology and Wildlife Diseases Faculty of Veterinary Hygiene and Ecology University of Veterinary Sciences Brno Palackého 1946 1 612 42 Brno Czech Republic

Ecology of Terrestrial and Aquatic Systems Laboratory Faculty of Sciences University Badji Mokhtar Annaba BP 12 El Hadjar Annaba 23000 Algeria

Environment and Biodiversity Research Division National Environmental Research Center Sidi Amar University Campus 2024 Annaba 23005 Algeria

Functional and Evolutionary Ecology Laboratory Faculty of Natural and Life Sciences University Chadli Bendjedid El Tarf 76 El Tarf 36000 Algeria

National Environmental Research Center Sidi Amar University Campus 2024 Annaba 23005 Algeria

Zobrazit více v PubMed

Lovich J.E., Znari M., Baamrane M.A.A., Naimi M., Mostalih A. Biphasic Geographic Variation in Sexual Size Dimorphism of Turtle (Mauremys leprosa) Populations along an Environmental Gradient in Morocco. Chelonian Conserv. Biol. 2010;9:45–53. doi: 10.2744/CCB-0788.1. DOI

Tiar-Saadi M. Ph.D. Thesis. Département de biologie, Université Badji Mokhtar; Annaba, Algeria: 2018. Bioécologie des Tortues d’eau en Algérie.

Attia El Hili R., Verneau O., Jrijer J., Achouri M. Reassessment of Distribution and Conservation Status of Freshwater Turtles (Testudines) in Tunisia. Salamandra. 2020;56:362–372.

Toledo M.A., de la Concha A., Rubio J.L. Space Use, Distribution and Conservation of the Spanish Pond Turtle (Mauremys leprosa Schewigger, 1812). A Review (Chordata, Geoemydidae) Soc. Esp. Hist. Nat. 2021;115:95–110.

Iverson J.B. A Checklist with Distribution Maps of the Turtles of the World. Erlham College; Richmond, Indiana: 1986. p. 283.

Escoriza D., Hassine J.B. Niche Separation among North-West African Semi-Aquatic Reptiles. Hydrobiologia. 2017;797:47–56. doi: 10.1007/s10750-017-3157-8. DOI

Schleich H.-H., Kästle W., Kabisch K. Amphibians and Reptiles of North Africa. Volume 63 Koeltz Scientific Books; Koenigstein Germany: 1996.

Ernst C.H., Barbour R.W., Altenburg R.G.M. Turtles of the World. Volume 272. Smithonian Institution Press; Washington, DC, USA: 1989. p. 313.

Franch M., Montori A., Sillero N., Llorente G.A. Temporal Analysis of Mauremys leprosa (Testudines, Geoemydidae) Distribution in Northeastern Iberia: Unusual Increase in the Distribution of a Native Species. Hydrobiologia. 2015;757:129–142. doi: 10.1007/s10750-015-2247-8. DOI

Courmont L., De Sousa L. Plan National d’actions en Faveur de l’Emyde lépreuse Mauremys leprosa 2012–2016. Ministère de l’Écologie, du Développement Durable, des Transports et du Logement; Paris, France: 2011. p. 105.

Panzeri M., Mori E., Mazza G., Menchetti M. Records of Introduced Stripe-Necked Terrapins (Mauremys Species) in Italy. Acta Herpetol. 2014;9:227–230.

Pinya S., Parpal L.L., Sunyer J.R. Sobre La Presència de Tortugues d’aigua Al· Lòctones d’introducció Recent a l’illa de Mallorca. On the Presence of Recent Introduced Alien Fresh Water Tortoises in the Mallorca Island. Bolletí Soc. Història Nat. Balears. 2007;50:209–216.

Bakhouche B., Tiar G., Escoriza D., Imed D. Phenology and Population Structure of the Mediterranean Stripe-Necked Terrapin Mauremys leprosa (Schweigger, 1812) in the Reghaia a Lake (Northern Algeria) Basic Appl. Herpetol. 2019;33:43–51. doi: 10.11160/bah.170. DOI

El Hassani M.S., El Mouden E.H., Slimani T., Bonnet X. Morphological and Physiological Assessments Reveal That Freshwater Turtle (Mauremys leprosa) Can Flourish under Extremely Degraded-Polluted Conditions. Chemosphere. 2019;220:432–441. doi: 10.1016/j.chemosphere.2018.12.142. PubMed DOI

Slimani T., El Hassani M.S., El Mouden E.H., Bonnet M., Bustamante P., Brischoux F., Brault-Favrou M., Bonnet X. Large-Scale Geographic Patterns of Mercury Contamination in Morocco Revealed by Freshwater Turtles. Environ. Sci. Pollut. Res. 2018;25:2350–2360. doi: 10.1007/s11356-017-0643-5. PubMed DOI

Combescot C.H. Sexualité et Cycle Génital de La Tortue d’eau Algérienne, Emys leprosa Schw. Bull. Société D’Histoire Nat. L’Afrique Nord. 1954;45:366–377.

Naimi M., Znari M., Lovich J.E., Feddadi Y., Baamrane M.A.A. Clutch and Egg Allometry of the Turtle Mauremys leprosa (Chelonia: Geoemydidae) from a Polluted Peri-Urban River in West-Central Morocco. Herpetol. J. 2012;22:43–49.

Andreu A.C., Villamor C. Calendario Reproductivo y Tamaño de Puesta En El Galápago Leproso, Mauremys leprosa (Schweigger, 1812) En Doñana, Huelva. Doñana. Acta Vertebr. 1989;16:167–172.

Da Silva E. Notes on Clutch Size and Egg Size of Mauremys leprosa from Spain. J. Herpetol. 1995;29:484–485. doi: 10.2307/1565008. DOI

Díaz-Paniagua C., Andreu A.C., Marco A., Nuez M., Hidalgo-Vila J., Perez-Santigosa N. Data on Nesting, Incubation, and Hatchling Emergence in the Two Native Aquatic Turtle Species (Emys orbicularis and Mauremys leprosa) from Doñana National Park. Basic Appl. Herpetol. 2014;28:147–151. doi: 10.11160/bah.13010. DOI

Keller C. Assessment of Reproductive State in the Turtle Mauremys leprosa: A Comparison between Inguinal Palpation and Radiography. Wildl. Res. 1998;25:527–531. doi: 10.1071/WR97013. DOI

Maran J. L’émyde Lépreuse Mauremys leprosa (Schweigger, 1812) Communauté D’Intérêts Pour Tortues En Suisse Bull. 1996;7:16–42.

Pérez M., Collado E., Ramo C. Crecimiento de Mauremys caspica leprosa (Schweigger, 1812)(Reptilia, Testudines) En La Reserva Biologica de Donana. Doñana Acta Vertebr. 1979;6:161–178.

Perez-Quintero J.C. Primeros Datos Sobre Oologia de Reptiles de La Provincia de Huelva; Proceedings of the Comunic. IV Congreso Nacional de Herpetologia; Madrid, Spain. 6–9 December 1989.

Segurado P., Ayres C., Cordero A. L’Emyde Lépreuse Mauremys leprosa Dans La Péninsule Ibérique. Manouria. 2005;8:26–27.

Loulida S., Naimi M., Znari M. Stress Environnemental et Instabilité Du Développement de l’émyde Lépreuse Mauremys leprosa (Schweigger, 1812) Dans Des Environnements Contrastés En Termes de Pollution Dans Le Bassin Du Tensift, Centre Ouest Du Maroc. J. Int. Sci. Tech. L’Eau L’Environnement. 2018;3:104–108.

Martínez-López E., Gómez-Ramírez P., Espín S., Aldeguer M.P., García-Fernández A.J. Influence of a Former Mining Area in the Heavy Metals Concentrations in Blood of Free-Living Mediterranean Pond Turtles (Mauremys leprosa) Bull. Environ. Contam. Toxicol. 2017;99:167–172. doi: 10.1007/s00128-017-2122-6. PubMed DOI

Héritier L., Meistertzheim A.-L., Verneau O. Oxidative Stress Biomarkers in the Mediterranean Pond Turtle (Mauremys leprosa) Reveal Contrasted Aquatic Environments in Southern France. Chemosphere. 2017;183:332–338. doi: 10.1016/j.chemosphere.2017.05.116. PubMed DOI

Gibbons J.W. Reproductive Dynamics of a Turtle (Pseudemys scripta) Population in a Reservoir Receiving Heated Effluent from a Nuclear Reactor. Can. J. Zool. 1970;48:881–885. doi: 10.1139/z70-154. DOI

Bergeron J.M., Crews D., McLachlan J.A. PCBs as Environmental Estrogens: Turtle Sex Determination as a Biomarker of Environmental Contamination. Environ. Health Perspect. 1994;102:780–781. doi: 10.1289/ehp.94102780. PubMed DOI PMC

Lamb T., Bickham J.W., Lyne T.B., Gibbons J.W. The Slider Turtle as an Environmental Sentinel: Multiple Tissue Assays Using Flow Cytometric Analysis. Ecotoxicology. 1995;4:5–13. PubMed

Guillette L.J., Jr., Crain D.A. Endocrine-Disrupting Contaminants and Reproductive Abnormalities in Reptiles. Comments Toxicol. 1996;5:381–398.

Gibbons J.W., Scott D.E., Ryan T.J., Buhlmann K.A., Tuberville T.D., Metts B.S., Greene J.L., Mills T., Leiden Y., Poppy S. The Global Decline of Reptiles, Déjà Vu Amphibians: Reptile Species Are Declining on a Global Scale. Six Significant Threats to Reptile Populations Are Habitat Loss and Degradation, Introduced Invasive Species, Environmental Pollution, Disease, Unsustainable Use, and Global Climate Change. BioScience. 2000;50:653–666. doi: 10.1641/0006-3568(2000)050[0653:TGDORD]2.0.CO;2. DOI

Tiar-Saadi M., Tiar G., Bouslama Z., Širokỳ P. First Data on the Population of the European Pond Turtle Emys orbicularis at Lake Tonga, El Kala National Park, Algeria. Biologia (Bratisl.) 2017;72:819–824. doi: 10.1515/biolog-2017-0089. DOI

Ernst C.H., Hershey M.F., Barbour R.W. A New Coding System for Hardshelled Turtles. Trans. Ky. Acad. Sci. 1974;35:27–28.

Zuffi M.A.L., Odetti F., Meozzi P. Body Size and Clutch Size in the European Pond Turtle (Emys orbicularis) from Central Italy. J. Zool. 1999;247:139–143. doi: 10.1111/j.1469-7998.1999.tb00977.x. DOI

Germano D.J. Ecology of Western Pond Turtles (Actinemys marmorata) at Sewage-Treatment Facilities in the San Joaquin Valley, California. Southwest. Nat. 2010;55:89–97. doi: 10.1894/GC-196.1. DOI

Lindeman P.V. Comparative Life History of Painted Turtles (Chrysemys picta) in Two Habitats in the Inland Pacific Northwest. Copeia. 1996;1:114–130. doi: 10.2307/1446947. DOI

Polo-Cavia N., Engstrom T., López P., Martín J. Body Condition Does Not Predict Immunocompetence of Western Pond Turtles in Altered versus Natural Habitats. Anim. Conserv. 2010;13:256–264. doi: 10.1111/j.1469-1795.2009.00329.x. DOI

Sidis I., Gasith A. Food Habits of the Caspian Terrapin (Mauremys caspica rivulata) in Unpolluted and Polluted Habitats in Israel. J. Herpetol. 1985;19:108–115. doi: 10.2307/1564426. DOI

Souza F.L., Abe A.S. Feeding Ecology, Density and Biomass of the Freshwater Turtle, Phrynops geoffroanus, Inhabiting a Polluted Urban River in South-Eastern Brazil. J. Zool. 2000;252:437–446. doi: 10.1111/j.1469-7998.2000.tb01226.x. DOI

Fritz U., Barata M., Busack S.D., Fritzsch G., Castilho R. Impact of Mountain Chains, Sea Straits and Peripheral Populations on Genetic and Taxonomic Structure of a Freshwater Turtle, Mauremys leprosa (Reptilia, Testudines, Geoemydidae) Zool. Scr. 2006;35:97–108. doi: 10.1111/j.1463-6409.2005.00218.x. DOI

Veríssimo J., Znari M., Stuckas H., Fritz U., Pereira P., Teixeira J., Arculeo M., Marrone F., Sacco F., Naimi M. Pleistocene Diversification in Morocco and Recent Demographic Expansion in the Mediterranean Pond Turtle Mauremys leprosa. Biol. J. Linn. Soc. 2016;119:943–959. doi: 10.1111/bij.12849. DOI

Rhodin A.G.J., Iverson J.B., Bour R., Fritz U., Georges A., Shaffer H.B., van Dijk P.P., Turtle Taxonomy Working Group . In: Turtles of the World: Annotated Checklist and Atlas of Taxonomy, Synonymy, Distribution, and Conservation Status. 9th ed. Rhodin A.G.J., Iverson J.B., van Dijk P.P., Stanford C.B., Goode E.V., Buhlmann K.A., Mittermeier R.A., editors. Vol. 8. Species Survival Commission; Gland, Switzerland: 2021. [(accessed on 19 October 2022)]. pp. 1–472. Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group. Chelonian Research Monographs. Available online: https://iucn-tftsg.org/checklist/

Bonnet X., Delmas V., El-Mouden H., Slimani T., Sterijovski B., Kuchling G. Is Sexual Body Shape Dimorphism Consistent in Aquatic and Terrestrial Chelonians? Zoology. 2010;113:213–220. doi: 10.1016/j.zool.2010.03.001. PubMed DOI

Tiar-Saadi M., Tiar G., Bouslama Z., Širokỳ P. Mechanisms Determining Body Size and Shape Difference in Algerian Spur-Thighed Tortoises (Testudo graeca) Animals. 2022;12:1330. doi: 10.3390/ani12101330. PubMed DOI PMC

Willemsen R.E., Hailey A. Variation of Adult Body Size of the Tortoise Testudo Hermanni in Greece: Proximate and Ultimate Causes. J. Zool. 1999;248:379–396. doi: 10.1111/j.1469-7998.1999.tb01037.x. DOI

Forsman A. Variation in Sexual Size Dimorphism and Maximum Body Size among Adder Populations: Effects of Prey Size. J. Anim. Ecol. 1991;60:253–267. doi: 10.2307/5458. DOI

Jorgewich-Cohen G., Henrique R.S., Dias P.H., Sánchez-Villagra M.R. The Evolution of Reproductive Strategies in Turtles. PeerJ. 2022;10:e13014. doi: 10.7717/peerj.13014. PubMed DOI PMC

Bayly I.A.E. Variation in Sexual Dimorphism in Nonmarine Calanoid Copepods and Its Ecological Significance. Limnol. Oceanogr. 1978;23:1224–1228. doi: 10.4319/lo.1978.23.6.1224. DOI

Gasith A., Sidis I. Polluted Water Bodies, the Main Habitat of the Caspian Terrapin (Mauremys caspica rivulata) in Israel. Copeia. 1984;1984:216–219. doi: 10.2307/1445059. DOI

Díaz-Paniagua C., Pérez-Santigosa N., Hidalgo-Vila J., Florencio M. Does the Exotic Invader Turtle, Trachemys scripta elegans, Compete for Food with Coexisting Native Turtles? Amphib.-Reptil. 2011;32:167–175. doi: 10.1163/017353710X552795. DOI

Bishop C.A., Ng P., Pettit K.E., Kennedy S.W., Stegeman J.J., Norstrom R.J., Brooks R.J. Environmental Contamination and Developmental Abnormalities in Eggs and Hatchlings of the Common Snapping Turtle (Chelydra serpentina serpentina) from the Great Lakes—St Lawrence River Basin (1989–1991) Environ. Pollut. 1998;101:143–156. doi: 10.1016/S0269-7491(98)00005-0. PubMed DOI

Bishop C.A., Brown G.P., Brooks R.J., Lean D.R.S., Carey J.H. Organochlorine Contaminant Concentrations in Eggs and Their Relationship to Body Size, and Clutch Characteristics of the Female Common Snapping Turtle (Chelydra serpentina serpentina) in Lake Ontario, Canada. Arch. Environ. Contam. Toxicol. 1994;27:82–87. doi: 10.1007/BF00203891. DOI

Bonin J., DesGranges J.-L., Bishop C.A., Rodrigue J., Gendron A., Elliott J.E. Comparative Study of Contaminants in the Mudpuppy (Amphibia) and the Common Snapping Turtle (Reptilia), St. Lawrence River, Canada. Arch. Environ. Contam. Toxicol. 1995;28:184–194. doi: 10.1007/BF00217615. DOI

Holliday D.K., Roosenburg W.M., Elskus A.A. Spatial Variation in Polycyclic Aromatic Hydrocarbon Concentrations in Eggs of Diamondback Terrapins, Malaclemys terrapin, from the Patuxent River, Maryland. Bull. Environ. Contam. Toxicol. 2008;80:119–122. doi: 10.1007/s00128-007-9328-y. PubMed DOI

Berry J.F., Shine R. Sexual Size Dimorphism and Sexual Selection in Turtles (Order Testudines) Oecologia. 1980;44:185–191. doi: 10.1007/BF00572678. PubMed DOI

Wilbur H.M., Morin P.J. Life History Evolution in Turtles. Biol. Reptil. 1988;16:387–439.

Gibbons J.W., Greene J.L., Patterson K.K. Variation in Reproductive Characteristics of Aquatic Turtles. Copeia. 1982;1982:776–784. doi: 10.2307/1444086. DOI

Janzen F.J., Warner D.A. Parent-Offspring Conflict and Selection on Egg Size in Turtles. J. Evol. Biol. 2009;22:2222–2230. doi: 10.1111/j.1420-9101.2009.01838.x. PubMed DOI

Packard G.C., Packard M.J. The Physiological Ecology of Reptilian Eggs and Embryos. In: Gans C., Huey R.B., editors. Biology of the Reptilia. Volume 16. Alan R. Liss.; New York, NY, USA: 1988. pp. 523–605.