A skeletochronological study of age in the Caspian pond turtle, Mauremys caspica caspica (Testudines: Geoemydidae) in Golestan Province, Iran

Document Type : Research Paper


Department of Biology, Faculty of Sciences, Golestan University, Gorgan, Iran


We estimated age of the Caspian pond turtle, Mauremys caspicacaspicain Golestan Province with the skeletochronological method, using specimens collected by nets in natural habitats such as ponds and fish farms. In adult M. c. caspica, lines of arrested growth (LAGs) were clearly discernable in the phalangeal and fibula bone cross-sections. The median age of M. c. caspica in the examined Golestan Province population(n = 22) was calculated 9.6 years (4-12) in males (n = 10), and 10.16 years (4-13) in females (n = 12) for the first time. The maximum straight carapace length (SCL2) was in the range of 83.74–221.41 (mean ± SD = 178.39 ± 48.89) mm in males and 103.02–236.84 (193.52 ± 41.32) mm in female specimens. Significant correlation was found between body size and age (p < 0.001). No difference was found in age composition between the sexes. Our study showed that skeletochronological method can be successfully applied to the Caspian pond turtle based on the clear arrest of growth in the hibernation period.


Aresco, MJ & Guyer, C 1998, Efficacy of using scute annuli to determine growth histories and age of Gopherus polyphemus in southern Alabama. Copeia, 1094-1100.
Auer, M & Taşkavak, E  2004, Population structures of syntopic Emys orbicularis and Mauremys rivulata in western Turkey. Biologia Bratislava, 59: 81-84.
Avens, L & Goshe, LR 2007, Comparative skeletochronological analysis of Kemp’s ridley (Lepidochelys kempii) and loggerhead (Caretta caretta) humeri and scleral ossicles. Marine Biology, 152: 1309-1317.‏
Berry, KH 2002, Using growth ring counts to age juvenile desert tortoises (Gopherus agassizii) in the wild. Chelonian Conservation and Biology, 4: 416-424.
Brophy, TR 2006, Allometry and sexual dimorphism in the snail-eating turtle Malayemys macrocephala from the Chao Phraya River basin of Central Thailand. Chelonian Conservation and Biology, 5: 159-165.‏
Brown, GP,  Bishop,  CA & Brooks,  RJ 1994, Growth rate, reproductive output, and temperature selection of snapping turtles in habitats of different productivities. Journal of Herpetology, 28: 405-410.
Buchanan, CR & Preece,  MA 1991, Hormonal control of bone growth, in Bone, Bone Growth-A, B.K. Hall (ed.), Boca Raton, FL: CRC Press, 53-90.
Carr, A & Goodman, D 1970, Ecological implications of size and growth in Chelonia. Copeia, 783-786.
Castanet, J & Cheylan, M 1979, Les marques de croissance des os et des ecailles comme indicateurde l’age chez Testudo hermanni et Testudo graeca (Reptilia, Chelonia, Testudinidae). Canadian Journal of Zoology, 57: 1649-1665.
Castanet, J, Francillon-Vieillot, H, Meunier, FJ & De Ricqles, A 1993, Bone and individual aging. In: BBK Hall (Ed.) Bone, bone growth B. CRC Press, Boca Raton, FL, 7:  245-283.
Castanet, JH, Meumier, FJ & de Ricqles, A 1977, L’enregistrement dela croissance cyclique parle tissue osseux chez les vertebres poikilothermes: Donnees comparatives et essai de synthese. Bulletin Biologique de la France et de la Belgique, 111: 183-202.
Chaloupka, MY & Musick, JA 1997, Age, growth, and population dynamics. In: P, Lutz & J Musick  (Eds.) The biology of sea turtles, CRC Press, Boca Raton, FL, 233-276.
Çiçek , K, Kumaş, M, Ayaz, D & Tok, CV  2016,  A skeletochronological study of age, growth and  longevity in two freshwater turtles, Emys orbicularis and Mauremys rivulata, from Mediterranean Turkey (Reptilia: Testudines). Zoology in the Middle East, 62: 29-38.
Chinsamy, A & Valenzuela, N 2008, Skeletochronology of the endangered side-neck turtle, Podocnemis expansa. South African Journal of Science, 104: 311-314.
Coles, WC, Musick, JA & Williamson, LA 2001, Skeletochronology validation from an adult loggerhead (Caretta caretta). Copeia, (1): 240-242.
Curtin, AJ, Zug, GR, Medica, PA & Spotila, JR 2008, Assessing age in the desert tortoise Gopherus agassizii: testing skeletochronology with individuals of known age. Endangered Species Research, 5: 21-27.
Germano, DJ & Bury, RB 1998, Age determination in turtles: evidence of annual deposition of scute rings. Chelonian Conservation and Biology, 3: 123-132.
Germano, DJ & Bury, RB 2009, Variation in body size, growth, and population structure of Actinemys marmorata from lentic and lotic habitats in Southern Oregon. Journal of Herpetology, 43: 510-520.
Gibbons, JW, Gereene, JL & Patterson, KK 1982, Variation in reproductive characteristics of aquatic turtles. Copeia, 4: 776-784.
Enlow, DH, Gans, C, Bellairs d’A, Parsons (eds.) TS 1969, The bone of reptiles in biology of the Reptilia. London: Academic Press, 1: 45-80.
Francillon-Vieillot, H, de Buffrenil, V, Castenet, J, Geraudie, J, Meunier, FJ, Sire, JY, Zylberberg, L & de Ricqles, A 1990, Microstructure and mineralization of vertebrate skeletal tissues, In: Skeletal bio-mineralization: patterns, processes and evolutionary trends, JG Carter (Ed.), New York: Van Nostrand Reinhold, 1: 471–530.
Frazer, NB, Andl, M & Ehrhar, T 1985, Preliminary growth models for green, Chelonia mydas, and loggerhead, Caretta caretta turtles in the wild. Copeia 1: 73-79.
Fritz, U, Ayaz, D, Boschbom, J, Kami, HG, Mazanaeva, LF, Aloufi, AA, Auer, M, Rifai, L, Silic, T & Hundsdorfer AK 2007, Go east: Phylogeographies of Mauremys caspica and M.rivulata_discordance of morphology, mitochondrial and nuclear genomic markers and rare hybridization. Journal of Evolutionary Biology, 21: 527-540.
Fritz, U & Wischuf, T 1997, Zur Systematik westasia tischsü dosteuropäischer Bachschildkröten (Gattung Mauremys) (Reptilia: Testudines: Bataguridae). Zoologische Abhandlungen, Staatliches Museum fürTierkunde Dresden, 49: 223-260 (In German).
Germano, DJ & Bury, RB 1998, Age determination in turtles: evidence of annual deposition of scute rings. Chelonian Conservation and Biology,3: 123-132.
GIBBONS, JW 1983, Reproductive characteristics and ecology of the mud turtle, Kinosternon subrubrum (Lacepede). Herpetologica, 39: 254-271.
Gmelin, SG 1774, Reise durch Rußland zur Untersuchung der drey Natur-Reiche. Vol. 3. Dritter Theil. Reise durch das nordliche Persien, in den Jahren 1770, 1771, bis im April 1772. St. Petersburg: Kayserliche Academie der Wissenschaften [In Germany].
Heppell, SS, Snover, ML & Crowder, LB 2003a, Sea turtle population ecology. In: PL, Lutz, JA,  Musick & J, Wyneken  (Eds.) The Biology of Sea Turtles, 2: 275-306.
Heppell, SS, Crowder, LB, Crouse, DT, Epperly, SP& Fraser, NB 2003b, Population models for Atlantic loggerheads: past, present, and future. In: AB, Bolten & BE, Witherington (Eds.) Loggerhead sea turtles. Smithsonian Books, Washington, DC, 255-273.
Iverson, JB, Balgooyen, C, Burd, KK & Lyddan, KK 1993, Latitudinal variation in egg and clutch size in turtles. Canadian Journal of Zoology, 71: 2448-2461.
Kami, HG, Hojati, V, Pashaee Rad, S & Sheidaee, M 2006, A biological study of the European pond turtle, Emys orbicularis persica, and the Caspian pond turtle, Mauremys caspica caspica, in the Golestan and Mazandaran provinces of Iran. Zoology in the Middle East, 37: 21-28.
Klinger, RC & Musick, JA 1992, Annular growth layers in juvenile loggerhead turtles (Caretta caretta), Bulletin of Marine Science,51: 224-230.
Lambert, MRK 1982, Studies on the growth, structure and abundance of the Mediterranean spur-thighed tortoise, Testudo graeca in field populations. Journal of Zoology, 196: 165-189.
Leuteritz, TEJ & Gantz, DT 2013, Sexual dimorphism in radiated tortoises (Astrochelys radiata), turtles on the Brink in Madagascar. Chelonian Research Monographs, 6: 105-112.
Leuteritz, TEJ & Ravolanaivo, R 2005, Reproductive ecology and egg production of the radiated tortoise (Geochelone radiata) in southern Madagascar. African Journal of Zoology, 40: 233–242.
Litzgus, JD & Brooks, RJ 1998, Testing the validity of counts of plastral scute rings in spotted turtles, Clemmys guttata. Copeia, 222-225.
Mattox, NT 1936, Annular rings in the long bones of turtles and their correlation with size, Trans. IL. State Acad. Sci., 28: 255–256.
McCreary, B, Pearl, CA, Adams, JM 2008, A protocol for aging Anurans using skeletochronology. US Geological Survey Open-File Report, 1209.
Narbaitz, R 1991, Effects of vitamins A, C, D, and K on bone growth, mineralization, and resorption. In: Bone, bone metabolism and mineralization, BK, Hall (Ed.), Boca Raton, FL: CRC Press, 4: 141–170.
PAUL, R 2003, Untersuchung zur Raumnutzung und Durchfu¨hrungeiner  Gefährdungsanalyseaneiner Population der Europäischen Sumpfschildkr¨ote (Emys orbicularis, Linnaeus, 1758) in NO Deutschland. PhD Thesis, Universität Hamburg, 106 [In Germany].
Perälä, J 2001, Morphological variation among middle eastern Tstudo graeca Linnaeus, 1758 (Sensu lato), with a focus on taxonomy. Chelonii, 3: 78-108.
Rastegar-Pouyani, N, Kami, HG, Rajabizadeh, M, Shafiei, S & Anderson, SC 2008, Annotated checklist of amphibians and reptiles of Iran. – Iranian Journal of Animal Biosystematics (IJAB), 4: 43-66.
Rodríguez-Caro, R, Graciá, E, Dos Santos, RM, Anadón , JD & Gimenez, A  2015, One scute ring per year in Testudo graeca? A novel method to identify ring deposition patterns in tortoises. Acta Herpetologica, 10: 77-84.‏
Safaei-Mahroo, B, Ghaffari, H, Fahimi, H, Broomand, S, Yazdanian, M, Najafi Majd, E, Hosseinian, SS, Yousefkhani, E, Rezazadeh, MS, Hosseinzadeh, R, Nasrabadi, M, Rajabizadeh, M, Mashayekhi, A, Motesharei, Naderi  A & Kazemi, SM 2015, The herpetofauna of Iran: checklist of taxonomy, distribution and conservation status. Asian Herpetological Research, 6: 257-290.
Schneeweiss, N 1998, Status and protection of the European pond turtle (Emys o. orbicularis) in Brandenburg, Northeast Germany. In:  U, Fritz, U, Joger, R, Podloucky & J, Servan (Eds.) Proceedings of the EMYS Symposium Dresden 96, Mertensiella 10, 219-226.
Schneeweiss, N 2004, Age structure of relict populations of the European pond turtle (Emys orbicularis) at the northwestern boundary of its range. Biologia, Bratislava, 59: 123-129.
Snover, ML 2002, Growth and ontogeny of sea turtles using skeletochronology: Methods, validation, and application to conservation, PhD Dissertation, Duke University, Durham, NC.
Snover, ML, Avens, L & Hohn, AA 2007a, Back-calculating length from skeletal growth marks in loggerhead sea turtles Caretta caretta. Endangered Species Research, 3: 95-104.
Snover, ML & Hohn, AA 2004, Validation and interpretation of annual skeletal marks in loggerhead (Caretta caretta) and Kemp’s ridley (Lepidochelys kempi) sea turtles. Fish Bull, 102: 682-692.
Snover,  ML, Hohn, AA, Goshe,  L R & Balazs, GH  2011, Validation of annual skeletal marks in green sea turtles Chelonia mydas using tetracycline labeling. Aquatic Biology, 12: 197-204.‏
Snover, ML, Hohn, AA, Crowder, LB & Heppell, SS 2007b, Age and growth in Kemp’s Ridley Sea turtles: Evidence from mark-recapture and skeletochronology. In: Biology and conservation of Ridley Sea Turtles, PT, Plotkin (Ed.), Baltimore, MD: Johns Hopkins University Press, 89-105.
Snover, M L, Hohn, AA, Crowder, LB & Macko, SA 2010, Combining stable isotopes and skeletal growth marks to detect habitat shifts in juvenile loggerhead sea turtles Caretta caretta. Endangered Species Research, 13: 25-31.
Snover, ML, Rhodin, AG 2007, Comparative ontogenetic and phylogenetic aspects of chelonian chondro-ossious growth and skeletochronology. The biology of turtles, CRC Press, Boca Raton.‏
Simmons, DJ 1992, Circadian aspects of bone biology, In: Bone, bone growth-A. BK, Hall (Ed.), Boca Raton, FL: CRC Press,6:  91-128.
Suryan, RM, Saba, VS, Wallace, BP, Hatch, SA, Frederiksen, M & Wanless, S 2009, Environmental forcing on life history strategies: Evidence for multi-trophic level responses at ocean basin scales. Progress in Oceanography, 81: 1-4.
Suzuki, HK 1963, Studies on the osseous system of the slider turtle. Annals of the New YorkAcademyof Sciences, 109: 351-410.
Terentev,  PV &  Chernov, SA 1949, Key to amphibians and reptiles, Third edition (Translated from Russian by the Israel program for scientific translation) Translated by L. Kochva, L, 195p.
Thomas, RB, Beckman, DW, Thompson, K, Buhlmann, KA , Gibbons, JW & Moll, DL 1997, Estimation of age for Trachemys scripta and Deirochelys reticularia by counting annual growth layers in claws. Copeia, 4: 842-845.‏
Tracy, CR 1995, Estimating age of desert tortoises (Gopherus agassizii) from scute rings. Copeia, 964-966.
Turner, FB, Medica, PA & Bury, RB 1987, Age-size relationship of desert tortoise (Gopherus agassizi) in southern Nevada. Copeia, 974-979.
Wilson, DS &Tracy, CR 2003, Estimating age of turtles from growth rings: a critical evaluation of the technique. Herpetologica, 59: 178-194.
Wischuf, T & Busack, SD 2001, Mauremys rivulata (Valenciennes in Bory de Saint-Vincent et al., 1833) – Ostmediterrane Bachschildkröte. Handbuch der Reptilien und Amphibien Europas, 3: 89-110.
Yadollahvand, R, Kami , HG, Mashroofeh, A & Bakhtiari, AR 2014, Assessment trace elements concentrations in tissues in Caspian Pond Turtle (Mauremys caspica) from Golestan province, Iran. Ecotoxicology and Environmental Safety, 101: 191-195.
Yazarloo, M & Kami, HG 2017, Sexual dimorphism and morphometric study of Caspian pond turtle, Mauremys caspica, (Testudines: Geoemydidae) in Golestan Province, southeast of the Caspian Sea. Caspian Journal of Environmental Sciences, 15: 321-334.
Zivari, S & Kami, HG 2017, Skeletochronological assessment of age in the Persian mountain salamander, Paradactylodon gorganensis (Clergue-Gazeau and Thorn, 1979) (Caudata: Hynobiidae) from Golestan Province, Iran.‏Caspian Journal of Environmental Sciences, 15: 75-84.
Zug, GR, Wynn, AH & Ruckdeschel, C 1986, Age determination of loggerhead sea turtles, Caretta caretta, by incremental growth marks in the skeleton. Smithsonian Contributions to Zoology, 427: 1-34.
ZUG, GR 1990, Age determination of long lived reptiles: some techniques for sea turtles. Annales des Sciences Naturelles, 11: 219-222.