Journal of Wildlife and Biodiversity3(4): 36-44 (2019) (http://jwb.araku.ac.ir/) DOI: 10.22120/jwb.2019.112091.1079 Research Article

A skeletochronological study of age in the Persian pond turtle (Emys orbicularis persica) from the north of Iran

Sharifeh Yamoudi, Haji Gholi Kami*, Zeinolabedin Mohammadi Department of , Faculty of Sciences, Introduction Golestan University, Gorgan, Iran Skeletochronology, growth models, and *email: [email protected] counting the growth rings are three main Received: 28 July 2019 / Revised: 4 August 2019 / Accepted: 13 techniques of age estimating in the August 2019 / Published online: 14 August 2019. Ministry of (Carr and Goodman 1970, Frazer and Ehrhart Sciences, Research and Technology, Arak University, Iran. 1985, Zug et al. 1986, Curtin et al. 2008, Rodríguez-Caro et al. 2015). The Abstract skeletochronology is the most common used The skeletochronological technique has been technique to determine the age in used to estimatethe age of the Persian pond turtle and which has been considerably used in in the north of Iran. In this study, the phalange turtles (Tsiora et al. 2002, Matthews and Miaud and femur bones were removed, decalcified in 2007, Nayak et al. 2007, Kutrup et al. 2010, chloric acid, and sections stained with Arakelyan et al. 2013, Makovický et al. 2015, Hematoxylin-Eosin. The age of the specimens Zivari and Kami 2017). One of the important was determined by the number of lines of demographic parameters is age structure in arrested growth (LAGs) in cross sections. turtles which may vary among populations as a Additionally, correlation between age and eight result of interpopulation variation in growth morphometric characters of E. o. persica were rates. Moreover, environmental parameters of analysed using Pearson correlation. The aquatic and seasonal climate skeletochronology results showed the mean age changescan affect the growth and body size of in the specimens (n=23) from the Golestan, freshwater turtles (Gibbons 1967, 1970, Tsiora Mazandaran and Guilan provinces were et al. 2002). In temperate climates, each year of estimated four years (range= from 3 to 6) in growth during the warm season, and the juveniles (n=4), nine years (range from 6 to 12) subsequent slowing of growth in , in males (n=8), and 9.5 years (range from 7 to commonly called Lines of Arrested Growth 15) in females (n=11). Females were (LAGs), and can be counted for age significantly longer (minimum straight carapace determination (McCreary et al. 2008). Because length (SCL1); 146.8±9.08 mm) than males turtles are ectotherms, cooler habitats reduce (SCL1; 123.36±8.11 mm) but there was no rates of food consumption and growth of statistically significant difference in the age individuals compared to warmer environments structures between the sexes. Moreover, the (Avery et al. 1993). Freshwater turtles living in results of correlation test shows that the small lentic habitats could experience warmer correlation coefficients were not significant water temperatures and faster growth rates than between morphometric characters and age (P> turtles that live in lotic sites. Ponds and marshes 0.05). can develop a thermocline when days are calm Keywords: Turtle age, Emys orbicularis, (Xenopoulos and Schindler 2001), and the LAGs, northern Iran, skeletochronology. relatively warm water in the summer can 37 | Journal of Wildlife and 3(4): 36-44 (2019)

increase growth rates of turtles live in these Fig.1). Eight morphometric characters including habitats (Gibbons 1970, Parmenter 1980). minimum straight carapace length (SCL1), The Persian pond turtle, E. o. persica Eichwald maximum straight carapace length (SCL2), 1831 is one of the subspecies of European pond Straight carapace width (SCW), Carapace height turtle, Emys orbicularis (Linnaeus 1758) which (CH), minimum plastron length (PL1), is widely distributed inthe northern parts of Iran maximum Plastron length (PL2), Inter anal seam (Ardabil, Guilan, Mazandaran, Golestan) and length in straight line (IASL) and maximum neighborhood countries like Azerbaijan, straight width of femuro-anal suture (FASW) Armenia, Georgia, Russia (Dagestan) and were measured to the nearest 0.01 mm using a Turkmenistan. It can be found in freshwater digital caliper. Sex was determined by habitats such as ponds, lakes, marshes, swamps, secondary sex characteristics (e.g. plastron streams, rivers (especially their deltas) and concavity, tail type, distance of cloaca to drainage canals (Fritz 2003, 2005, Schneeweiss plastron end, iris coloration). The smallest E. o. 2004, Kami et al. 2006, Peter Mikulíček et al. persica (male) with secondary sex 2015). The , food habits (Luiselli 2016), characteristics represented SCL1 of 103.57 mm and phylogeny of Persian pond turtle (Fritz so that individuals with a lower SCL1 were 2003, Schneeweiss 2004) has been studied in its considered juveniles (Çieçek et al. 2016). Two distribution range whereas the age structure of different bones including phalange and femur of the subspecies has been overlooked. the left hind limb were used for estimation of age There are reports of skeletochronological age using skeletochronology approach. Bones were estimation in some reptiles and amphibians in fixed in 10% formalin; the bones were Iran and adjacent countries (Çieçek et al. 2016, decalcified in 10% (v/v) chloric acid during the Zivari and Kami 2017, Yazarloo et al. 2019). period of decalcification for 48 hours (h). After Çieçeket al. (2016) estimated growth parameters decalcification, bones were washed thoroughly of E. orbicularis and Mauremys rivulata in for 24 h and dehydrated with 70, 80, 90, 95, Turkey. The age of the Caspian pond turtle 100% methanol (each for 1.5 h). Cleaning the (Mauremys caspica caspica) were estimated in surrounding tissues with Xylol (for 1.5 h), Golestan, Iran (Yazarloo et al. 2019). However, processed in paraffin block preparation (for 1.5 there is no data on skeletochronological age h); tissues were embedded in small paraffin estimation of E. o. persica from north of Iran. block. Serial sections (5, 7, 10 micrometer (μm) This research is the first study on and for some specimens15 μm) were cut using a skeletochronology of the Persian pond turtle, rotary microtome, stained with Hematoxylin and E.o. persica Eichwald 1831, in Iran. Eosin, and observed under an Olympus BX51 Our aim was age determination of E. o. persica microscope equipped with digital camera DP12. populations in from the north of Iran. We also The camera mounted and linked to a monitor investigated correlation between age and and computer with image software (Zivari and morphometric characters in the Persian pond Kami 2017). The number of lines of arrested turtle. growth (LAGs) was counted in the periosteal bone. Pearson's correlation coefficient was used Materials and Methods to examine the relationship between age and In this study, 23 dead and fixed E. o. persica morphometric characters, and Shapiro-Wilk specimens (four juveniles, nine males, 10 normality test was applied for testing normality. females) from the north of Iran were studied to Data analysis was performed using R (R estimate the age structure of turtles in Golestan, Development Core Team 2018). Mazandaran and Guilan provinces (Table 1 and 38 | Journal of Wildlife and Biodiversity 3(4): 36-44 (2019)

Figure 1. Map of sampling localities for E. o.persica in the north of Iran and distribution of the E. o. persica (based on Rhodin et al. 2017). Table1. Sampling localities, age determination, and number of individuals used for skeletochronology analyses in E. o. persica specimens from the north of Iran (See Fig. 1 for localitiy numbers).

Locality Localityno Latitude Longitude skeletochronology study Age

Juvenile Male Female

Sijoval 1 36° 51′ 54° 11′ - - 2 9,10

Kordkuy 2 36°48' 54° 02' - - 1 7

Qaemshahr 3 36°27' 52°53' - 2 1 8-11-12

UchTappeh 4 37° 04' 54°40' - - 2 7-9

AghDegish 5 37° 04' 54°33' - 2 2 9-12

Voshmgir 6 37°12' 54°43' 4 - 1 3-3-4-6-15

Khan Bebin 7 37° 00' 55° 00' - 1 - 7

MianKaleh 8 36°48' 53°33' - 1 1 7-10

Nur 9 36°34' 52° 01' - 1 1 8-9

Rasht 10 37°15' 49°37' - 1 - 6

Results sections (Fig. 2). The endosteal resorption was In all examined sections, lines of arrested not found in juveniles (Fig. 2A). From 23 growth (LAGs) were observed in the cross- specimens 87% (n=19) were studied with femur 39 | Journal of Wildlife and Biodiversity 3(4): 36-44 (2019)

(Fig. 2B, C and D) and 13% (n=3) with phalange three to 15 years; females ranged in age from (Fig. 2A). The LAGs were generally in the ring seven to 15 years and had a mean age of 9.5 form and located outside the cancellous bone (Table 1). Males ranged in age from six to12 (Fig. 2C and D). The first LAG was partially or years and had a mean age of nine and juveniles completely resorbed by endosteal resorption in ranged in age from three to six and had a mean some individuals. In some specimens two very age of four years (Table 1). No statistically close hematoxynophilic lines were found and significant difference was observed in the age considered as double LAGs. As a rule, these structures between the sexes. However, the lines were counted as a single true LAG in the females were larger than males (mean SCL1 samples. A total of the 23 Persian pond turtle 123.36±8.11 mm for males, and 146.8±9.08mm age-estimated were 11 females, eight males, and for females, Table 2), but there was no four juveniles. The age distribution ranged from difference in the mean ages (t-test: p= 0.78).

Figure 2. Photographs of histological cross-section of phalange and femur of E. o. perscia. Arrows show the line of arrested growth (LAGs). (A) Phalangeal bone cross-section in juvenile (SCL1= 44.50 mm), four LAGs; (B) Femoral bone cross-section at diaphyseal level, female (SCL1=138.61 mm), nine LAGs; (C) Femoral bone cross-section at diaphyseal level, Male (SCL1=128.25 mm), 12 LAGs; and (D) Femoral bone cross-section at diaphyseal level, female (SCL1=125.34 mm), 15 LAGs. Abbreviation: EB= Endosteal bone; m.c= marrow cavity; PB= Periosteal bone. Table 2. Descriptive statistics of eight morphometric characters (char.) for juvenile, male, and female of E. o. persica from the north of Iran. Values are in millimeters. Abbreviations: char. = Characters; SD= Standard deviation; Max= Maximum; Min= Minimum; SCL1 = minimum straight carapace length; SCL2 = maximum straight carapace length; SCW = Straight carapace width; CH = Carapace height; PL1= minimum Plastron 40 | Journal of Wildlife and Biodiversity 3(4): 36-44 (2019)

length; PL2= maximum plastron length; IASL= Inter anal seam length in straight line; FASW= Maximum straight width of femuro-anal suture.

Juvenile (n=4) Female (n=11) Male (n=8)

char. Mean±SD Max Min Mean±SD Max Min Mean±SD Max Min SCL1 44.17±13.76 57.44 25.14 135.01±9.08 148.31 121.98 123.36±8.11 130.11 104.33 SCL2 45.07±14.31 58.70 25.33 136.24±9.08 150.13 123.35 124.98±8.14 131.52 105.90 SCW 39.38±10.61 49.78 24.62 104.32±6.30 116.17 96.37 94.52±4.59 98.29 84.09 PL1 39.34±11.59 48.82 22.84 124.58±8.60 140.52 114.13 107.39±5.19 113.30 95.97 PL2 40.70±12.62 51.97 23.06 128.33±8.70 144.60 117.28 110.70±6.08 117.87 96.87 CH 19.72±5.21 23.28 12.15 62.51±5.07 72.90 56.94 55.91±11.70 84.08 47.96 IASL 17.66±5.93 23.89 9.78 56.94±5.00 64.78 47.75 50.42±2.23 53.81 46.96 FASW 9.78±2.91 11.93 5.50 35.05±2.44 39.35 31.54 29.10±2.07 31.32 25.41

The morphometric data were not significantly (Table 3). For instance, the SCL and age were different from normal distribution (P>0.05). The not correlated in E. o. persica specimens from results of Pearson correlation test shows that the north of Iran (Spearman’s correlation there is no correlation between age and coefficient, r=0.019, P>0.05; Fig. 3). morphometric characters in adult specimens

Table 3. Summary of Pearson's correlation analyses on morphometric data in E.o.persica. Abbreviations: t= t-test statistic value; df=degrees of freedom; p-value: significance level of the t-test; R= correlation coefficient.

Character Number t df p-value R

SCL1 23 0.07 16 0.94 0.019

SCL2 23 0.02 16 0.99 0.004

SCW 23 0.43 16 0.67 0.110

PL1 23 -0.02 16 0.98 -0.006

PL2 23 -0.20 16 0.84 -0.050

CH 23 -1.29 16 0.21 -0.310

IASL 23 -0.04 16 0.97 -0.010

FASW 23 0.17 16 0.86 0.043

Discussion persica was estimated nine years in males and Skeletochronology has been applied to 9.5 in females by skeletochronology method. determine the age in amphibians and reptiles in Among reptiles, turtles are considered as a long- a wide range of climate regions (Kutrup et al. living animal with longevity of more than 70 to 2010, Arakelyan et al. 2013, Makovický et al. 120 years (Fritz and Günther 1996). There is a 2015). In this study, the mean age of E. o. record of longevity ranging between 41 | Journal of Wildlife and Biodiversity 3(4): 36-44 (2019)

Figure 3. Relationship between age (LAGs) and SCL1 in adult male and female Persian pond turtle from north of Iran. : Females; : Males. eight to 30 years in the northeasternmost revealed a significant correlation between age population of E. orbicularis whereas the age and body size for both sexes (Çieçeket al. 2016, structure of the main part of population is Yazarloo et al. 2019).The age of maturity is also considerably more than 50 year (Schneeweiss various in different parts of the species range. 2004). In Eastern Europe, there is a report of Mitrus and Zemanek (2004) estimated 11 and 12 four to15 years for males and 11-17 years for years for the age of maturity in males and females (Mitrus and Zemanek 2004). The most females respectively in eastern Europe while the geographically close population which was age of sexual maturity was recorded 12 (for skeletochronologically studied belongs to a males) and 17 (for females) years in France Central Anatolian population of E. orbicularis (Girondot and Pieau 1993) so that, we can with a mean age of 5.6 years (ranges from four conclude that the population understudy are to nine) for males and 6.1 years (ranges from relatively young and close to age at maturity. four to nine) in females (Erol 2010). The age structure of E. o. persica population in This is the first study to estimate the age of from north of Iran can be deducted to be sexually Persian pond turtle from Iran. In accordance to active and evoke less priority for conservation. Zivari and Kami (2017) and Altunisik et al. Although, the age of maturity is essentially (2014), this study showed that the age of E. o. depending on geographical variations persica is not significantly correlated with body (Bannikov 1951, Shcherbak 1966, Girondot and size within sexes, however, other studies 42 | Journal of Wildlife and Biodiversity 3(4): 36-44 (2019)

Pieau 1993, Keller et al. 1998, Mitrus and References Zemanek 2004, Erol 2010). Altunisik A., Ergul T., Gul C., Özdemir N.,

Comparing longevity of different reptiles in Tosunoglu M. 2014. A skeletochronological various geographical regions revealed that study of the smooth newt Lissotriton longevity of individuals living in arctic and cold vulgaris (Amphibia: Urodela) from island climates are higher than animals and reptiles and mainland population in Turkey. Italian living in warm and temperate region (Sinsch and Journal of Zoology 81(3):381-388. Dehling 2017). Growth and body size of Arakelyan M., Ruzanna P., Ilgaz C., Kumlutas freshwater turtles vary among different climate Y., Durmus S.H., Tayhan Y., Danielyan F. regimes (Gibbons 1970). Temperature, food 2013. A skeletochronological study of abundance and diets (carnivory or herbivory) are parthenogenetic lizards of genus Darevskia the main factors which presumably affect growth and body size of turtles (Gibbons 1967, from Turkey. Acta Herpetologica 8:99-104. Gibbons 1970, Parmenter 1980, Dunham and Avery H.W., Spotila J.R., Congdon J.D., Gibbons 1990). Growth rings may not be always Fischer R.U., Standora E.A., Avery S.B. produced annually (Zug 1991, Keller et al. 1993. Roles of diet protein and temperature 1998), thus our estimations could be imprecise. in the growth and nutritional energetics of However, we observed annual production of juvenile slider turtles, Trachemys scripta. growth rings in young turtles. Females were Physiological Zoology 66: 902-925 larger than males in size, which may be a result Bannikov A.G. 1951. Materialy k poznaniyu of their possibly higher vulnerability to biologii kavkazskikh cherepakh.[Materials predation although more data are needed to to the knowledge of the biology of the confirm. The difference in body size between Caucasian turtles]. Uchenye Zapiski sexes is also often explained by the fact that Moskovskogo Gorodskogo Pedagogiche- females need more stored energy to allocate skogo Instituta 18:129-167. much more to gonad and embryo development Carr A., Goodman D. 1970. Ecologic (Shine 1979, Halliday and Verrell 1988). By implications of size and growth in Chelonia. contrary, males need relatively low investment of energy for reproduction in that Copeia 4:783-786. spermatogenesis is less costly than Çieçek K., Kumaş M., Ayaz D., Tok C.V. 2016. vitellogenetic growth of oocytes (Jørgensen A skeletochronological study of age, 1992). growth and longevity in two freshwater turtles, Emys orbicularis and Mauremys Conclusion rivulata, from Mediterranean Turkey Based on the observed (LAGs) in the cross- (Reptilia: Testudines). Zoology in the sections, the age of the Persian pond turtle from Middle East 62 (1): 29-38. the north of Iran was estimated from 3- 15. We Curtin A.J., Zug G.R., Medica P.A., Spotila J.R. also found that there is no correlation between 2008. Assessing age in the desert tortoise age and morphometric characters in adult Gopherus agassizii: testing specimens of the Persian pond turtle in the north of Iran. skeletochronology with individuals of known age. Endangered Species Research Acknowledgements 5: 21-27. We thank Farzaneh Ganji, Raziyeh Amerian, Dunham A.E., Gibbons J.W. 1990. Growth of Najmeh Okhli and Afzalsadat Borhani for their the slider turtle. In Gibbons J.W. (Eds.), laboratory assistance. Life History and Ecology of the Slider

43 | Journal of Wildlife and Biodiversity 3(4): 36-44 (2019)

Turtle. Washington D.C: Smithsonian amphibians, Chicago University Press, Institution Press. Chicago, pp. 439-467. Erol Y. 2010. Skeletokronolojik yöntem ile Kami H.G., Hojati V., Pashaee Rad S., Emys orbicularis (Linnaeus 1758)’in yaş Sheidaee M. 2006. A biological study of the tayininin belirlenmesi [Determining age European pond turtle, Emys orbicularis structure of Emys orbicularis (Linnaeus persica, and the Caspian pond turtle, 1758) via skeletochronology method]. Mauremys caspica caspica, in the Golestan Afyon Kocatepe University, Institut of and Mazandaran provinces of Iran. Zoology Natural and Applied Science’s. in the Middle East 37: 21-28. Frazer N.B., Ehrhar L.M. 1985. Preliminary Keller C., Andreu A.C., Ramo C. 1998. Aspects growth models for green, Chelonia mydas, of the population structure of Emys and log- gerhead, Caretta caretta, turtles in orbicularis hispanica from southern Spain. the wild. Copeia 1985 (1):73-79. In: Fritz U., Joger U., Podloucky R., Servan

Fritz U. 2003. Die Europäische Sumpfschildkö- j. (Eds), Proceedings of the Emys te. Laurenti, Bielefeld. Symposium Dresden 96. Mertensiella, 10: Fritz U., Fattizzo T., Guicking D., Tripepi S., 147–158. Pennisi M. G., Lenk P., Joger U., Wink M. Kutrup B., Özdemir N., Bülbül U., Çakır E. 2005. A new cryptic species of pond turtle 2011. A skeletochronological study of age, from southern Italy, the hottest spot in the growth and longevity of Rana macrocnemis range of the genus Emys (Reptilia, populations from four locations at different Testudines, Emydidae). Zoologica Scripta altitudes in Turkey. Amphibia- Reptilia 32: 34: 351-371 13-118. Fritz U., Günther R. 1996. Europäische Luiselli L., Amori G. 2016. Diet. In: Dodd C.K. Sumpfschildkröte – Emys orbicularis (Eed), ecology and conservation: A (Linnaeus1758). pp. 518-534. handbook of techniques. Oxford University Gibbons J.W. 1967. Variation in growth rates in Press, Oxford, pp. 97-109. three populations of the Painted Turtle, Makovický P., Kopecky O., Makovický P., Chrysemys picta. Herpetologica 23: 296- Matlach R. 2015. The using of 303. skeletochronology as a screening method Gibbons J.W. 1970. Reproductive dynamics of for age determination of Alpine newts a turtle (Pseudemys scripta) population in a (Mesotriton alpestris): A Technical Report. reservoir receiving heated effluent from a Acta Universitat is Agriculturae et nuclear reactor. Canadian Journal of Silviculturae Mendelianae Brunensis 63 Zoology 48: 881–885. (2): 439-446. Girondot M., Pieau C. 1993. Effects of sexual Matthews K.R., Miaud C. 2007. A differences of age at maturity and survival skeletochronological study of the age on population sex ratio. Evolutionary structure, growth, and longevity of the Ecology 7: 645-650. mountain Yellow-legged , Rana Halliday T.R., Verrell P.A. 1988. Body size and muscosa, in the Sierra Nevada, California. age in amphibians and reptiles. Journal of Copeia 4: 986-993. Herpetology 22: 253-265. McCreary B., Pearl C.A., Adams M.J. 2008. A Jørgensen C.B. 1992. Growth and reproduction. protocol for aging anurans using In: Feder M.E., Burggren W.W. (Eds), skeletochronology. U.S. Geological Survey Environmental physiology of the Open-File Report 2008-1209, 38 p. 44 | Journal of Wildlife and Biodiversity 3(4): 36-44 (2019)

Mitrus, S., Zemanek M. 2004. Body size and [Amphibians and Reptiles of the Crimeal, survivorship of the European pond turtle Herpetologia Taurica]. Naukovadumka, Emys orbicularis in Central Poland. Kiev pp 240. Biologia Bratislava 59: 103-107. Shine R. 1979. Sexual selection and sexual Nayak S., Mahapatra P.K., Mishra S., Dutta dimorphism in the Amphibia. Copeia 2: SK. 2007. Age determination by 297-306. skeletochronology in the common Indian Sinsch U., Dehling J.M. 2017. Tropical anurans toad Bufo melanostictus Schneider, 1799 mature early and die young: Evidence from (Anura: Bufonidae). Herpetozoa 19 (3/4): eight Afromontane Hyperolius species and 111-119. a meta-analysis. PlOS One 12(2): Parmenter R.P. 1980. Effects of food e0171666. availability and water temperature on the Tsiora A., Kyriakopoulou P. 2002. A feeding ecology of pond sliders (Chrysemys skeletochronological study of age and s. scripta). Copeia 1980: 503–514. growth in relation to adult size in the water Rhodin A.G.J., Iverson J.B., Bour R., Fritz U., frog Rana epeirotica. Zoology 105:55-60. Georges A., Shaffer H.B., van Dijk P.P. Xenopoulos M.A., Schindler D.W. 2001. The 2017. Turtles of the World: Annotated environmental control of near-surface Checklist and Atlas of Taxonomy, thermoclines in boreal lakes. Ecosystems 4: Synonymy, Distribution, and Conservation 699-707. Status (8th Ed.). In: Rhodin A.G.J., Iverson Yazarloo M, Kami H.G, Bagherian Yazdi A. J.B., van Dijk P.P., Saumure R.A., 2019. A skeletochronological study of age Buhlmann K.A., Pritchard P.C.H., in the Caspian pond turtle (Mauremys Mittermeier R.A. (Eds). Conservation caspica caspica) in Golestan province of Biology of Freshwater Turtles and Iran (Testudines: Geoemydidae). Caspian Tortoises: A Compilation Project of the Journal of Environmental Sciences 17 (3). IUCN/SSC Tortoise and Freshwater Turtle Zivari S., Kami H.G. 2017. Specialist Group. Chelonian Research Skeletochronological assessment of age in Monographs 7:1–292. the Persian mountain , Rodríguez-Caro R., Graciá E., Dos Santos Paradactylodon gorganensis (Clergue- R.M., Anadón J.D., Gimenez A. 2015. One Gazeau and Thorn, 1979) (Caudata: scute ring per year in Testudo graeca. A Hynobiidae) from Golestan Province, Iran. novel method to identify ring deposition Caspian Journal of Environmental Sciences patterns in tortoises. Acta Herpetologica 10 15(1): 75-84. (2): 77-84. Zug G.R. 1991. Age determination in turtles. Schneeweiss N. 2004. Age structure of relict SSAR Herpetol, Circular 20:1-28. populations of the European pond turtle Zug GR, Wynn A.H., Ruckdeschel C. 1986. (Emys orbicularis) at the northwestern Age determination of loggerhead sea boundary of its range. Biologia, Bratislava turtles, Caretta caretta, by incremental 59(14): 123-129. growth marks in the skeleton. Smithsonian Shcherbak N.N. 1966. Zemnovodnye ipresmy- Contributions to Zoology 427: 1-3.

kayushchiesya Kryma.Herpetologia Taurica