A Skeletochronological Study of Age in the Persian Pond Turtle (Emys Orbicularis Persica) from the North of Iran

Journal of Wildlife and Biodiversity3(4): 36-44 (2019) (http://jwb.araku.ac.ir/) Research Article DOI: 10.22120/jwb.2019.112091.1079 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 Biology, 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 vertebrates 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 amphibians used to estimatethe age of the Persian pond turtle and reptiles 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 habitats 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 hibernation, 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 Biodiversity 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 ecology, 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.

Load more