a preliminary study on the mediterranean spur-thighed tortoise

Introduction

Today, testudonine tortoises have a wide geographic distribution that includes the Palearctic, Oriental and Ethiopian biogeographic realms (Parham et al., 2006a). A large portion of this area is inhabited by the Mediterranean spur-thighed tortoise Testudo graeca Linnaeus 1758. These tortoises occur under very different climatic and environmental conditions, ranging from a Mediterranean climate with mild, frost-free winters to an extreme continental steppe climate with severe winter frost (Fritz et al., 2007).

There are 11 known species of turtle and tortoise including six families and nine genera in Iran. Two species of Testudinidae, Testudo graeca and Testudo horsfieldi Gray 1844 are known from Iran (Rastegar-Pouyani et al., 2008). Anderson (1979) has described two subspecies of T. graeca on the Iranian Plateau: T. g. ibera and T. g. zarudnyi, whereas more recent molecular researches (Fritz et al., 2007; Parham et al., 2012) have introduced three subspecies of T .graeca that exist in Iran: T. g. perses, T. g. buxtoni, and T. g. zarudnyi. Several investigations have already been conducted on molecular phylogeny (Parham et al.,

2006a, Fritz et al., 2007; Parham et al., 2012; Mikulíček et al., 2013; Mashkaryan et al., 2013), population dynamics (Bayley and Highfield, 1996; El Mouden et al., 2001; Slimani et al., 2001), general ecology (Lambert, 1969, 1981, 1983), geographic variations (Highfield, 1990a, b), feeding ecology (El Mouden et al., 2006), morphological comparison (Turkozan and Olgun, 2005) and reproduction behavior (Sadeghi and Torki, 2012). However, T. graeca in Iran has received little scientific attention and its biology, ecology and habitat affinities are poorly known. Since this species is listed on the IUCN Red List as a Vulnerable species, such information is essential for planning conservation measures. The present study aims to present new data on morphological characteristics, habitat features, distribution, feeding, ectoparasite infection, reproduction and conservation status of T. graeca populations in the Ardabil province, NW Iran.

Material and Methods

Study area

The study area was located in the northwestern part of Iran, Ardabil Province (38°15’ E, to 39°40’ E, 47°30’ N to 48°00’ N). The region is surrounded by the Alborz Mountains and the Caspian Sea to the east, Aras River to the north, Arasbaran protected area and Gare-Dagh Mountain to the west and the Talesh Mountains to the south (Fig. 1A). Altitude ranges between 20 m in the Moghan steppe to 4811 m above sea level in the Sabalan Mountain. The prominent vegetation is alpine and semi alpine steppe.

Herpetology Notes, volume 7: 127-133 (2014) (published online on 11 April 2014)

A preliminary study on the Mediterranean spur-thighed tortoise Testudo graeca Linnaeus, 1758 from northwestern Iran

Elham Rezazadeh1, Ramin Mohammadi Alucheh1* and Haji Gholi Kami2

1 Young Researchers and elites Club, Ardabil Branch, Islamic Azad University, P. O. Box 196, Ardabil, Iran

2 Department of Biology, Faculty of Sciences, Golestan University, P.O. Box 49165, Gorgan, Iran

*Corresponding author; e-mail: [email protected]

Abstract. There are two species of Testudinidae, Testudo graeca Linnaeus 1758 and Testudo horsfieldi Gray 1844 in Iran. The ecological and biological status of Testudo graeca population in northwest of Iran is poorly known. Therefore in this study we provide morphological, coloration and distribution data on32 specimens (20 males, 12 females) from northwest of Iran. Additionally, new data on feeding, habitat features and threats of the species were studied. In this area some reproductive aspects including reproduction time, egg size and number were reported for the first time.

Key words. Testudo graeca, Morphological characteristics, Biological status, Ardabil, Iran.

Elham Rezazadeh et al.128

Field studies and analysis

In order to determine the occurrence of T. graeca, we visited different stations in Ardabil Province of northwestern Iran between 2009 and 2011. Distribution localities are shown in Fig. 1B. Habitat characteristics including vegetation and sympatric reptiles were also taken into consideration. Morphometric characteristics of 32 captured specimens (20 male, 12 female) were measured with calipers (to 0.02 mm). Captured animals were considered as juveniles when midline carapace length was less than 100 mm (Slimani et al., 2001); based on that, juveniles were not measured. Sexes were determined and the color pattern of specimens was recorded before releasing them. The tortoises were thoroughly checked for ectoparasites and the number of attached ticks was recorded. Nurtured plants by the species, in direct observation, were collected for identification; other plants in the habitat were also sampled for recognizing the habitat plant coverage. Reproduction behavior, nesting and egg laying were observed too. Eggs were measured (to 0.01 mm) and weighed (to 0.01 gr) before incubation.

The morphometric characteristics that were measured are: Straight Carapace Length (SCL), Straight-line measurement from the outermost projection of the nuchal plate to the posterior end of the supracaudalia; Straight Carapace width (SCW), Greatest width in a straight line directly across turtle.; Carapace Height (CH), the vertical measurement between the highest point of carapace and the lowest point of plastron; Plastron Length (PL), the straight-line measurement from the outermost projection of the gular to the posterior end of the anal scute.

For distinguish similarities and differences between males and females, some statistical analyses on morphometric variables were carried out. Data were examined for conformation to assumption of normality (the Shapiro-Wilk test) and homogeneity (Leven’s test for equality of variance). The status of the sexual dimorphism was tested with an Independent t-test. Non normal data was analyzed by Mann-Withney U test. Regarding all statistical tests, significance level was set at p<0.05. Statistical analyses were carried out using the program SPSS 16.0.

Figure 1. A: Map of the study area. B: Sampling stations in Ardabil province.

A preliminary study on the Mediterranean spur-thighed tortoise Testudo graeca 129

Results

Morphology

The ground color of the carapace is uniformly dark olive with some pale yellow-brown spots, especially on the lateral margins. Head is black with small brown spots, limbs and forelimbs are brown with black scales. Descriptive statistics of morphometric measurements of all specimens of T. graeca and separately by gender are provided in Table 1. SCL ranges between 150.6- 460.4 mm (mean = 222.5 mm) were found for mature male specimens, whereas the mean value of this character in females was 171.2 mm (range: 120.1-300.2 mm). Among our specimens, maximum straight carapace

length of males and femles was 460.4 mm and 300 mm, respectively. Sexual dimorphism was found in SCL (t = 2.234, df = 30, p = 033), SCW (t = 2.497, df = 30, p = 018), CH (t = 2.67, df = 30, p = 012), PLmax (t = 1.99, df = 30, p = 0.049), and PLmin (t = 2.109, df = 30, p = 0.043) measured characters (Table 2). In all metric measurements males have larger body size than females; SCL in males (222.5 mm) has higher mean value than that in females (171.2 mm). Mean value of SCW in males (155.9 mm) was higher than that in females (124.6 mm). Also males (mean = 93 mm) have higher carapace than females (mean = 70.6 mm). In addition, males PLmax and PLmin (mean = 185.4 mm, 179 mm respectively) have higher mean value than those in females (mean = 156.2 mm, 148.7 mm respectively).

Reproduction

In the study area, courtship occurred in mid-April. The largest number of matings took place in shady places between 2 pm and 4 pm. In one case, mating lasted twelve minutes at 16:30 pm (Fig. 2). Approximately one month later, females started to lay eggs. Egg laying in one of the females was observed on 26 May and nine mature eggs were numbered. This process started at 16:20 pm and lasted 25-30 minutes. At first, the animal dug up soil with her claws to a depth of 12-13 cm. Entrance of burrow was narrow and deep seated part was broad. After egg laying the nest was filled up to 2-3 cm higher than the soil surface. While finishing this process, shakes were observed in fore- and hindlimbs of the animal, after minutes it began feeding. Collected data from the eggs of this specimen are provided in Table 3. The length of the largest egg was 39 mm, 33 mm width and 24.78 gr weights.

Feeding, habitat affinities and threats

This species is completely herbivorous and in study area it was observed while feeding on Astragalus sp., and Agrpyron sp. The habitats of this species are stony foothills, hillsides covered with meadow, and foothill vegetation is alpine steppe with plant species such as Stachys sp., Eremostachys sp.,Nepeta sp., Tris sp., Verbascum sp., Alyssum sp., Sencio sp., Agrpyron sp. and some other species of Astragalus. Additionally, T. graeca also occurs in plains and farmlands. In its habitat, T. graeca was sympatric with some reptiles, Ophisops elegans, Laudakia caucasia and Ophisaurus apodus.

Table1. Descriptive statistics of morphometric characters obtained from Testudo graeca

specimens collected from northwestern Iran (Ardabil province). For abbreviations, see

text (N: number of specimens; min: minimum value; max: maximum value; SE:

standard error of the mean; SD: standard deviation)

Table 2. Results of Independent t-test comparing males and females in terms of

morphometric characteristics.

Table 3. Egg measurements for female Testudo graeca from northwestern Iran (Ardabil

Province).

Overall Characters

N Min Max Mean S.E S. D

SCL 32 120.10 460.40 203.26 13.56 76.70

SCW 32 80.30 310.90 144.21 7.74 43.84

CH 32 40.20 180.30 90.60 5.12 29.01

PLmax 32 110.20 360.80 174.59 8.80 49.82

PLmin 32 100.40 360.10 167.65 8.71 49.30

Characters t df Sig.

SCL 2.234 30 .033

SCW 2.497 30 .037

CH 2.67 30 .027

PLmax 1.99 30 .055

PLmin 2.109 30 .043

Characters N Min Max Mean S.E S. D

Egg length(mm) 9 35.00 39.00 36.8889 .48432 1.45297

Egg width(mm) 9 31.00 33.00 31.8889 .20031 .60093

Egg weight(gr) 9 21.19 24.78 22.7389 .38287 1.14860

Table 1. Descriptive statistics of morphometric characters obtained from Testudo graeca specimens collected from northwestern Iran (Ardabil province). For abbreviations, see text (N: number of specimens; min: minimum value; max: maximum value; S.E: standard error of the mean; S. D: standard deviation)

Table 2. Results of Independent t-test comparing males and females in terms of morphometric characteristics.








Province).

Overall Characters


SCL 32 120.10 460.40 203.26 13.56 76.70

SCW 32 80.30 310.90 144.21 7.74 43.84

CH 32 40.20 180.30 90.60 5.12 29.01

PLmax 32 110.20 360.80 174.59 8.80 49.82

PLmin 32 100.40 360.10 167.65 8.71 49.30


SCL 2.234 30 .033

SCW 2.497 30 .037

CH 2.67 30 .027

PLmax 1.99 30 .055

PLmin 2.109 30 .043


Egg length(mm) 9 35.00 39.00 36.8889 .48432 1.45297

Egg width(mm) 9 31.00 33.00 31.8889 .20031 .60093

Egg weight(gr) 9 21.19 24.78 22.7389 .38287 1.14860








Province).

Overall Characters


SCL 32 120.10 460.40 203.26 13.56 76.70

SCW 32 80.30 310.90 144.21 7.74 43.84

CH 32 40.20 180.30 90.60 5.12 29.01

PLmax 32 110.20 360.80 174.59 8.80 49.82

PLmin 32 100.40 360.10 167.65 8.71 49.30


SCL 2.234 30 .033

SCW 2.497 30 .037

CH 2.67 30 .027

PLmax 1.99 30 .055

PLmin 2.109 30 .043


Egg length(mm) 9 35.00 39.00 36.8889 .48432 1.45297

Egg width(mm) 9 31.00 33.00 31.8889 .20031 .60093

Egg weight(gr) 9 21.19 24.78 22.7389 .38287 1.14860

Table 3. Egg measurements for female Testudo graeca from northwestern Iran (Ardabil Province).

Development of modern farming in the study area in one hand and live stock overgrazing on the other hand, have caused to destruct the habitat of species. However, there are some additional threat factors in the study area; one of the main predators of this species is Buteo buteo (common buzzard). As we observed, this bird collected an adult tortoise and dropped it from 25 meters elevation, due to hitting a stone its carapace was broken (Fig. 3A). Also in some study sites skeletons of the species were observed (Fig. 3B). Likewise, ectoparasites pose another threat; multiple taxa of ticks infect the species. Most of these parasites attach to soft parts of animal body where hands and limbs join the body and under marginals as well. In our specimens prevalence of infection in males was 100% and in females was 66% (overall = 88% of specimens). Also, average numbers of ticks in males and females was six and two parasites per specimen,

respectively. Hence, males are more vulnerable than females in this case.

Discussion

Some researchers have asserted that Middle Eastern T. graeca should be split into more than nine species, but Parham et al. (2006b) by genetic evidence have considered that this species in the Middle East is a single species, pending further study. However, according to this molecular study and recent research (Parham et al., 2012), the subspecies occurring in study area is T. g. buxtoni.

In the measured characters there were significant differences between the two sexes. Males have a larger and wider carapace than females. Also, they have a higher carapace and larger plastron than females. The results of straight carapace measurements revealed that


Figure 2. Testudo graeca while mating.

males (mean = 222.5 mm) are significantly larger than females (mean = 171.20mm). Disregarding subspecies, there are clear differences between Iranian and Turkish populations. Turkozan, et al. (2003) studied a population of this species from Mardin, southeastern Turkey. Males in this study were larger than females. Males in the Iranian population (mean = 222.5 mm) are larger than the Turkish ones (mean = 203.75mm), but females of the Turkish population (mean = 208.6 mm) are larger than Iranian ones (mean = 171.2 mm). The maximum SCL recorded from the Mediterranean region is 295 mm, Aegean region is 242 mm and Mardin population is

239 mm respectively (Turkozan, et al., 2005), while the maximum SCL of the Iranian population in this study is 460.4 mm. Anderson (1979) has indicated that most Iranian specimen’s SCL are under 300 mm. According to this, and to author’s knowledge, the represented SCL measurement is a new size record for Iran. It shows that the Iranian population has a larger body size in comparison with a Turkish population. Comparison between two populations, south-east Anatolia and north-west Iran, shows significant morphometric differences (Table 4). This difference may be due to geographical barriers and mountain chains like Ararat and Sabalan


Figure 3. A: Testudo graeca hit by a common buzzard in Ardabil. B: Skeleton of T. graeca in study area.

Table 4. Morphometric comparison for males and females between two population of

Testudo graeca from Northwestern Iran (this study) and Southeastern Anatolia

(Turkozan et al., 2005).

Table 5. Egg Size and weight comparison of Testudo graeca between two populations of Testudo

graeca ibera from Northern Greece and Western Iran (Zagros), with one population of Testudo graeca

buxtoni from Northwestern Iran (Transcaucasia).

Males

Northwest Iran South-east Anatolia

Characters N Min Max Mean S.E S. D N Min Max Mean S.E S. D

SCL 20 150.60 460.40 222.50 18.38 82.21 16 135 239 203.75 5.87 23.49

SCW 20 120.30 310.90 155.94 9.51 42.56 16 64 78 70 1.00 4.00

CH 20 60.20 180.30 93.00 6.13 27.45 16 44 53 49 1.00 3.00

PL 20 140.80 360.80 185.64 11.31 50.62 16 81 95 87 1.00 4.00

Females



SCL 12 120.10 300.20 171.20 16.10 55.78 8 155 238 208.63 8.62 24.38

SCW 12 80.30 180.10 124.65 11.61 40.23 8 70 74 72 1.00 1.00

CH 12 40.20 110.40 70.61 7.79 27.01 8 47 54 51 1.00 2.00

PL 12 110.20 240.20 156.19 12.84 44.48 8 88 94 91 1.00 2.00

Hiley and

Loumbourdis, 1988

Sadeghi and Torki,

2012 Present study

Year assessment 1985-1986 2010 2011

Location Northern Greece Western Iran (Zagros) Northwestern Iran

(Transcaucasia)

Egg length (mm) 35.4± 2.0 44.8± 0.5 36.8± 1.4

Egg width (mm) 29.2± 1.9 33.68± 0.7 31.8± 0.6

Egg weight (gr) 17.5± 2.0 28± 0.8 22.7± 1.1

Table 4. Morphometric comparison for males and females between two population of Testudo graeca from Northwestern Iran (this study) and Southeastern Anatolia (Turkozan et al., 2005).

crests with 5000 m and 4811 m above sea level respectively. These two populations may tend to differ from each other and additional measurement features should be examined closely in subsequent studies to clarify other differences.

Nikolosky (1915) recorded courtship in Transcaucasia in April-May, our observations confirm this study. Sadeghi and Torki (2012) have studied the reproduction phases of Testudo graeca ibera in Zagros Mountains, Iran. They compared their results with Hiley and Loumbourdis study (1988) on northern Greek population of the species. Sadeghi and Torki (2012) showed that eggs of the Iranian population have greater length (mean: 44.8±0.5 mm), width, and especially mass. But interestingly, egg size (length) of northwestern Iran population (this study; mean = 36.8± 1.4 mm) is more similar to the Greek population (mean = 35.4± 2.0 mm) rather than the Zagros ones (Table 5). Sadeghi and Torki (2012) reported four eggs for a female while egg laying whereas we observed nine eggs for one female. Clearly, more studies are needed to explore why it varies.

Although T. graeca is widespread, it is classified as Vulnerable on the IUCN Red List. This group is often threatened by human activity: pet-trade, hunting for food, or habitat destruction (Van Abbema, 1997; Parham et al., 2006a). In Iran, the meat of this tortoise is generally not consumed and it seems that the major threat for the Iranian population in the study site is habitat destruction because of obvious development of farming and excessive live stock pasturage. In addition, bird as a predator and high intensity of the infection can be of the threatening factors. To protect the population of T. graeca, some conservation measures should be taken: protection of nesting area, prevention of overgrazing and disturbing pastures, and education programs for local people.

This study is presenting preliminary information regarding morphological and biological status of T. graeca. Therefore, further investigations are necessary to better clarify other detailed biological and ecological aspects, habitat status and define a strategy for conservation of the species in NW Iran.

Acknowledgements. The authors are indebted to Steven. C. Anderson for reviewing manuscript. We are grateful to Hadi Rabti for helping in field work, Mehdi Asadi, head of the Department of the Environment of Pars Abad for his advice and collaboration. Also thanks to Ms. Madani for her support on the manuscript.

References

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Table 4. Morphometric comparison for males and females between two population of

Testudo graeca from Northwestern Iran (this study) and Southeastern Anatolia

(Turkozan et al., 2005).

Table 5. Egg Size and weight comparison of Testudo graeca between two populations of Testudo

graeca ibera from Northern Greece and Western Iran (Zagros), with one population of Testudo graeca

buxtoni from Northwestern Iran (Transcaucasia).

Males



SCL 20 150.60 460.40 222.50 18.38 82.21 16 135 239 203.75 5.87 23.49

SCW 20 120.30 310.90 155.94 9.51 42.56 16 64 78 70 1.00 4.00

CH 20 60.20 180.30 93.00 6.13 27.45 16 44 53 49 1.00 3.00

PL 20 140.80 360.80 185.64 11.31 50.62 16 81 95 87 1.00 4.00

Females



SCL 12 120.10 300.20 171.20 16.10 55.78 8 155 238 208.63 8.62 24.38

SCW 12 80.30 180.10 124.65 11.61 40.23 8 70 74 72 1.00 1.00

CH 12 40.20 110.40 70.61 7.79 27.01 8 47 54 51 1.00 2.00

PL 12 110.20 240.20 156.19 12.84 44.48 8 88 94 91 1.00 2.00

Hiley and

Loumbourdis, 1988

Sadeghi and Torki,

2012 Present study

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(Transcaucasia)

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Egg width (mm) 29.2± 1.9 33.68± 0.7 31.8± 0.6

Egg weight (gr) 17.5± 2.0 28± 0.8 22.7± 1.1

Table 5. Egg Size and weight comparison of Testudo graeca between two populations of Testudo graeca ibera from Northern Greece and Western Iran (Zagros), with one population of Testudo graeca buxtoni from Northwestern Iran (Transcaucasia).


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Accepted by Philip de Pous; Managing Editor: Gholamreza Naderi


a preliminary study on the mediterranean spur-thighed tortoise

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