Activity budget of free-ranging male and female
Abstract
The Souss Valley tortoise, Testudo graeca soussensis, is endemic to the semi-arid and arid low quality habitats of west central Morocco. Populations of this area are among the best-investigated populations in western Mediterranean. The long-term conservation of these declining populations is of particular management concern for this endemic and threatened subspecies. Here we present a data review on biological and ecological aspects of this subspecies dealing with morphology, distribution range and climatic niche, habitat use, food habits, activity cycle, and thermal responses to arid hot conditions, post-hatching growth, sexual maturity, sexual dimorphism, breeding ecology and demographics. After an analysis of the major threats on populations, we proposed management actions required to improve the conservation outcomes for this endangered tortoise in arid areas of west central Morocco. Conservation and restoration potentials of the declining populations and their habitat are also described, including habitat restoration and a captive breeding program.
Keywords
- Testudo graeca soussensis
- arid environments
- west-central Morocco
- taxonomic status
- biology
- ecology
- life history
- threatened subspecies
- conservation
1. Introduction
The Spur-thighed Mediterranean (or Greek/Moorish) tortoise,
2. Description of the subspecies
The subspecies was originally described, based on morphology, as
In their detailed morphometric study, Carretero et al. [6] questioned the validity of the taxon
2.1. Morphological variation and sexual dimorphism
Using 41 carapace dimensions, Carretero et al. [6] found a significant morphological differentiation among tortoises from Admine Forest, Essaouira and Jbilet Mts, west-central Morocco (Figure 1). The population from Jbilet was the most differentiated (no overlap), those from Essaouira on the coast and from Admine showed limited overlap (5%). Tortoises from Jbilet living under harsher conditions (low precipitation, high thermal amplitude, low plant cover) were smaller, lighter, more flattened and less dimorphic in shape than the others. This morphological variation contrasted with the non-significant genetic difference based on 12S rRNA mtDNA among these three populations [12]. The observed morphological differences either have arisen very recently or can be attributed to phenotypic plasticity.
Indeed,
As
3. Taxonomy
As for the other populations of Northwest Africa, all Moroccan populations were put together with
4. Current distribution and quaternary range dynamics
The distribution range of
Following a purportedly tortoise-free zone (from the Atlantic coast around Safi via the Chemaia Plateau east to where the Middle and High Atlas merge [20], the northern parts of the High Atlas are where the distribution range of
Using ecological niche modeling, Anadón et al. [21] showed a clear niche differentiation among the five subspecies of
5. Ecology and behavior
5.1. Habitat
Comparatively to the other North African subspecies,
In the arid-steppe lands of the Haouz plain and central Jbilet Mountains, tortoises were found to depend on the occurrence of large (taller than 1.25 m) and relatively abundant Jujube bushes (
5.1.1. Habitat use
The Souss tortoises do not appear most of the time in places where the vegetation overtops the height of cereal fields almost exclusively in or near Jujube bushes (
5.1.2. Tortoise scrapes and burrows
In the Souss Valley, tortoises use scrapes and burrows to avoid the mid-day heat, for shelter at night and for prolonged aestivation periods. These scrapes and burrows vary considerably in opening size and depth. If some relatively small ones can be produced by tortoises, others clearly surpass their digging abilities and shows signs of previous occupation by mammals such as honey badger (
During the hottest and driest periods (late May to early September) in the central Jbilet mountains [9], radio-tracked tortoises were all found sheltered for a long period under large bushes. Most of them (~90%) were immobile and partly buried. During cooler periods, notably spring and autumn, the tortoises were more frequently under the bushes, but moving regularly
5.2. Activity cycle and time-activity budget
5.2.1. Annual activity
According to Bayley and Highfield [5], brumation (i.e., a hibernation-like state that cold-blooded animals utilize during very cold weather) does not occur in the Admine Forest, Souss Valley, where average monthly mean temperatures in the coolest part of the year (December and January) do not fall below 14.8 and 13.6°C respectively. Average daily temperatures in winter are typically 23.8°C in November, 20.8°C in December and 31.1°C in January. Air temperatures at sites where active tortoises were observed in mid-December 1994 ranged from 24 to 27°C between 10.00 and 14.00 h. The temperature recorded in scrapes and shallow burrows occupied by tortoises was typically 24–26°C and the relative humidity there ranged from 48 to 60% compared to 20% or less in exposed areas.
Aestivation typically begins in June and ends in September. The precise timing is affected by prevailing temperature and, especially, by precipitation. In drought years aestivation may be considerably extended. Tortoises are invariably aestivating during July and August where average mean monthly temperatures are 22.2 and 22.5°C, respectively. Peak daily temperatures during these months can exceed 48°C [5, 8, 9].
Utilizing automatic acceleration recorders, Lagarde et al. [8] characterized and monitored long time behavioral sequences of free-ranging tortoises in central Jbilet Mountains. They recorded and compared the activity budget of males and females under natural conditions during the spring (Figure 5). Tortoises monitored during 24 consecutive hours, remained inactive at night. The average daily activity time was 7650 min. Under unfavorable climatic conditions (strong wind combined with an ambient temperature <15°C), some individuals were mostly inactive with a total activity of less than 5 min/day and few others remained motionless. The duration of the total activity time in active animals was on average less than 2 h/day. The mean daily active time (including the inactive animals) was significantly longer in females compared to males (9455 min versus 6039 min, respectively) [8, 9].
The tortoises devoted most of their activity time to walking and foraging behaviors (40 and 36% of the total activity time, respectively). Sexual and fighting behaviors were very infrequent representing less than 2% of the total activity time, in both sexes. Burrowing and walking behaviors lasted respectively less than 25 and 40 min per day without difference between sexes. Females spent more time foraging than males, but these were more frequently immobile (Table 1) [9].
5.3. Thermal ecology
Like most animals, the Souss Valley tortoise must navigate between microhabitats to find essential feeding resources and thermal refuges. Combining radio-tracking of free-ranging individuals, microhabitat temperature monitoring and transects in a range of habitats, in central Jbilet Mts, Lagarde et al. [8] found tortoises to depend on the occurrence of large and relatively abundant Jujube bushes (
As suggested by the null models, both the air temperature and the body temperature (Tb) of tortoises do not reach 40°C during cool/cloudy days. During sunny days, the tortoises are exposed to potential overheating (Tb > 40°C) and solar radiation for a minimum of 1 h. Large bushes provide thermally buffered conditions while other habitats are potentially risky. Females are less subject to overheating, owing to their much larger size (mean adult body mass: 1.0 versus 0.46 kg) [8, 9].
In central Jbilet Mts, during hot periods, the tortoises could safely travel around 900 m in the open in an average time of nearly 3 h. However, these values vary according to the time of emergence. The estimated safe distance rapidly decreased from 8:00 to 13:00, and then tended to stabilize after 15:30; reflecting the reducing intensity of solar radiation in the afternoon and concomitant decreasing overheating risk. However, individuals must shelter before night; tortoises leaving the bushes after 17:00 could not travel far as the activity stops around 19:00–19:30. In the afternoon the body temperature of the sheltered tortoises was already elevated, thereby improving locomotors performance compared to individuals leaving their refuge in the morning and that must bask in the sun prior movements (night temperatures were often low), but this also accelerated overheating risk [8, 9].
The estimated maximal Tb (recorded between 16:00 and 19:36) of the free-ranging tortoises, walking in the open was 34.7°C for males and 33.6°C for females. Males exhibited higher maximum Tb than females (33.1 ± 0.8°C versus 31.3 ± 0.7°C). The large body size of the females provided a buffering advantage and they were able to travel farther than males. For example, during the hottest periods (at 11:00), the estimated theoretical maximum distance, a tortoise can move is 494 m for males and 673 m for females [8, 9].
5.4. Food habits
The dietary constituents of the species in Admine forest (Souss Valley), included, in addition to various wild plant species, several cultivated species [5]. In this area, displacement of tortoises from the Argan forest because of overgrazing, loss of ground cover and drought has led to their concentration along the margins of cultivated fields. In these situations a high proportion of their diet now consists of
The spring specific richness of plants in the Jbilet habitat was reduced during drier years (2011 and 2012) compared to that reported in a previous above-normal rainfall year [22] (44 and 27 versus 88 plant species). The dry plant biomass density differed greatly between under and out of the Jujube. The mean plant species richness and the total dry biomass density were higher in under than in out Jujube. Tortoises tended to consume only about 5–6 and almost the same species, out of all the available annual forbs and grasses. The total number of plant species that were counted as being within the top 5 for all tortoises included more than 8–10 species. Many other species, abundant in the habitat, were rather avoided. It was suggested that the few herbaceous plants that represented ~90% of tortoise diet, might be important in sustaining tortoise populations during droughts. These results underline the tortoises’ vulnerability to global change on the availability of their preferred food plants [22].
The diet composition showed significant differences among seasons, either qualitatively or quantitatively [22]. The spring diet was more diverse with 16 plant species consumed against only 5 and 7 species in summer and autumn-winter respectively, with 5 shared species (
5.5. Growth and sexual maturity
Both male and female tortoises from the central Jbilet Mountains, the Admine Forest, and near Essaouira, grew relatively quickly for 10–12 year in all three populations, after which their growth rates decreased markedly. Females in all three populations had greater asymptotic sizes than males, and CL and log mass differed significantly between sexes by age 9 year for the three populations, except for log mass of tortoises from Essaouira, which differed by age 6. Mean CLs and log masses were significantly greater in Admine and Essaouira tortoises than in tortoises from Jbilet [13].
The growth period T, equivalent to the age at which 90% of the asymptotic CL is reached, was delayed by approximately 3 year in females relative to males in tortoises from Jbilet (males 14.9 year; females 11.8 year) and Admine (males 12.0 year; females 9.0 year), but not in Essaouira (males 11.4 year; females 11.8 year). Growth was relatively fast for the first 7–10 year of life for tortoises in all three populations whether based on CL or log mass. Growth decreased rapidly after about 10–12 year. Based on calculated CL and calculated mass, tortoises from Admine became larger than tortoises from Jbilet between 3 and 6 year and tortoises from Essaouira exceeded the size of tortoises from Jbilet between 1 and 3 year. A significant sexual size dimorphism occurred by 9 year of age for the three populations based on calculated CL. Based on calculated mass, male and female tortoises from Essaouira diverged in size by 6 year of age, whereas there was no divergence between sexes in mass until 9 year of age for tortoises from Jbilet and Admine. Growth patterns differ significantly between sexes at an age below 8 years, but not between 1 and 5 years of age. From an age of 5 years, a decrease in growth rates of males is observed, whereas those in females increased until 6–7 years of age and then strongly decrease afterward. There was no significant difference in growth patterns between sexes after the age of 8 years [13].
The age at sexual maturity, estimated using large carapace growth annuli, varies from 6 to 9 years for males and from 8 to 11 years for females (7 versus 9 years in average) [13, 22]. The males reached their sexual maturity at a lower mean minimal size (90.7 ± 10 mm, range: 91.4–131.4 mm) than females (146.2 ± 16.5, range: 71.8–114.6 mm). More than 60% of males attained the sexual maturity between 6 and 7 years with a carapace length of 100–120 mm, while around 60% of females are mature between 9 and 10 years with a carapace length ranging from 140 to 170 mm. The estimated minimal size at maturity, based on the sexual behaviors observed in the wild (courtship, mating) is 104.8 and 152 mm, respectively for males and females [13].
Sexual size dimorphism index (SDI) calculated by dividing the size (mean CL) of the females by the size males and subtracting one [23], is almost constant in the three populations and averaged 0.17. Mass of all tortoises (all age classes and sexes combined) from the three populations is highly correlated to CL.
5.6. Reproductive ecology
Only limited data are available on breeding cycle and clutch characteristics in
Mating activity in the Souss Valley tortoises from Admine Forest occurs bimodally in the early spring and in September, immediately following emergence from aestivation. In semi-captive Souss Valley tortoises from central Jbilet Mts, courtship and mating activities in occurred in early spring, from March to early May, and again in mid-Autumn, for a shorter period from late October to early November [10].
Serreau et al. [25] reported low plasma testosterone levels that were associated with mating periods in spring and to a lesser extent in autumn whereas two peaks, one in winter and one in summer, corresponded to periods of inactivity. Strong contrasts in plasma hormone levels induced by experimental treatments did not result in changes in activity budget or space use, both in the short-term or more than one month after the beginning of the hormonal treatment. It was concluded that testosterone levels did not affect directly behavioral activity in
The egg-laying season occurs in May and June in the Souss Valley [5] and from late May to early July in central Jbilet Mts [10]. Nesting sites in the Souss Valley are usually located in sandy banks on the periphery of cultivated fields and at the base of
Mean clutch size in
Average incubation duration at 31°C in
Emergence occurs in September. Mean hatchling body mass and carapace length in central Jbilet were 12.8 g and 35.7 mm, respectively (Figure 7). In semi-captive
5.7. Population structure and dynamics
In the early 1990s, the Admine population showed a highly unbalanced sex-ratio of 2.25 (69.2% of males) and only 27.6% of immature individuals. A predominance of young males was encountered with 66% of the males or 41.4% of the total population. These males were aged of 11–25 years compared with 75% of the females or 20.7% of the total population [5].
In spring-summer 2001, Znari et al. [13] reported significant differences in size-structure, but not age-structure among three populations (the central Jbilet Mts, Admine forest and Near Essaouira) of west-central Morocco (Figure 8). No tortoises older than 16–18 years were found at any site. Most populations of tortoises suffered over-collecting for the tourist trade in the past, and some collecting still continues, which probably explains the lack of older tortoises. Juveniles (age < 7 year) represented 21 and 23% of the population for Jbilet and Essaouira, respectively, but only 14% for Admine. Young adults (7–12 year) were less frequently encountered in Essaouira (47%) than in Jbilet (61%) and Admine (68%). Conversely adults older than 12 year were more frequently encountered in Essaouira (28%) than in Jbilet and Admine (18% each). Sex-ratios were not significantly different from 1 (or 1:1) for both Jbilet and Essaouira populations, whereas for Admine, the sex-ratio was male biased (1.69 or 1:0.59) [13].
In the central Jbilet Mts, the apparent age-structure of tortoises captured during the activity season (mid-February to late May 2003) was characterized by the lack of juveniles aged from 2 to 5 years old. Most of the individuals (74%) were larger than 100 mm in carapace length and 72% more than 7 years old [14]. The age distribution was not significantly different between males and females [22]. In spring 2012, the apparent frequency distribution of the captured tortoises was characterized by the scarcity of juveniles aged 1–5 years, which accounted only for 5% of the total population. Most individuals observed (95%) were adults with a carapace length > 100 mm. The age-class structure among male and female subpopulations was significantly different. The adult sex ratio was male-biased, estimated to 1.2 (55% of males) [22] and 1.57 (61% of males), respectively in spring 2003 [7] and 2012 [22]. Females were significantly distributed in larger classes, the largest adult female and male reached the respective sizes of 190 and 148 mm.
The estimated population size in spring 2003 was 192 ± 20 corresponding to a 5.9 ind./ha population density [7]. Male and female subpopulation size estimates were respectively 121 ± 19 and 100 ± 18. In spring 2012, the estimated population size declined to an average of 88 ± 4 ind. leading to a mean population density of 2.7 ind./ha [22]. This indicates a considerable decline of 54% in less than 10 years. Mean annual survival rates for adult male and female tortoises, estimated during the period of 2008–2012, were respectively 0.86 ± 0.12 (confidence interval range: 0.743–0.978) and 0.81 ± 0.18 (confidence interval range: 0.634–0.987) [22].
5.8. Predation and parasites
5.8.1. Predation
Predation, while almost exclusively a threat to eggs, hatchlings, and small juvenile tortoises, continues to be an ever-present threat. Nevertheless, in hatchlings, and to a lesser extent, in juveniles the shell is soft and/or not solid enough to resist to many predators such as canids, or birds for example (e.g., [26, 27]). In an open landscape, the predation on these fragile tortoises can be severe; sometimes leaving strong marks on the population dynamics [27]. In the Admine forest (Souss Valley), common predators of hatchlings observed in this region include hedgehogs, rats and birds of prey [5]. In an Argan (
5.8.2. Parasitism
Most of tortoises in central Jbilet Mts are infested, at various degrees, with ticks (with up to 10 ticks on the same tortoise) [21]. The infesting ticks, mostly
6. Threats and conservation status
As the other Mediterranean populations, North African populations of
Znari et al. [13] reported on having counted not less than 692
Tortoises are long-lived animals with high adult survival rates, late sexual maturity, low hatching and juvenile survival rates and a specialized diet. Because of this, increases in adult mortality due to overexploitation of adult specimens in a tortoise population will have long-term impacts on the population viability, making them very sensitive to the pet trade ([7, 18, 22, 33]. Bayley and Highfield [5] indicated that the population of tortoises observed in the lower Souss Valley near Agadir was not sustainable; the age sex structure showed a marked predominance of males and a notably small percentage of juveniles. This could be the same case for the population of the central Jbilet [22] and maybe other populations in west-central Morocco. The lower Souss Valley is not currently subject to collecting, although it was a collecting area in the past [4]. However, the current population structure has also been adversely affected by the severe environmental degradation, this area has suffered as a result of the collection of wood, overgrazing and cultivation resulting in deforestation and soil erosion both of which result in a serious reduction in availability of plant fodder which forms the natural diet of
In other parts of Morocco, like the Jbilet Mts, the jujube,
7. Conservation and restoration potentials
An analysis of the conservation and restoration potentials of
8. Conclusion
The Souss Valley tortoise,
Acknowledgments
We are very indebted to all students and colleagues who helped in the field and/or laboratory works, especially M Naimi and S Namous; with a special thank to the inhabitants of Douar (small village) Salas. We would like to thank all colleagues who collaborated in various aspects of our research works, namely M Carretero, JD Harris, D Germano, J Anadon and JC Macé. Finally, we would like to thank the British Ecological Society, UK for the grant they provided for research on trophic and nutritional ecology of
Conflict of interest
There is no conflict of interest between the two authors about the content of the present chapter.
References
- 1.
Schleich HH, Kästle W, Kabisch K. Amphibians and Reptiles of North Africa. Koenigstein: Koeltz Scientific Books; 1996. p. 630. ISBN-13: 978-3874293778 - 2.
Anadón JD, Giménez A, Graciá E, Pérez I, Ferrández M, Fahd S, EL Mouden EH, Kalboussi M, Jdeidi T, Larbes S, Rouag R, Slimani T, Znari M, Fritz U. Distribution of Testudo graeca in the Western Mediterranean according to climatic factors. Amphibia-Reptilia. 2012;33 :285-296. DOI: 10.1163/156853812X643710 - 3.
Lambert MRK. Studies on the growth, structure and abundance of the mediterranean spur-thighed tortoise, Testudo graeca , in field populations. Journal of Zoology. 1982;196 :165-189 - 4.
Lambert MRK. Some factors influencing the Moroccan distribution of the western Mediterranean spur thighed tortoise, Testudo graeca graeca L. and those precluding its survival in NW Europe. Zoological Journal of the Linnean Society. 1983;79 (2):149-179 - 5.
Bayley JR, Highfield AC. Observations on ecological changes threatening a population of Testudo graeca graeca in the Souss Valley, Southern Morocco. Chelonian Conservation and Biology. 1996;2 :36-42 - 6.
Carretero MA, Znari M, Harris DJ, Macé JC. Morphological divergence among populations of Testudo graeca from west-central Morocco. Animal Biology. 2005;55 :259-279 - 7.
El Mouden EH, Slimani T, Ben Kaddour K, Lagarde F, Ouhammou A, Bonnet X. Testudo graeca graeca feeding ecology in an arid and overgrazed zone in Morocco. Journal of Arid Environments. 2006;64 :422-435. DOI: 10.1016/j.jaridenv.2005.06.010 - 8.
Lagarde F, Louzizi T, Slimani T, El Mouden H, Ben Kaddour K, Moulherat S. Bushes protect tortoises from lethal overheating in arid areas of Morocco. Environmental Conservation. 2012; 39 :172-182. DOI: 10.1017/S0376892911000634 - 9.
Moulherat S, Delmas V, Slimani T, El Mouden EH, Louzizi T, Lagarde F, Bonnet X. How far can a tortoise walk in open habitat before overheating? Implications for conservation. Journal for Nature Conservation. 2014; 22 :186-192. DOI: /10.1016/j.jnc.2013.11.004 - 10.
Hichami N, Znari M, Naimi M, Namous S. Clutch, egg and hatchling characteristics in the Souss Valley tortoises, Testudo graeca soussensis Pieh, 2001 (Testudines: Testudinidae) from an arid steppe-land of west-central Morocco. African Journal of Herpetology. 2016;65 (1):21-32. DOI: 10.1080/21564574.2015.1136701 - 11.
Pieh A. Testudo graeca soussensis , eine neue Unterart der Maurischen Landschildkröte aus dem Sousstal (Nordwest-Marokko). Salamandra. 2001;36 :209-222 - 12.
Harris DJ, Znari M, Macé JC, Carretero MA. Genetic variation in Testudo graeca from Morocco estimated using 12S rRNA DNA sequencing. Revista Española de Herpetología. 2003;16 :5-9 - 13.
Znari M, Germano DJ, Macé JC. Growth and population structure of the Moorish tortoise ( Testudo graeca graeca ), in western central Morocco: Possible effect of over-collecting for the tourist trade. Journal of Arid Environments. 2005. DOI: 10.1016/j.jaridenv.2004.11.013 - 14.
Ben Kaddour K, El Mouden EH, Slimani T, Bonnet X, Lagarde F. Sexual dimorphism in the Greek Tortoise: A test of the body shape hypothesis. Chelonian Conservation and Biology. 2008; 7 :21-27. DOI: 10.2744/CCB-0649.1 - 15.
Highfield AC, Martin J. Testudo whitei Bennet 1839. New light on an old carapace—Gilbert White’s Selborne tortoise re-discovered. Journal of Chelonian Herpetology. London. 1989;1 (1):13-22 - 16.
Highfield AC. Tortoises of north Africa; taxonomy, nomenclature, phylogeny and evolution with notes on feld studies in Tunisia. Journal of Chelonian Herpetology. London. 1990; 1 (2):1 - 17.
Fritz U, Harris DJ, Fahd S, Rouag R, Martínez EG, Casalduero AG, Široký P, Kalboussi M, Jdeidi TB, Hundsdörfer AK. Mitochondrial phylogeography of Testudo graeca in the Western Mediterranean: Old complex divergence in North Africa and recent arrival in Europe. Amphibia-Reptilia. 2009;30 :63-80. DOI: 10.1163/156853809787392702 - 18.
Schweiger M. Herpetologische Beobachtungen im Gebiet von Ouarzazate (Marokko). Herpetozoa, Vienna. 1992; 5 (1/2):13-31 - 19.
Bons J, Geniez P. Amphibiens et Reptiles du Maroc (Sahara Occidental compris). Atlas biogéographique. Barcelona (Asociación Herpetológica Española). 1996:320 - 20.
Pieh A, Perälä J. Variabilität der Maurischen Landschildkröten ( Testudo graeca Linnaeus, 1758 – Komplex) im zentralen und nordwestlichen Marokko mit Beschreibung zweier neuer Taxa. Herpetozoa. 2004;17 :19-47 - 21.
Anadón JD, Graciá E, Botella F, Giménez A, Fahd S, Fritz U. Individualistic response to past climate changes: Niche differentiation promotes diverging Quaternary range dynamics in the subspecies of Testudo graeca . Ecography. 2015;38 (9):956-966. DOI: 10.1111/ecog.01163 - 22.
Hichami N. Ecophysiology & Conservation ecology of the Souss Valley tortoises, Testudo graeca soussensis Pieh, 2001 (Testudines: Testudinidae), in an arid area of west central Morocco [thesis]. Faculty of Science—Semlalia, Marrakech, Morocco: Cadi Ayyad University; 2017 - 23.
Lovich JE, Gibbons JW. A review of techniques for quantifying sexual size dimorphism. Growth, Development and Aging. 1992; 56 :269-281 - 24.
Krüger E. Near-natural incubation of Testudo graeca soussensis Pieh, 2000. Eggs. Radiata. 2007;16 :42-43 - 25.
Sereau M, Lagarde F, Bonnet X, El Mouden EH, Slimani T, Dubroca L, Trouvé C, Dano S, Lacroix A. Does testosterone influence activity budget in the male Greek tortoise ( Testudo graeca graeca )? General and Comparative Endocrinology. 2010;167 :181-189. DOI: 10.1016/j.ygcen.2010.03.002 - 26.
Keller C, Diaz-Paniagua C, Andreu AC. Survival rates and causes of mortality of Testudo graeca hatchlings in south western Spain. Journal of Herpetology. 1998;32 :238-243. DOI: 10.2307/1565303 - 27.
Boarman WI. Reducing predation by Common Ravens on Desert Tortoises in the Mojave and Colorado deserts. USGS: Science for a Changing World; 2002. p. 39 - 28.
Barje F, Slimani T, EL Mouden EH, Lagarde F, Bonnet X, Ben Kaddour K. Shrewd shrikes and spiny shrubs: A calmity for hatchling Moorish tortoises ( Testudo graeca graeca ). Amphibia-Reptilia. 2005;26 :113-115. DOI: 10.1163/1568538053693341 - 29.
Kireçci E, Özer A, Balkaya I, Taniş H, Deveci S. Identification of Ticks on Tortoises ( Testudo graeca ) and Investigation of Some Pathogens in these Ticks in Kahramanmaraş, Turkey. KSU Journal of Natural Sciences. 2013;16 (1):42-46 - 30.
Hidalgo-Vila J, Dıaz-Paniagua C, Ruiz X, Portheault A, El Mouden EH, Slimani T, Frutos-Escobar C, De Caso MS. Salmonella in free-living spur-thighed ( Testudo graeca ) from Central Western Morocco. Veterinary Record. 2008;162 (7):218-219 - 31.
Lambert MRK. On growth of captive-bred Mediterranean Testudo in N. Europe. In: Rocek Z, editor. Studies in Herpetology. Prague: Charles University; 1985. pp. 309-314 - 32.
Pleguezuelos JM, Brito JC, Fahd S, Feriche M, Mateo JA, Rueda GM, Reques R, Santos X. Setting conservation priorities for the Moroccan herpetofauna: The utility of regional red lists. Fauna & Flora International, Oryx. 2010; 44 (4):501-508. DOI: 10.1017/S0030605310000992 - 33.
Nijman V, Bergin D. Trade in spur-thighed tortoises Testudo graeca in Morocco: volumes, value and variation between markets. Amphibia-Reptilia. 2017;38 (3):1-13. DOI: 10. 1163/15685381-00003109