Acta Herpetologica 14(1): 65-68, 2019 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.13128/Acta_Herpetol-24806 Age structure of a population of Discoglossus scovazzi Camerano, 1878 (Anura - Discoglossidae) in extreme environmental conditions (High Atlas, Morocco) Mohamed Amine Samlali, Abderrahim S’khifa, Tahar Slimani* Cadi Ayyad University, Faculty of Sciences Semlalia, Biodiversity and Ecosystems Dynamic Laboratory, PO Box 2390, Marrakech 40 000, Morocco. *Corresponding author. Email: slimani@uca.ac.ma Submitted on: 2019, 25th February; Revised on: 2019, 12thApril; Accepted on: 2019, 29th April Editor: Fabio M. Guarino Abstract. The age structure and growth of the Moroccan Painted Frog (Discoglossus scovazzi Camerano, 1878) in a population living in the High Atlas at the upper altitudinal limit of the species’ range was estimated for the first time by skeletochronology. Individual age was determined by counting the lines of arrested growth (LAGs) from cross- sections of the phalanges. Both males and females reached sexual maturity at 3-4 years of age at which point the speed of osteogenesis and body growth slow down. Males and females have maximum lifespans of six and five years, and average sizes of 47. 50 mm (n = 21, SD = 1.40) and 39.70 mm (n = 53, SD = 0.90) respectively. We detected a positive relationship between age and size, suggesting that the oldest individuals are always bigger and heavier. Sizes corre- sponding to the same age class are very heterogeneous reflecting divergent conditions and growth strategies. Keywords. Endemic species, skeletochronology, life-history traits, extreme environment, Morocco. Degradation and fragmentation of natural habitats due to human activities have harmful effects on amphib- ian populations (Collins and Crump, 2009; Hamer and Mcdonnell, 2008, 2010; Collins and Fahrig, 2017). The central plateau of the Oukaimeden massif in the High Atlas region of Morocco has been heavily impacted by overgrazing and the banks of its two main rivers are seri- ously degraded by the bulk removal of sand for construc- tion (Ait Babahmad, 2012; Ait Zidan, 2018). Both human activities have degraded water habitats and altered the richness and abundance of their amphibian communi- ties. Morphological abnormalities have been recorded in adults and tadpoles (Ait Babahmad, 2012; Lansari, 2018), especially in the frog Pelophylax saharicus, which is wide- spread in the massif. This habitat degradation could cause a demographic collapse leading to local disappearances (Mckinney, 2002; Löfvenhaft et al., 2004; Bionda et al., 2013; Babini et al., 2015; Green and Bailey, 2015; Zhelev et al., 2017), especially in species that are relatively sen- sitive to human activities due to habitat specialization or specific life history (Rubbo and Kiesecker, 2005; Hamer and Mcdonnell, 2008, 2010). The Moroccan Painted Frog (Discoglossus scovazzi Camerano 1878, family Discoglossidae) is listed as Least Concern in the IUCN Red List of Threatened Species (Salvador et al., 2009; Başkale et al., 2018). Endemic to Morocco, the species is generally common, especially in sub-humid and humid areas. They are quite cryptic out- side the breeding season, with adults preferring the prox- imity of small bodies of water such as temporary ponds, low-flow streams and sources. Although the species may tolerate a slight modification of its habitat, its sensitivity to the particular conditions and the quality of its aquatic and terrestrial environment remains largely unknown (Reques et al., 2013). Because the demographic changes are in response to environmental conditions (Sinsch et al., 2004; 66 Mohamed Amine Samlali, Abderrahim S’khifa, Tahar Slimani Sinsch et al., 2007; Spear et al., 2009), the purpose of this study is to estimate the age structure, age at first repro- duction and longevity of a high mountain population of Discoglossus scovazzi, by using skeletochronology. Discoglossus scovazzi is an anuran of small body size known from a large number of aquatic biotopes through- out Morocco from sea level up to the Atlas Mountains, excluding the Saharan areas. It reaches its upper altitudi- nal limit in the High Atlas at Oukaimeden, over 2600 m a.s.l. (Bons and Geniez, 1996). This study is based on mark-recapture tracking of 74 adult individuals (21 males and 53 females) between 2016 and 2018. The study took place at the population’s breeding site, which consists of small pools of water fed by a permanent watercourse. Solitary and discreet during most of the year, Discoglossus scovazzi begins reproduc- tion in early spring (Ait Babahmad, 2012; Beukema et al., 2013; Samlali, 2016). Egg-laying is spread over 8 to 10 days from early April to mid-June. During this peri- od, the water temperature is about 13 °C and the outside temperature is about 10 °C. The population is located at 2660 m of altitude in the Oukaimeden massif (31°11’N, 07°50’W) about 75 km South-East of Marrakech. The climate is typically Medi- terranean with cold winters and an average annual tem- perature of 9.5 °C. The average maximum temperature of the hottest month (July) is 22.2 °C and the average minimum temperature of the coldest month (January) is -3.3 °C. The average annual precipitation is circa 518 mm and snow fall mainly between November and March. The dry period lasts about four months (June-September). The vegetation consists of spiny xerophytes and a herba- ceous layer, essentially graminaceous, relatively rich dur- ing rainy periods but heavily overgrazed. The population breeds in pits (diameter 6-7 m and at least one meter deep) that resulted from sand extraction and used as waterers in the bed of a permanent river (Assif-N-Irène). Intensive use for livestock watering negatively impacts water quality and accelerates drying (Ait Babahmad, 2012; Samlali, 2016). Sampling by hand occurred from February to June. We measured the frogs from snout to cloaca with calipers and weighed them using a field balance (accuracy: 0.1 g). We determined sex by the presence of nuptial callosities and calling in males. After measurements, we collect- ed the third toe of the left hind leg and we immediately released the frog at the place of its capture. The samples are kept in absolute alcohol. We sectioned phalanges from the toe to count lines of arrested growth (LAGs) following the method by Cas- tanet and Smirina (1990), which is based on the detec- tion of LAGs generated by the cold season (each LAG is interpreted as one year of age). In order to avoid the errors of the estimation of the age induced by the med- ullary resorption (Francillon-Vieillot, 1987; Fretey and Le Garff, 1992; Tsiora and Kyriakopoulou-Sklavounou, 2002; Guarino et al., 2003; 2008; Liao and Lu, 2010; Liao, 2011; Huang et al., 2013; Bionda et al., 2015; Jin et al., 2017), we selected, for each individual, diaphysis sections in which the size of the medullar cavity was at its minimum and that of the periosteal bone at its maximum (Oromi et al., 2016). On the other hand, bone remodeling and the close rapprochement of the outer most lines, espe- cially in the oldest individuals (Wagner et al., 2011) could also compromise the age estimation. In these cases, at the insertion site of the phalangeal ligament allows to discern the peripheral LAGs and to reliably count them (Bion- da et al., 2018). The number of lines of arrested growth (LAGs) in each section is counted by three authors (M.A.S., A.S. and T.S.). Since all the individuals studied were collected during the breeding season, the age at sex- ual maturity was revealed by the presence of LAGs sud- denly becoming very closely adjacent, reflecting the slow- ing of growth after sexual maturity. All variables were first tested for normality (Kol- mogorov-Smirnov test) and the difference between sexes was tested using ANOVA. In addition, the relationship between size and age was analyzed by Spearman correla- tion test. We used the significance level of alpha = 0.05 in all tests. A total of 74 reproductive adults (21 males and 53 female) were studied. Individuals were collected at breeding sites during the reproduction periods in 2016, 2017 and 2018. The cross-sections show the presence of strongly stained growth lines in periosteal bone in most individuals (Fig. 1). Since the frogs were collected in March and April, we considered the perimeter of the bone as corresponding to an indicator LAG of last win- ter. We clearly detected a decrease in the distance that Fig. 1. Transverse sections at diaphysal region of phalanx bones of Discoglossus scovazzi. (A) Male with 6 visible LAGs. (B) Female with 4 visible LAGs (CM: medullary cavity. 67Age structure of Discoglossus scovazzi separating the LAGs suggesting that sexual maturity is reached at 3-4 years in both males and females (Fig.1 A, B). At the breeding site, we sampled some females young- er than three years, although three-year individuals were the most frequently observed (Fig. 2). Highest estimated age is six years in males and five years in females. Body size varied from 34.0 to 64.0 mm in males (mean ± SD = 47.5 ± 1.4 mm, n = 21) and from 33.0 to 56.1 mm in females (39.7 ± 0.9 mm, n = 53), with a mass of 14.5 ± 5.17 g in males and 8.05 ± 3.45 g in females. The observed pattern of sexual dimorphism in body size was significant (F1, 72 = 21.4; P < 0.0001). Because we did detect a significant relationship between age and body size in males (r = 0.786, P = 0.018, n = 21) and in females (r = 0.847, P = 0.003, n = 53) (Fig. 3), the oldest individ- uals were always the largest ones. Indeed, anurans often exhibit continuous growth, particularly females because of the strong relationship between fecundity and body size (Lengagne et al., 2007). In most anuran species, males are smaller than females (Shine, 1979). For D. scovazzi, the sexual size dimorphism is inversed (García-Paris et al., 2004; Oromi et al., 2016). The variation in size dimorphism results from differences in the age structure between sexes (Monnet and Cherry, 2002; Liao et al., 2013a, b). In fact, in species where females exhibit smaller sizes (Rhinella achalensis, Rana cascadae and Hylarana nigrovittata), males mature at later ages (Monnet and Cherry, 2002), suggesting that delayed maturity in males produces size dimorphism as stated in the Rensch’s rule (Liao et al., 2015). However, as in D. pictus (Oromi et al., 2016), we did not find differences in the age structure between the sexes in D. scovazzi which suggests that these two species failed to support Rensch’s rule. In some anuran species, increased male body size is an important determinant of male mating success (Wells, 2007; Liao and Lu, 2011). Furthermore, large males are more likely to breed than smaller ones if competition for females is intense (Oromi et al., 2016). However, little information is available on the mating tactics of D. scovazzi and other factors might explain the sexual size dimorphism in this species. Our study provides original data on the structure of a population at the upper altitudinal limit of this endem- ic species of Morocco. The earliest age at which sexual maturity was attained in most individuals of both sexes is about 3 years. However, the three-year-old frogs, theo- retically fewer numerous than those aged two as a result of annual mortality, are more frequent at breeding sites than younger females. As observed in Brongersma’s Toad in arid environments (Fattah et al., 2014), this asym- metrical age structure in females of Discoglossus scovazzi in the High Atlas suggests that this difference in young females is due to the fact that not all the females reach sexual maturity before three years, or that some females reach sexual maturity at the age of two years. Compared to its Mediterranean congener, D. pictus, studied by Oromi et al. (2016) in North Africa, the late age at maturity in our population suggests a low growth rate in juveniles, strongly constrained by the harsh cli- matic conditions of this alpine environment (low tem- perature, snowfall, strong wind), or the modification of aquatic environments (due to excessive sand removal) and the deterioration of their physico-chemical quality (due to livestock). The low values in terms of longevity (5-6 years) and reproductive potential (about two years) recorded in this population are related to climatic conditions and ongo- ing changes in habitat quality. Several other hypotheses could, however, be formulated, including moving larg- er adults /older to other sites, the low survival of larger individuals /older, or the case of an unstable population maintained by smaller / younger adults. This highlights a need monitoring. Fig. 2. Age distribution of the reproductive population of Discoglos- sus scovazzi at Oukaimeden in 2016-2018. Fig. 3. Relationship between estimated age (X-axis, in year) and body size (Y-axis, snout-vent length in mm) in the studied population. 68 Mohamed Amine Samlali, Abderrahim S’khifa, Tahar Slimani ACKNOWLEDGEMENTS This research was financed by funds from Hassan II Academy of Science and Technics (ICGVSA project, PI Slimani T.). It was authorized by the High Commissariat for Water and Forest (Decision Number 05/2013 HCE- FLCD/DLCDPN/DPRN/CFF) - Morocco. We would like to thank the two anonymous reviewers who provided important comments to improve the manuscript. REFERENCES Ait Babahmad, A. (2012): Diversité en amphibiens dans le massif de l’Oukaimeden (Haut Atlas Central). “Implications en termes de conservation dans le cadre du changement climatique global”. Master II. Faculté des Sciences Semlalia. Ait Zidan, A. 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