Herpetology Notes, volume 14: 959-963 (2021) (published online on 30 June 2021)

First record of abnormal tail regeneration in the Moroccan endemic gecko, Quedenfeldtia trachyblepharus (Boettger, 1874), and for the family Sphaerodactylidae

Jalal Mouadi1, Abderrafea Elbahi3, Omar Er-rguibi2, El-Mustapha Laghzaoui2, Abdessamad Aglagane1, Ahmed Aamiri1, El Hassan El Mouden2,*, and Mohamed Aourir1

The Atlas Day Gecko, Quedenfeldtia trachyblepharus (ca. 31.20°N, 7.87°W, elevation 2700 m). The site is (Boettger, 1874), is a small high-elevation gecko covered in fractured sandstone rocks and characterized (maximum snout–vent length, SVL 4.4 cm; weight 3 by mountainous vegetation with plants of alpine and g) endemic to the High Atlas Mountains of Morocco boreal origin (Haroni et al., 2009). The climate is cold (Loveridge, 1947). These geckos generally live temperate, with precipitation around 500–600 mm per in open rocky habitats and are regularly observed year and mean temperatures ranges from 4–22°C. basking close to rock crevices, often communally. Mean snout-to-vent length and the mean weight of The species is oviparous, and females typically lay the four abnormal individuals were 46.2 ± 1.7 mm their eggs in rock crevices (Schleich et al., 1996; and 2.02 ± 0.28 g respectively. Two males and one Bouazza et al., 2016). Quedenfeldtia trachyblepharus female presented with a bifurcation of regenerated is the dominant species in the alpine lizard assemblage tail material, whereas the second female possessed above an elevation of 2500 m (Bons and Geniez, 1996; a trifurcation (Fig. 1). In all cases, the anomalies are Comas et al., 2014). A clear sexual dimorphism in well defined with distinctive branches. dorsal colouration exists (Blouin-Demers et al., 2013) In one male individual (Fig. 1A), the tail appears to allowing identification of sex by sight. Like many have been injured at a distance 44.1 mm from the vent, lizards, Q. trachyblepharus can shed its tail (caudal with the distal portion preserved past the breakage autotomy) to escape predation and sometimes during point. There, beginning regeneration of a second intra-specific territorial conflicts (Arnold, 1984). After branch is visible (Fig. 1A’). The development of this a tail is shed, a process of regeneration is initiated to abnormal branch appears to have caused healing of the replace the autotomized one. Here, we report on four original tail in a deviating position, at an angle > 130° individuals of Q. trachyblepharus (two females, two towards the body of the gecko. The row of subcaudal males) with abnormal tail regeneration. scales continues in a single, unbroken line onto the The geckos were among a sample of 199 individuals original tail in its angled position (Fig. 1A’). captured and examined during 2019–20 in the In the second male individual (Fig. 1B, B’), Oukaimeden Region, High Atlas Mountains, Morocco branching begins at approximately the same point as seen in the first male, 42.3 mm from the vent. Based on its length and colour pattern it appears that the longer branch is the original tail (branch length = 14.9 mm), 1 Laboratory of Biodiversity and Ecosystem Functioning, Faculty and the shorter (length 6.2 mm), plain black portion is of Sciences, Ibn Zohr University, Agadir, Morocco. regenerated. Both parts of the bifurcation are oriented 2 Laboratory of Water, Biodiversity, and Climatic Change, in the same direction. The abnormality may impede the Faculty of Sciences Semlalia, Cadi Ayyad University, gecko’s ability to shed its skin cleanly, as evidenced by Marrakech, Morocco. 3 Venom Systems and Proteomics Lab, Ryan Institute, National the skin remnant still attached to the original portion of University of Ireland Galway, Ireland; and Laboratory of the tail (Fig. 1B’). Oceanography and Fisheries, Faculty of Sciences, Ibn Zohr One of the females presents with a very unusual University, Agadir, Morocco. bifurcation, in which a short branch of the tail appears * Corresponding author. E-mail: [email protected] to grow in an anterior direction, with a larger branch © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. continuing in the normal direction along the body axis. 960 Jalal Mouadi et al.

Figure 1. Male and female Atlas Day geckos, Quedenfeldtia trachyblepharus, from the Oukaimeden Region, Morocco, presenting with abnormal, regenerated tails. In each image pair, the right image shows a close-up of the abnormal section. (A, A’) Male gecko with a healed, incomplete tail break and a short, abnormal growth at the site of the break. The ventral view in (A’) shows the continuing subcaudal scale row at the site of the break. (B, B’) Male gecko with a narrow bifurcation, which did not allow the complete shedding of the skin. (C, C’) Female gecko displaying extra growth, presumably after an incomplete tail break, in the proximal half of the tail. (D, D’) Female with a branched, trifurcated tail, displaying two consecutive, Y-shaped branches. Photos by O. Er-rguibi (A, B, D) and J. Mouadi (C). Abnormal Tail Regeneration in Quedenfeldtia trachyblepharus 961

The entire tail of this female had been autotomized in of the Family Sphaerodactylidae, which is widely the past, based on the change in colour pattern and the distributed across South America, the Caribbean, narrowing of the tail proximally (Fig. 1C). This break northern Africa, and the Middle East (Gamble et al., likely occurred in one of the most proximal autotomic 2008; Uetz et al., 2021). In Morocco, this family is caudal vertebrae. The regenerated bifurcation is represented by two species of Quedenfeldtia and six therefore the result of a second tail breakage about species of Saurodactylus (Bons and Geniez, 1996; 7.5 mm from the base of the tail, and the unusual Javanmardi et al., 2019). Our finding therefore morphology probably derived from an injury to the represents the not only the first record of abnormal tail region of active regrowth. In dorsal view (Fig. 1C’), growth and regrowth in Q. trachyblepharus but for the the right, better developed branch has a length of 19.2 entire Family Sphaerodactylidae. mm; it is probably the primary regenerated branch and Abnormal tail regeneration in Q. trachyblepharus grew unimpeded by the injury to the regrowth region. seems to occur as a result of incomplete caudal The left, shorter branch is 8.2 mm long and diverges autotomy when a new tail grows out of the side rather from the right branch at an angle of approximately than at the tip of the injured, original tail (Bateman 90°, with its tip beginning to align itself to the gecko’s and Fleming, 2009; Pheasey et al., 2014). The injured body axis. It likely constitutes a secondary centre of point allows the generation of an additional tip (Chan regeneration, with growth slowed by both injury and et al., 1984; Gogliath et al., 2012), which may induce abnormal direction. one or more structures to regenerate In general, tail The other female displays a “trifurcation” anomaly, abnormalities in lizards range from bifurcations to comprising two successive bifurcations (Fig. 1D, D’). hexafurcations, with bifurcation much more frequent The first bifurcation begins 24.9 mm posterior to the (86%) than trifurcations (12%) or multifurcations vent, the second 7.7 mm beyond the first. In this case, (2%) (Barr et al., 2020). In fact, tail bifurcation has the cause for the successive bifurcations is not obvious been widely documented for several groups of lizards and, given that the shorter portions are consistent with (Chan et al., 1984; Anajeva and Danov, 1991; Gogliath the morphology and scalation of the main tail (at left et al., 2012; Martins et al., 2013; Koleska et al., 2017; in Fig. 1D’), they may do not appear to be related to Vergilov and Natchev, 2017; Koleska, 2018). In tail autotomy. Perhaps slight injury of distal elements geckos, the percentage of species with abnormal tail in the tail can prompt non-regenerative growth as regeneration in each family ranges from 2–4%, but observed here. This situation therefore appears to be in the Sphaerodactylidae and Carphodactylidae these different than in the three other individuals, which values are lower (0.4% and 0%, respectively; Table 1). presented with definite tail regeneration. The low documentation of abnormal tail regeneration Abnormal tail regeneration has been documented in in these two families is probably due to reduced over 175 different species of lepidosaurs across 22 of sampling effort. It is possible, but speculative, that 45 recognized families (Barr et al., 2020), but until low incidence could be linked to low survival rates of now it has not been reported in any of the 228 species individuals with abnormal regeneration, perhaps by

Table 1. Gecko families with abnormal, regenerated tails (Barr et al., 2020) and the total number of species in each family (Uetz et al., 2021‎). The asterisk (*) denotes the current record.

Species with Tail Family Species Total Abnormalities Carphodactylidae 0 32 Pygopodidae 2 46 Diplodactylidae 6 157 Eublepharidae 1 43 Phyllodactylidae 5 151 Gekkonidae 26 1400 Sphaerodactylidae 1* 228 962 Jalal Mouadi et al. affecting their ability to escape (Gamble et al., 2015). C. (1984): Morphological anomalies of two geckos, Future studies are needed to test the ecological impact Hemidactylus frenatus and Lepidodactylus lugubris, and the of these abnormalities on gecko families with small toad, Bufo marinus, on the island of Hawaii. In: Proceedings of the Fifth Conference in Natural Sciences, Hawaii Volcanoes and cryptic individuals. National Park, p. 41–50. Smith, C.W., Ed., Manoa, Hawaii, In terms of our surveys, geckos with abnormal tails USA, University of Hawaii. represented four of 199 individuals (2%), a figure Comas, M., Escoriza, D., Moreno-Rueda, G. (2014): Stable close to the mean of 2.75 ± 3.41% estimated within isotope analysis reveals variation in trophic niche depending lizard populations in general (Barr et al., 2020). on altitude in an endemic alpine gecko. Basic and Applied According to previous studies, species that readily use Ecology 15: 362–369. caudal autotomy may be predicted to be less likely to Gamble, T., Bauer, A.M., Greenbaum, E., Jackman, T.R. (2008): Evidence for Gondwanan vicariance in an ancient clade of generate abnormal regenerations (Barr et al., 2020). gecko lizards. Journal of Biogeography 35: 88–104. Our observations do not allow us to elucidate the Gamble, T., Greenbaum, E., Jackman, T.R., Bauer, A.M. (2015): effects of abnormal tail regeneration on gecko survival. Into the light: diurnality has evolved multiple times in geckos. However, a lizard with an abnormality could be Biological Journal of the Linnean Society 115: 896–910. competitively inferior and sexually unattractive, which Gogliath, M., Pereira, L.C.M., Nicola, P., Ribeiro, L.B. (2012): may result in a decline in social status and reproductive Natural history notes. Ameiva ameiva (Giant Ameiva). fitness (Martin and Salvador, 1993; Maginnis, 2016). Bifurcation. Herpetological Review 43(1): 129. Haroni, A., Alifriqui, M., Simonneaux, V. (2009): Recent Furthermore, morphological anomalies may affect dynamics of the wet pastures at Oukaimeden plateau lizards by negatively influencing locomotion, escape (High Atlas mountains, Morroco) [sic]. Biodiversity and mechanisms, and anti-predator tactics (Barr et al., Conservation 18: 167–189. 2020). In fact, intact tails are important for territorial Higham, T.E., Russell, A.P., Zani, P.A. (2013): Integrative biology defence and play crucial roles in locomotion and intra- of tail autotomy in lizards. Physiological and Biochemical specific social interactions (Bateman and Fleming, Zoology 86: 603–610. 2009; Higham et al., 2013; McElroy and Bergmann, Jagnandan, K., Russell, A.P., Higham, T.E. (2014): Tail autotomy and subsequent regeneration alter the mechanics of locomotion 2013; Jagnandan et al., 2014). in lizards. Journal of Experimental Biology 217: 3891–3897. Javanmardi, S., Vogler, S., Joger, U. (2019): Phylogenetic References differentiation and taxonomic consequences in the Ananjeva, N.B., Danov, R.A. (1991): A rare case of bifurcated Saurodactylus brosseti species complex (Squamata: caudal regeneration in the Caucasian agama, Stellio caucasius. Sphaerodactylidae), with description of four new species. Amphibia-Reptilia 12: 343–356. Zootaxa 4674(4): 401–425. Arnold, E.N. (1984): Evolutionary aspects of tail shedding Koleska, D. (2018): First record of tail bifurcation in Asaccus in lizards and their relatives. Journal of Natural History 18: gallagheri from the United Arabian Emirates. Herpetology 127–169. Notes 11: 115–116. Barr, J.I., Somaweera, R., Godfrey, S.S., Gardner, M.G., Koleska, D., Svobodová, V., Husák, T., Kulma, M., Jablonski, Bateman, P.W. (2020): When one tail isn’t enough: abnormal D. (2017): Tail bifurcation recorded in Sauromalus ater. caudal regeneration in lepidosaurs and its potential ecological Herpetology Notes 10: 363–364. impacts. Biological Reviews 3: 1–18. Loveridge, A. (1947): Revision of the African lizards of the Bateman, P.W., Fleming, P.A. (2009): There will be blood: family Gekkondiae. Bulletin of the Museum of Comparative autohaemorrhage behaviour as part of the defence repertoire Zoology 98(1): 1–469. of an insect. Journal of Zoology 278: 342–348. Maginnis, T.L. (2016): The costs of autotomy and regeneration Blouin-Demers, G., Lourdais, O., Bouazza, A., Verreault, C., in animals: a review and framework for future research. El Mouden, H., Slimani, T. (2013): Patterns of throat colour Behavioral Ecology 17: 185–189. variation in Quedenfeldtia trachyblepharus, a high-altitude Martin, J., Salvador, A. (1993): Tail loss reduces mating success gecko endemic to the High Atlas Mountains of Morocco. in the Iberian rock-lizard, Lacerta monticola. Behavioral Amphibia Reptilia 34: 567–572. Ecology and Sociobiology 32: 185–189. Bons, J., Geniez, P. (1996): Amphibiens et Reptiles du Maroc Martins, R.L., Peixoto, P.G., Fonseca, P.H.M., Martinelli, A.G., (Sahara Occidental Compris). Atlas Biogéographique. Silva, W.R., Pelli, A. (2013): Abnormality in the tail of the Barcelona, Spain, Asociación Herpetológica. collated lizard Tropidurus gr. torquatus (Iguania, Tropiduridae) Bouazza, A., Slimani, T., El Mouden, H., Lourdais, O. (2016): from Uberaba City, Minas Gerais State, Brazil. Herpetology Thermal constraints and the influence of reproduction on Notes 6: 369–371. thermoregulation in a high-altitude gecko (Quedenfeldtia McElroy, E.J., Bergmann, P.J. (2013): Tail autotomy, tail size, trachyblepharus). Journal of Zoology 300: 36–44. and locomotor performance in lizards. Physiological and Chan, J.G., Young, L.L., Chang, P.R.K., Shero C.M., Watts, Biochemical Zoology 86: 669–679. Abnormal Tail Regeneration in Quedenfeldtia trachyblepharus 963

Pheasey, H., Smith, P., Atkinson, K. (2014): Natural history notes. Vanzosaura rubricauda (Red-tailed Vanzosaur). Bifurcation and Trifurcation. Herpetological Review 45: 138–139. Schleich, H.H., Kästle, W., Kabisch, K. (1996): Amphibians and Reptiles of North Africa: Biology, Systematics, Field Guide. Königstein, Germany, Koeltz Scientific Books. Uetz, P., Freed, P., Hošek, J. (2021): The Reptile Database. Available at: http://www.reptile-database.org. Accessed on 12 February 2021. Vergilov, V., Natchev, N. (2017): First record of tail bifurcations in the snake-eyed skink (Ablepharus kitaibelii Bibron & Bory de Saint-Vincent, 1833) from Pastrina Hill (northwestern Bulgaria). Arxius de Miscellania Zoologica 15: 224–228.

Accepted by Timothy Colston