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

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First record of abnormal tail regeneration in the Moroccan endemic gecko, Quedenfeldtia trachyblepharus (Boettger, 1874), and for the family ...
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: elmouden@uca.ac.ma                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
                                                                       toad, Bufo marinus, on the island of Hawaii. In: Proceedings
of these abnormalities on gecko families with small
                                                                       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.
                                                                    Gamble, T., Bauer, A.M., Greenbaum, E., Jackman, T.R. (2008):
caudal autotomy may be predicted to be less likely to
                                                                       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).
                                                                       Bifurcation. Herpetological Review 43(1): 129.
fitness (Martin and Salvador, 1993; Maginnis, 2016).
                                                                    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.
                                                                    Jagnandan, K., Russell, A.P., Higham, T.E. (2014): Tail autotomy
2009; Higham et al., 2013; McElroy and Bergmann,
                                                                       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
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                                                                      Accepted by Timothy Colston
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