Acanthodactylus margaritae, Tamar & Geniez & Brito & Crochet, 2017

Tamar, Karin, Geniez, Philippe, Brito, José C. & Crochet, Pierre-André, 2017, Systematic revision of Acanthodactylus busacki (Squamata: Lacertidae) with a description of a new species from Morocco, Zootaxa 4276 (3), pp. 357-386 : 368-375

Acanthodactylus margaritae sp. nov.

( Tables 1 –3; Figs. 1–8 ; Appendices I–III)

Chresonyms

Acanthodactylus busacki Salvador, 1982: 88 (part.)

Acanthodactylus pardalis bedriagai Arnold, 1983: 319 (part.)

Acanthodactylus bedriagai Harris & Arnold 2000: 352 (part.)

Acanthodactylus busacki Mellado & Dakki 1988: 175 (part.); Mellado & Olmedo 1990: 133 (part.); Bons & Geniez 1996: 162 (part.); Schleich et al. 1996: 391 (part.); Geniez et al. 2004: 102 (part.); Brito et al. 2008: 21 (part.); Sindaco & Jeremčenko 2008: 218 (part.); Fonseca et al. 2008: 9 (part.); Harris el al. 2010: 22 (part.); Barata et al. 2011: 7 (part.); Carretero et al. 2011: 139 (part.); Trape et al. 2012: 302 (part.); Pyron et al. 2013: 17 (part.); Tamar et al. 2016: 8 (part.)

Name bearing type. Muséum national d'Histoire naturelle (Paris) MNHN-RA-2016.0105 (formerly BEV.9439, tissue sample in the BEV tissue collection, code T1176), adult male, collected on the 11th of February 2008 by P.-A. Crochet ( Fig. 6 ).

Type locality. 500 m north-east of Sidi Binzarne , approximately 3 km south-east of Sidi R’bat (Massa), Morocco, 30.0580°N, 9.6456°W (WGS84).

Paratypes. BEV.9440 (tissue sample code T1177, adult female, collected in the Ademine forest 1.6 km past the Agadir-Taroudant road towards Biougra, Morocco, 30.31579°N 9.36004°W, on the 11th of February 2008 by P.- A. Crochet) ; MCCI-R.560 (adult male, collected from between Inchaden and Tifnite, Morocco, 30.15°N, 9.59°W, on the 9th of May 1993 by R. Sindaco and N. Fedrighini) ; MCCI-R.561 (adult male, collected from Souss valley , outskirts of Biougra, Morocco, 30.21°N, 9.38°W, on the 9th of May 1993 by R. Sindaco and N. Fedrighini); MCCI- R.562 (sub-adult female, collected from Souss valley, outskirts of Biougra, Morocco, 30.21°N 9.38°W, on the 9th of May 1993 by R. Sindaco and N. Fedrighini) ( Fig. 7 ).

Other material. Thirty-three voucher specimens listed in Appendix II under A. margaritae sp. nov. apart from the holotype and paratypes. Photographic material of 19 voucher specimens from the BMNH, CAS, FMNH, MB, and ZMH are listed in Appendix II, and of 29 individuals photographed in the wild (only meristic characters and colouration documented; Appendix II).

Etymology. The specific epithet “ margaritae ”, a noun in the genitive case, honours Dr Margarita Metallinou who tragically lost her life during field-work in Africa in July 2015. The new species is dedicated to Margarita Metallinou from all the authors in recognition of her passion, interest and strong contribution to the study of reptile systematics (especially of geckoes of the genera Stenodactylus and Ptyodactylus ) and to her friendship over the years.

Diagnosis. A new species of the pardalis species-group (i.e., small flat or carinated dorsal scales; three series of scales on the fingers; three supraoculars; 12 and sometimes 14 straight longitudinal row of ventrals; slightly pectinate toes; body pattern combining longitudinal rows of light ocelli and black reticulation) from between the High Atlas and Anti-Atlas Mountains characterized by the combination of the following characters: (1) maximum recorded snout-vent length 71 mm (54–71 mm in adult males and 54–64.7 mm in adult females); (2) three supraoculars, the first supraocular is either entire or fragmented with usually one row of granules between the supraoculars and the superciliaries; (3) 16–48 granules around the supraoculars (mean 29.7); (4) subocular with a distinct keel is situated between the fourth and fifth upper labials and does not contact the lip; (5) upper temporals small and pointed whereas the lower temporals are large and smooth; (6) 10–14 collar scales; (7) usually 12 longitudinal rows of ventral scales; (8) 27–34 (mean 31.2) ventral transverse rows; (9) 14–24 (mean 21.1) femoral pores on each side (higher number in males; 14–23 in females vs. 18–24 in males; mostly in contact in males, separated in females); (10) three rows of scales on fingers with slight lateral pectination, with 16–23 (mean 19.5) lamellae underneath the fourth toe; (11) dorsal scales weakly carinated, flat and imbricate; (12) dorsal colour pattern consists of three longitudinal pale lines or rows of whitish, elongated ocelli on each side (six longitudinal dorsal lines in total), with obvious black reticulation between the two outer ones and no or little reticulation between the inner ones on the middle of the dorsum; (13) the dorsal and ventral scales of the nape and body show yellowish colouration in both males and females during the spring, which fades later during the summer; (14) juveniles have blue colouration of the tail, and sub-adult females sometimes have a reddish ventral tail colour.

Differential diagnosis. Acanthodactylus margaritae sp. nov. is a typical member of the pardalis speciesgroup, differing from the other geographically-close members of the species-group by the following characters:

Acanthodactylus margaritae sp. nov. differs from A. busacki in having weakly carinated, irregular and imbricate dorsal scales (vs. small, pointed or granular, and smooth in A. busacki ; Fig. 4 ).

Acanthodactylus margaritae sp. nov. further differs from A. busacki in its colour pattern ( Figs. 4–8 ): it has three pale longitudinal lines or series of ocelli on each side of the body, six lines in total (vs. two on each side, four in total in A. busacki ). It also exhibits a moderate sexual dimorphism (stronger in A. busacki ) and less marked ontogenic changes ( Figs. 5–8 ). Juveniles, females and males of A. margaritae sp. nov. all present the typical pattern of three whitish stripes or series of ocelli on each side (six in total). Juvenile, females and sub-adult males of A. busacki have two whitish stripes or series of ocelli on each side but these pale lines disappear or become indistinct in many adult males of A. busacki (they remain obvious in adult males of A. margaritae sp. nov.).

The colour pattern of adult males of the two species is thus usually quite different. Adult males of A. margaritae sp. nov. still exhibit three whitish stripes or series of ocelli on each side of the body with weak or no dark reticulation between the inner ones on the middle of the dorsum. In adult males of A. busacki the two whitish stripes or series of ocelli tend to disappear into a pattern of strong dark reticulation that extends to the middle of the back between the two inner pale stripes. Adult males of A. margaritae sp. nov. have a yellowish colour over the anterior dorsal and ventral areas, in A. busacki males acquire a reddish/pink colouration on the neck and upper dorsum contrasting with yellowish colouration at the lower dorsum and white ventral areas.

Adult females of the two species differ in the number of pale longitudinal lines (see above), in the absence (in A. margaritae sp. nov.) or presence ( A. busacki ) of dark reticulation on the middle of the dorsum, and in the presence (in A. margaritae sp. nov.) or absence (in A. busacki ) of yellowish colouration on the anterior part of the body (see also Table 2).

Less marked and non-diagnostic differences in males also include a higher number of collar scales (10–14 in A. margaritae sp. nov. vs. 8–11 in A. busacki ; P <0.0001), a higher number of granules around the supraoculars (16– 48 in A. margaritae sp. nov. vs. 13–27 in A. busacki ; P <0.0001), and a lower number of femoral pores on the right side (18–24 in A. margaritae sp. nov. vs. 20–26 in A. busacki ; P =0.017) ( Table 2).

Acanthodactylus margaritae sp. nov. differs from the north-eastern Moroccan populations classified as A. maculatus by Bons and Geniez (1996, probably a composite assemblage of several species; Fig. 2 ) in having weakly keeled dorsal scales (vs. flat dorsal scales in A. cf. maculatus ). It further differs in having small and pointed upper temporals and large and smooth lower temporals (vs. granular and flat upper temporals that gradually increase in size in A. cf. maculatus ); by having 10–14 collar scales (vs. 8–11 in A. cf. maculatus ); a higher number of granules around the supraoculars (16–48 vs. 14–21, respectively); and by the absence of a small upper labial scale beneath the subocular (at time present in A. cf. maculatus ). In addition, A. margaritae sp. nov. is slenderer than A. cf. maculatus which is more robust and stubby with a shorter tail, especially females.

Description of the holotype. Habitus robust ( Fig. 6 ). Total length 196 mm (SVL 65.1 mm; un-regenerated tail 130.9 mm). The head presents a well-defined lanceolate concavity from the frontal to the supranasal scales. Snout is pointed, but not very narrow. Rostral shield is not prominent, followed by paired supranasals, their suture very short. Frotonasal is hexagonal and slightly broader than long. Prefrontals are longer than broad; the length of the suture is almost as long as their width. Frontal is narrow and long, broader anteriorly than posteriorly; its length is almost its distance from the tip of the snout. Frontoparietals suture is almost half the length of the frontal, and almost the same length at their posterior margins with the parietals. Parietals are rather broader than longer. Interparietal is relatively large with a diamond shape and a clear parietal foramen; its length equals to its width. Occipital scale is absent. Three supraoculars, the first supraocular is broken into two fragments, the second and third supraoculars intact; six supraciliaries on each side, the first is the longest; 48/44 (left/right) supraciliary granules arranged in two continuous rows contacting the inner border of supraciliaries on each side. Nostrils situated at the cross-point of three scales, bordered dorsally by the supranasal, posteriorly by a single postnasal, and inferiorly by the first upper labial, which is broader above than below. Two loreal scales, the anterior one smaller, the posterior longer and in contact with the anterior first supraciliaries and subocular. Two suboculars with a sharp keel close to their upper margin, the anterior smaller, the posterior longer and wedged between the fourth and fifth upper labials, not contacting the lip. Scales along the upper margin of the suboculars are long and thin, followed by the postocular scales. Upper postocular in contact with the anterior supratemporal, separated from the posterior supraciliary and the supraoculars by granules. Scales in centre of lower eyelid small, round and granular. Seven upper labials on each side, four anterior to the subocular; the fourth upper labial is the longest, followed by the fifth. Two keeled supratemporals, the anterior longer than the posterior. Upper temporals small, pointed and granular, progressively larger and smoother towards the upper labials. A small tympanic scale is present. Anterior margin of the ear opening with six denticulations on each side, the middle four larger and subtriangular. Six lower labials on either side. Five pairs of submaxillaries, the three anterior from each side in contact in the middle. There are 33 gular scales in a straight line between the symphysis of the submaxillaries and the median collar plate, slightly enlarged and imbricate towards the collar; gular fold absent. Collar curved, composed of 11 scales.

Dorsal scales are small and pointed at the nape, slightly larger and weakly keeled between the limbs, becoming larger and flat with a keel on the tail; 55 rows of dorsal scales at midbody. Scales on the flanks are small, almost granular, pointed or slightly keeled, becoming larger and flat ventrally. Ventral scales arranged in 12 longitudinal rows and 33 transverse rows, arranged anteriorly in oblique transverse rows. Three enlarged preanal plates in a transversal row between the anterior cloacal margin and the gap between the two series of femoral pores. Two continuous rows of 21/23 femoral pores, the two series are in contact anteriorly and extending close to the knee.

Dorsal surfaces of the limbs covered by medium sized, imbricate, keeled scales; anterior surface of the limbs covered by larger, unkeeled, imbricate scales; posterior covered with smaller granular scales. The right forelimb is amputated just before the fingers. The ventral side of the forelimbs is covered with small, smooth scales; ventral surface of hind limbs covered with large flat scales. Three longitudinal rows of scales on the toes, except the first which has only two; pectination along the toes is weak; 21 smooth sub-digital lamellae under the fourth toe.

Upper caudal scales are rectangular, larger than the posterior dorsals, flat and keeled; small scales are situated in a longitudinal straight line at the base of the tail on the vertebral row; ventral scales large and smooth.

Background colouration in alcohol mainly brown. Pileus brown, head becoming brighter-whitish from the upper and lower labials ventrally, white inframaxillars. Dorsum brown with three lines of white ocelli extending from the nape to the tail; the central lines close to the centre of the dorsum start from the mid parietals and extend to the base of the tail. The middle lines start from the posterior supratemporals and continue to the sides of the tail. The outer lines are made of roundish ocelli and extend from the temporals to the hind-limbs. A black reticulation is present between the outer and middle lines, but is much reduced between the two inner lines. Fore and hind limbs with dark reticulation and white spots on a brown background. The entire underside of the head, body, limbs and tail is white.

Variation. The paratypes do not differ substantially from the holotype in the meristic or discrete characters, varying slightly in size related measurements (Table 3). Paratype MCCI-R.560 has a partially broken tail at a third of its length, and paratypes MCCI-R.561 and BEV.9440 both have broken tails, but, in the former, the severed tail is preserved intact together with the specimens ( Fig. 7 ). The number of femoral pores is lower in the two female paratypes, MCCI-R.562 and BEV.9440, for which the femoral rows are also not in contact.

Colour and pattern of the adults of both sexes are similar to that of the holotype (based on the photographic material of individuals in the wild). Head dorsally brown with dark brown or black spots. Laterally the upper and lower labials are brighter with dark spots, and the gulars are whitish. The dorsum has a grey/brown background with three longitudinal whitish stripes (in juveniles) or series of ocelli (sub-adults and adults) on each side, starting from the back of the head. An additional whitish stripe is at the border between the dorsals and ventrals. A black reticulation is present among the stripes, which fades closer to the head, or present at lesser amount at midbody between the two central stripes. Adult males and females (prominent in males, not seen in alcohol) exhibit lateral yellow colouration from head to tail on the dorsum and ventrals during the spring; this yellowish colouration fades during the summer. Between the three dorsal stripes on each side, the two central stripes meet at the base of the tail, whereas the two lateral stripes continue along the tail (more obvious in juveniles). The tail is dorsally brown with transverse, continuous or discontinuous black bands laterally and between the two whitish stripes. The limbs have an irregular black and brownish background with whitish spots; this pattern is less obvious on the forelimbs. The ventral colour is off-white. Juveniles exhibit a more prominent contrast of colours on the dorsum and limbs. Juveniles have a blackish ground colour with four shining creamy longitudinal stripes on the dorsum and a row of ocelli of the same colour on each flank; the two median dorsal light stripes come together at the base of the tail while the blackish ground colour continues until the first third part of the tail; the tail is bluish to shining blue ( Fig. 8 ).

Distribution. Acanthodactylus margaritae sp. nov. is endemic to Morocco ( Fig. 1 ), from around 10 km north of Tamri in the north to Tiznit surroundings in the south (southernmost known locality: 3 km north-east of Sidi Boulfdail; PGe.151 & 152), and along the Souss valley to the east, as far as 25 km east of Taroudant (present study; PGe.150), but probably as far as Aoulouz ( Salvador 1982; Bons & Geniez 1996). Its range is limited by the High Atlas and Anti-Atlas Mountains to the north, east and south, and is entirely included in the arid and semi-arid climates with warm or temperate winters ( Bons & Geniez 1996).

Natural history. Acanthodactylus margaritae sp. nov. is a ground-dwelling, diurnal, oviparous, medium-sized lizard, relatively large and stout-bodied. It mostly inhabits stony plains with fine grained soils, stable sands and fixed dunes, or hard clay grounds with scarce low vegetation but also, especially in the Souss valley, open argan tree forests. It is often sympatric with Acanthodactylus aureus in the coastal area, though the latter species prefers softer, looser sands.

Figures

FIGURE 1. Localities of the material examined in this study for Acanthodactylus margaritae sp. nov. (green symbols) and A. busacki (orange symbols), with type localities (star), samples used for the genetic analyses (circle), voucher specimens (square), and photographic material (triangle). Numbers correspond to samples listed in Table 1. Taxon names correspond to changes proposed in this paper.

FIGURE 2. Bayesian inference phylogenetic tree of the pardalis species-group reconstructed from 2405 bp of mitochondrial (12 S, cytb) and nuclear (MC 1 R, ACM 4, c-mos) gene fragments. Bootstrap and posterior probabilities values are presented near the nodes (ML / BI; values ± 70 % and ± 0.95, respectively). Taxon names correspond to changes proposed in this paper.

FIGURE 3. Unrooted networks of the phased nuclear markers (MC 1 R, ACM 4, c-mos). Circle size is proportional to the number of alleles, with colours corresponding to species in Figs. 1 & 2. Codes correlate to the two alleles (i. e., a and b) of specimens listed in Table 1.

FIGURE 4. Comparison of dorsal scales of adult males. A – B) Acanthodactylus margaritae sp. nov. (BEV. 5504); C – D) A. busacki (BEV. 11435). Photos by Karin Tamar.

FIGURE 5. Comparison of dorsal colour patterns. A) Acanthodactylus busacki, holotype, adult male (BMNH 1970.250), photo by Patrick Campbell; B) A. margaritae sp. nov., holotype, adult male (MNHN-RA- 2016.0105), photo by Pierre-André Crochet; C) A. busacki, adult female (PGe. 154), photo by Michel Geniez; D) A. margaritae sp. nov., adult female (PGe. 1143), photo by Alexandre Cluchier; E) A. busacki, adult male (PGe. 1167), photo by Gabriel Martínez & Raúl León; F) A. margaritae sp. nov., adult male (PGe. 1170), photo by Barny Barnestein; G) A. busacki, adult male (BEV. 10829), photo by Pierre-André Crochet; H) A. margaritae sp. nov., adult male (PGe. 1176), photo by Jean-Michel Bompar.

FIGURE 6. Holotype of Acanthodactylus margaritae sp. nov. MNHN-RA- 2016.0105 (former BEV. 9439), adult male. A) Habitus, dorsal and ventral views; B) Head, dorsal and ventral views; C) Lateral head view. Scale bars = 5 mm. Photos by Oz Rittner.

FIGURE 7. Four paratypes of Acanthodactylus margaritae sp. nov. A – B) BEV. 9440, adult female; C – D) MCCI-R. 560, adult male; E – F) MCCI-R. 561, adult male; G – H) MCCI-R. 562, sub-adult female. Scale bars = 5 mm. Photos by Oz Rittner and Pierre-André Crochet.

FIGURE 8. Live specimens of Acanthodactylus margaritae sp. nov. and natural habitats. A) juvenile (PGe. 150), photo by Philippe Geniez; B) sub-adult female (PGe. 1147), photo by Sébastien Durand; C) adult female (PGe. 1174), photo by Hugo Cayuela; D) adult male (PGe. 1173), photo by Raul León; E – F) Oued Massa, Agadir-Tiznit, Morocco, photos by José C. Brito.