Herpetology Notes, volume 13: 593-597 (2020) (published online on 05 August 2020)

Description of the striking ontogenetic colour variation of Anadia antioquensis Arredondo, 2013 (: ), with new data on its morphology, distribution, and microhabitat use

Juan D. Vásquez-Restrepo1,* and Diego A. Rivera-Prieto1

The cercosaurine Anadia Gray, 1845 Materials and Methods currently includes 19 recognised species (Uetz et al., We examined a total of six individuals of Anadia 2020) distributed from Costa Rica to southern Ecuador, antioquensis, including the two types and four additional and from western Colombia to eastern Venezuela (Rivas specimens recently deposited in the collection of et al., 2012), with most species having small or disjunct the Museo de Herpetología Universidad de Antioquia distributions. Due to their secretive habits (terrestrial (MHUA-R), Medellín, Colombia. Detailed information and arboreal), these are rare in biological about specimens, including the type series, is listed in collections and many aspects of their biology, ecology, the Appendix. Among the newly available specimens, and systematics remain poorly studied (Oftedal, 1974; Torres-Carvajal et al., 2016; Betancourt et al., 2018). Anadia antioquensis Arredondo, 2013 is endemic to Colombia, occurring at elevations of 1500–1850 m in the Cordillera Central in Antioquia and Caldas Departments (Fig. 1). It is listed as Vulnerable (VU) both in national and global assessments (Castañeda et al., 2015; Arredondo and Bolivar, 2017). The species was originally described based on an adult male (MHUA-R 10537; holotype) and a young female (MHUA-R 11254; paratype) from Antioquia Department (Arredondo, 2013). Since its description, the only new information on this species was the discovery of a southern population in Caldas Department (Castañeda et al., 2015). Here we describe previously unknown colour variation of A. antioquensis, present for the first time photos in life to show the ontogenetic variation in colour from juveniles to adults, and provide new data on scale counts and microhabitat use.

Figure 1. Distribution of Anadia antioquensis in Colombia, 1 Grupo Herpetológico de Antioquia, Instituto de Biología, showing Antioquia Department in the centre and Caldas Facultad de Ciencias Exactas y Naturales, Universidad de Department below it. Yellow circles are records from Antioquia, calle 67 #53-108, Laboratorio 7-121, Medellín, Arredondo (2013) and Castañeda et al. (2015), while white Colombia. circles are new records. The inset shows the position of the * Corresponding author. ������� ��������������������� main map in Colombia. 594 Juan D. Vásquez-Restrepo & Diego A. Rivera-Prieto two are adults (MHUA-R 13397, 13455) and two are Discussion juveniles (MHUA-R 13606, 13646). We identified Our evidence suggests that juveniles of A. antioquensis them based on the list of characters in the original undergo a dramatic ontogenetic change in colouration, description of the species (Arredondo, 2013) and by shifting their bluish-black dorsal colouration to brown directly comparing them with the type specimens. Sex olive and in males apparently losing the yellow and was determined by noting the presence or absence of red from the limbs and acquiring dark blotches on hemipenes. If hemipenes were not everted, sex was the ventral surface. The colouration of adult females determined by subcaudal incision. Colouration was remains unknown at this time, with only a juvenile described from preserved specimens (in 70% ethanol) female known (paratype). Sexual dimorphism in and using in-life photographs. Meristic variation is colouration was previously reported in adults of summarised in Table 1. Field notes associated with A. rhombifera and A. petersi (Oftedal, 1974), and specimens were used to discuss about microhabitat use. although the colour of adult females of A. antioquensis is not known, differences in ventral marks among the Results examined specimens suggest that sexual dichromatism Colouration of Anadia antioquensis was originally described as follows: (1) dorsally a brown background colour with seven longitudinal rows of large black ocelli, each ocellus formed by an anterior and a posterior black blotch with a cream-coloured spot between them; and (2) ventrally clear, with irregular dark spots in adult males, while in juvenile females immaculate (Arredondo, 2013). Four of the newly collected specimens are males, according to the presence of hemipenes and adult colouration. Both juveniles (MHUA-R 13606, 13646) had a dorsal colouration in-life featuring a bluish-black background with clear ocelli, yellow forelimbs, and hind limbs with a deep red colour (Fig. 2A). Ventrally, juvenile males do not have dark blotches, except for a longitudinal line of dark spots near the belly edges, but possess a pale yellow and pale red colouration on limbs and adjacent areas of the pectoral and pelvic girdle. Finally, near the hind limbs there are a few clear spots that become two solid bluish grey lines extending laterally along the tail. In preservative, juveniles had the same colouration pattern, but with less brilliant red and yellow. Colouration of adult males (MHUA-R 13397, 13455) in preservative coincides dorsally and ventrally with the original description. Nevertheless, both individuals kept the lower bluish grey line on tail in life (Fig. 2B, C). Additionally, MHUA-R 13455 still had dark reddish hind limbs, showing that there is an apparent transition Figure 2. Juvenile (A) and adult males (B, C) of Anadia from juvenile to adult colouration. The juvenile female antioquensis. The snout–vent length of the juvenile (MHUA- (paratype) differs from the juvenile males by the lack R 13646) is 42 mm, while those of the adults are 63 mm (MHUA-R 13455) and 86 mm SVL (MHUA-R 13397). The of vivid colours on the limbs and the absence of dark specimen in (B) shows a transitional stage that consists of an spots along the ventral edges. The recently collected olive background, well-formed edges on the ocelli, a yellowish specimens examined also exhibit slight, previously tone in the anterior part of the body, and reddish hind limbs. unknown variation in some meristic characters Photographs by Juan D. Vásquez-Restrepo (A), Carlos M. compared with the type series (Table 1). Marín (B), and Paola Martinez (C). Description of the striking ontogenetic colour variation of Anadia antioquensis 595

Table 1. Meristic variation of selected characters in Anadia antioquensis. When not equal for bilateral characters, counts are presentedTable 1. Meristic as left/right. variation of Weselected use characters the scale in Anadia names antioquensis as in Arredondo. When not equal (2013). for bilateral characters, counts are presented as left/right. We use the scale names as in Arredondo (2013).

MHUA-R 10537 MHUA-R 11254 MHUA-R 13397 MHUA-R 13455 MHUA-R 13606 MHUA R- 13646 (holotype) (paratype) Frontonasal 1 1 1 1 1 1 Prefrontals 2 2 2 2 2 2 Frontal 1 1 1 1 1 1 Frontoparietals 2/3 2 2 2 2 2 Interparietal 1 1 1 1 1 1 Parietals 2 2 2 2 2 2 Postparietals 2 2 2 2 2 2 Nasal Single Single Single Single Single Single Supraoculars 4 4 4 4 4 4 Presuperciliary Present Present Present Present Present Present Suboculars 3 3 4 3 3 3 Frenocular Present Present Present Present Present Present Preocular 1 1 1 1 1 1 Postocular 3 3 3 4 2/3 3 Lower palpebral disk scales 5 3/4 4/5 4/3 5 4/3 Supralabials 10 10/9 10 8 9 8/9 Infralabials 9 8 9 8 6/7 8 Pair of genials 3 (first in middle 3 (first in middle 3 (first two in middle 3 (first in middle 3 (first two in middle 3 (first in middle contact) contact) contact) contact) contact) contact) Dorsals Subhexagonal Subhexagonal Subhexagonal and Subhexagonal and Subhexagonal and Subhexagonal and rectangular rectangular rectangular rectangular Transverse dorsal row by About 2 About 2 About 2 About 2 About 2 About 2 ventrals Transverse rows on dorsum 54/55 55 51 54 51 54 Transverse rows on dorsum 37 35 35 36 37 36 (groin-armpit) Ventrals Quadrangular Quadrangular Quadrangular Quadrangular Quadrangular Quadrangular Transverse rows ventral 24 23 23 22 22 23 Scales around midbody 36 (26 + 10) 36 (26 + 10) 36 (26 + 10) 36 (26 + 10) 36 (26 + 10) 36 (26 + 10) (dorsal + ventral) Scales under 4th finger 15 13 13 13 12/13 13 Scales under 4th toe 21 18 18 17 18 18 Femoral pores 10 10 11 9 10/11 9 Cloacal plates 4 anterior + 3 4 anterior + 3 4 anterior + 3 4 anterior + 3 4 anterior + 3 4 anterior + 3 posterior posterior posterior posterior posterior posterior Dorsolateral fold Absent Absent Absent Absent Absent Absent

in adults is likely. An example of ontogenetic colour in phenomenon, including anti-predatory mechanisms, other gymnophthalmids is the tail of mechanisms to reduce conspecific aggression, indicators speciosus, which becomes darker in adults (Hernández- of sexual maturity, or crypsis associated with habitat Ruz, 2006). Nevertheless, A. antioquensis would be the use (Wilson et al., 2007; Fresnillo et al., 2015, 2016). first known gymnophthalmid with both an ontogenetic Our data leads to several questions about the biology colour change and sexual dimorphism since early stages. and ecology of this rare lizard species. For example, Finally, given that A. antioquensis was described based we wonder why this colour change would apparently on only two individuals, variation in scale counts can be occur only in males and what its effects on predation expected as the sample size increases, but in general the and visual communication may be. It is also interesting scale counts seems to be very homogeneous (Table 1). to determine how this change relates to habitat use, In many organisms there is a phenomenon of colour perhaps linked to a possible differentiation between change during development to adulthood, shifting sexes or maturation stages. from less to more conspicuous colourations or vice Regarding microhabitat use, one of the juvenile males versa (Booth, 1990; Duarte et al., 2017; Murphy et al., (MHUA-R 13606) was encountered near a country 2019). In there are several hypotheses about this house after having been injured by a domestic cat, 596 Juan D. Vásquez-Restrepo & Diego A. Rivera-Prieto and the other (MHUA-R 13646) was found in a coffee Booth, C.L. (1990): Evolutionary significance of ontogenetic plantation. One of the adult males (MHUA-R 13397) colour-change in . Biological Journal of the Linnean was found running through the mud on a rural road Society 40: 125–163. Castañeda, M.R., Arredondo, J.C., Gutiérrez-Cárdenas, P.D.A. after the passage of a backhoe, while the other (MHUA- (2015): Anadia antioquensis Arredondo, 2013. In: Libro rojo R 13455) was found in a creek in pristine forest. It de reptiles de Colombia, p. 70–71. Morales-Betancourt, M.A., therefore appears that this species can tolerate a certain Lasso, C.A., Páez, V.P., Bock, B.C. (Eds), Bogotá, D.C., level of habitat modification and is more of a generalist Colombia, Instituto de Investigación de Recursos Biológicos than previously thought: it is known to inhabiting active Alexander von Humboldt (IAvH), Universidad de Antioquia. agricultural areas, primary and secondary vegetation, Duarte, R.C., Flores, A.A.V., Stevens, M. (2017): Camouflage human settlements, and gallery forests. Additionally, through color change: mechanisms, adaptive value and ecological significance. Philosophical Transactions of the Royal these new records extend the lower elevational Society B: Biological Sciences 372: 20160342. distribution limit of the species by nearly 200 m, from Fresnillo, B., Belliure, J., Cuervo, J.J. (2015): Red coloration in 1500 to 1330 m. juvenile spiny-footed lizards, Acanthodactylus erythrurus, Anadia antioquensis is considered a threatened species reduces adult aggression. Behaviour 102: 59–67. based on the low number of known populations and the Fresnillo, B., Belliure, J., Cuervo, J.J. (2016): Ontogenetic shifts in continuing process of habitat fragmentation (Castañeda risk behaviours are related to body size and coloration in spiny- et al., 2015). However, considering that these lizards footed lizards. Animal Behaviour 119: 165–172. Hernández-Ruz, E.J. (2006): Gymnophthalmus speciosus are secretive ground dwellers with low detectability, (Hallowell 1861) (Squamata, Gymnophthalmidae) en Colombia. their “rarity” may in part be a reflection of sampling Caldasia 28: 79–88. bias (Restrepo et al., 2017). Finally, we consider that Murphy, J.C., Salvi, D., Santos, J.L., Braswell, A.L., Charles, S.P., predation by domestic and feral cats must be considered Borzée, A., Jowers, M.J. (2019): The reduced limbed lizards of as a significant risk factor associated with the habitat the genus Bachia (Reptilia, Squamata, Gymnophthalmidae); degradation and modification. biogeography, cryptic diversity, and morphological convergence in the eastern Caribbean. Organisms, Diversity & Evolution 19: 321–340. Acknowledgements. We thank Museo de Herpetología Oftedal, O.T. (1974): A revision of the genus Anadia (Sauria, Universidad de Antioquia for allowing us to use its biological Teiidae). Arquivos de Zoologia 25: 203–265. collection. We are very grateful to E. Atehortua for giving us Restrepo, A., Velasco, J.A., Daza, J.M. (2017): Extinction risk or information about species localities, and we thank J.M. Daza, C. lack of sampling in a threatened species: Genetic structure and Martinez, and R. Builes for helping us with logistic issues. We environmental suitability of the neotropical frog Pristimantis are grateful to P. Martinez and C.M. Marín for sharing with us penelopus (Anura: Craugastoridae). Papéis Avulsos de Zoologia pictures of in-life adults (from GEN+ and EPM respectively). And 57: 1–15. finally, we thank S.J. Sánchez-Pacheco, J.P. Hurtado, and C.M. Rivas, G.A., Sales-Nunes, P.M., Dixon, J.R., Schargel, W.E., Marín for reviewing earlier drafts of the manuscript. Photographs Caicedo, J.R., Barros, T.R., Camargo, E.G., Barrio-Amorós, C.L. from EPM were taken in “convenio de cooperación N° CT-2017- (2012): , hemipenial morphology, and natural history 001714 Universidad de Antioquia - EPM,” and those from GEN+ of two poorly known species of Anadia (Gymnophthalmidae) from “marco de la formulación del Estudio de Impacto Ambiental from northern South America. Journal of Herpetology 46: 33– para la PCH Argelia. Empresa de Generación y Promoción de 40. Energía de Antioquia – GENMAS S.A. E.S.P. Argelia, Antioquia. Torres-Carvajal, O., Lobos, S.E., Venegas, P.J., Chávez, G., Aguirre- 2018”. Peñafiel, V., Zurita, D., Echevarría, L. (2016): Phylogeny and biogeography of the most diverse clade of South American References gymnophthalmid lizards (Squamata, Gymnophthalmidae, Cercosaurinae). Molecular Phylogenetics and Evolution 99: Arredondo, J.C. (2013): A new species of gymnophthalmid lizard 63–75. of the genus Anadia (Gymnophthalmidae: Cercosaurinae) from Uetz, P., Freed, P., Hošek, J. (2020): Anadia antioquensis Arredondo, Northern Andes of Colombia. Amphibia-Reptilia 34: 173–184. 2013. The . Available at: http://reptile-database. Arredondo, J.C., Bolívar, W. (2017): Anadia antioquensis. The IUCN reptarium.cz. Accessed on 5 July 2020. Red List of Threatened Species 2017: e.T48832571A48832574. Wilson, D., Heinsohn, R., Endler J.A. (2007): The adaptative Accessed on 5 July 2019. significance of ontogenetic colour change in a tropical python. Betancourt, R., Reyes-Puig, C., Lobos, S.E., Yánez-Muñoz, M.H., Biology Letters 3: 40–43. Torres-Carvajal, O. (2018): Sistemática de los saurios Anadia Gray, 1845 (Squamata: Gymnophthalmidae) de Ecuador: límite de especies, distribución geográfica y descripción de una especie nueva. Neotropical Biodiversity 4: 82–101. Description of the striking ontogenetic colour variation of Anadia antioquensis 597

Appendix Voucher numbers and localities of Anadia antioquensis specimens examined. All specimens were collected in Antioquia Department, Colombia. GPS coordinates use the WGS84 datum.

MHUA-R 10537 (holotype).—An adult male from La Cejita, Barbosa Municipality (6.5011°N, 75.1919°W, elevation 1850 m), collected in 2000. MHUA-R 11254 (paratype).—A juvenile female from El Retiro, Anorí Municipality (6.9869°N, 75.1375°W, elevation 1700 m), collected in 2004. MHUA-R 13397.—An adult male from El Zancudo, Argelia Municipality (5.6959°N, 75.1603°W, elevation 1332 m), collected in 2018. MHUA-R 13455—An adult male from El Retiro, Anorí Municipality (6.9856°N, 75.1129°W, elevation 1689 m), collected in 2018. MHUA-R 13606.—A juvenile male from El Hatillo, Barbosa Municipality (6.4171°N, 75.3886°W, elevation 1385 m), collected in 2019. MHUA-R 13646.—A juvenile male from near the Calderas River, San Carlos Municipality (6.1566°N, 75.0790°W, elevation 1567 m), collected in 2019.

Accepted by Hinrich Kaiser