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Description of the striking ontogenetic colour variation of Anadia


antioquensis Arredondo, 2013 (Squamata: Gymnophthalmidae), with new data
on its morphology, distribution, and mic...

Article  in  Herpetology Notes · August 2020

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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 (Squamata:
Gymnophthalmidae), with new data on its morphology,
distribution, and microhabitat use

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

The cercosaurine lizard genus 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 reptile 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 lizards 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-
R 13646) is 42 mm, while those of the adults are 63 mm
(paratype) differs from the juvenile males by the lack
(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
presented as left/right.
Table 1. Meristic variation of We usecharacters
selected the scale names
in Anadia as in Arredondo
antioquensis. (2013).
When not equal 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 Gymnophthalmus 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 reptiles 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 animals. Biological Journal of the Linnean
Society 40: 125–163.
was found running through the mud on a rural road
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
through color change: mechanisms, adaptive value and
human settlements, and gallery forests. Additionally,
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. Animal 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-
footed lizards. Animal Behaviour 119: 165–172.
et al., 2015). However, considering that these lizards
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): Taxonomy, 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
gymnophthalmid lizards (Squamata, Gymnophthalmidae,
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Northern Andes of Colombia. Amphibia-Reptilia 34: 173–184. 2013. The Reptile Database. 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
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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

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