Anolis limon, Velasco, Julián A. & Hurtado-Gómez, Juan Pablo, 2014

Velasco, Julián A. & Hurtado-Gómez, Juan Pablo, 2014, A new green anole lizard of the " Dactyloa " clade (Squamata: Dactyloidae) from the Magdalena river valley of Colombia, Zootaxa 3785 (2), pp. 201-216 : 203-212

Anolis limon sp. nov.

( Figure 1 and 2 )

Holotype. MHUA-R 11760; adult male, from department of Antioquia, Gómez Plata municipality, Vereda La Clara, Hacienda Vegas de la Clara; 6°34’53”N, 75°11’43’’W (1093 m) collected by Wilmar Munera on April 22, 2008 ( Figure 1 , 2 and 3 ).

Paratypes (all from Colombia). MHUA-R 10053, 11267 collected in department of Antioquia, Yolombo municipality, Normandia, 6°44'6''N, 75°4'51''W (935 m); MHUA-R 10939 department of Antioquia, Amalfi municipality, vereda San Ignacio, 6°54'43''N, 75°4'42''W (1000 m); MHUA-R 11020 collected in department of Caldas, Norcasia municipality, vereda El Tigre, 5°33'32.7''N, 74°52'5,6''W (520 m); MHUA-R 11248 collected in department of Antioquia, Anor municipality, vereda El Retiro 6°48'46.66''N, 75°3'34,34''W (1538 m).

Diagnosis. An Anolis of the “ Dactyloa ” clade ( Savage et al. 1989; Castañeda & de Queiroz 2011, 2013) and the latifrons series (Etheridge 1959; Williams 1976a) according to the following combination of osteological characters: eight or less septate caudal vertebrae, lack of transverse processes on most or all of the autotomic caudal vertebra and having at least four parasternal chevrons attached to the dorsal ribs.

Anolis limon differs from most species of the punctatus and tigrinus groups ( Williams 1992) by having relatively smaller head scales; from the laevis species group ( Williams 1979) by lacking a soft proboscis ; from the roquet species group (Williams 1976b) by possessing supraorbital semicircles separated from each other, the interparietal separated from the supraorbital semicircles, and a straight posterior border of the mental ( Poe 2004); and from the latifrons clade (Castañeda & de Quieroz 2011, 2013) by having a snout-vent length in adults less than 100 mm ( Savage 2002).

Anolis limon shares intermediate adult body size (65–95 mm SVL), smooth ventral scales, and mostly green dorsal coloration with A. chocorum and A. ibanezi , (see Poe et al. 2009a), but differs of these both species in dewlap and color pattern ( Figure 2 ). Anolis limon is distinguished from A. chocorum and A. ibanezi by its uniform light tan or yellow near the throat and tan in the distal portion with rows of green scales in males and color pattern. The dewlap in A. chocorum is orange and white anteriorly with rows of white scales. The dewlap in A. ibanezi is green and white anteriorly orange with rows of green scales ( Poe et al. 2009). The color pattern in A. limon males is green with wide black bands on the flanks of males (males of A. chocorum exhibit rows of ocelli and males of A. ibanezi exhibit thin lines). In females of A. limon there is diffuse dark green spots on the flanks (there are rows of ocelli in females of A. chocorum and thin lines in females of A. ibanezi ; however, we do not known whether these spots would be homologous with the ocelli present in A. chocorum ) ( Figure 1 and 2 ). Furthermore, A. limon exhibits fewer scales across the snout than A. chocorum (mean = 9.7, range = 8–11 in A. limon ; mean = 12, range = 10–15 in A. chocorum ) ( Figure 4 ).

Description of external morphology of the holotype (paratype variation in parentheses) ( Figure 3 and 4 ): Morphological dimensions are shown in Table 1 . Dorsal head scales smooth; weak frontal depression; rostral canthus distinct; seven postrostrals (5–7); two sublabial scales slightly enlarged, (one enlarged sublabial scales on each side); seven postmentals (6–7); interparietal separated from supraorbital semicircles by four scales (2–4); three scales between supraorbital semicircles (2–3); nine supralabials to center of eye (8–9); eight infralabials to center of eye (7–9); one superciliary scale enlarged followed by granular scales; none scales rows between suboculars and supralabial (1); ten scales across snout between second canthals (8–11); six loreal rows (5–7); circumnasal in contact with supralabial, separated from rostral by one scale (not in contact with supralabial in MHUA-R 11267); rostral slightly overlapping mental; mental broader than rostral, extending posterolaterally beyond rostral; posterior border of mental concave (convex in all paratypes); mental partially divided; scales surrounding the interparietal are smooth; some enlarged scales in supraocular disc, the rest granular. Dorsal scales keeled; two rows of slightly enlarged middorsal scales (0–2); nine dorsal scales counted longitudinally in 5% of SVL (8–11); nine ventral scales counted longitudinally in 5% of SVL (8–12) (see Poe 2004 for a description of this character); ventrals smooth, each scale bordered posteriorly by two scales (i.e., in transverse rows). Anterior part of the arm with unicarinate scales, elbow with multicarinate scales; thigh with unicarinate scales, knee with multicarinate scales; postcloacal greatly scales enlarged (absent in paratypes); scales on dewlap in rows of three scales (3–4); 22 expanded lamellae under third and four phalanges of fourth toe (20–22) (second and third phalanges of Williams et al. 1995); tail with keeled scales and a double middorsal row.

*There was only one male additional to the holotype during this work.

Osteological description (based in MHUA-R 11020). Postcranial skeleton: Interclavicles T-shaped; 24 presacral vertebrae; four lumbar vertebrae; eight caudal vertebrae with transverse processes anterior, gradually lost posteriorly ("alpha" condition in Anolis ; Etheridge 1959); Caudal autotomy septa absent; five postxiphisternal inscriptional ribs, four pairs attached to dorsal ribs and one pair free (5:1); Two sternal ribs and two xiphisternal ribs.

Skull: Supraoccipital cresting continuous across supraoccipital; dorsal surface of skull smooth; parietal crests Y-shaped; anterolateral corners of parietal crests reach posterolateral corners of frontal; parietal casque absent; position of pineal foramen at parietal/frontal suture; supratemporal processes leave supraoccipital exposed above; postfrontal present; prefrontal contacts nasal; frontal sutures contacts only with nasals anteriorly; dorsal processes of jugal terminates on lateral aspect of postorbital; contact between jugal and squamosal absent; posteroventral corner of jugal is anterior to posterior edge of jugal; epipterygoid does not contact parietal; pterygoid teeth absent; lateral edges of vomer smooth; maxilla extends posteriorly to ectopterygoid; quadrate lateral shelf absent; premaxilla overlaps nasals laterally; posterior of skull slopes superiorly; crenulation along lateral edges of parietal absent; parietal roof flat; posteriormost tooth is posterior to anterior inferior alveolar foramen; angular processes of articular large; posterior suture of dentary pronged; posterior border of dentary extending within mandibular fossa; splenial large; ventral aspect of anteromedial process of coronoid projects posteriorly; surangular foramen completely in surangular; coronoid labial process present; posterolateral aspect of coronoid terminates anterior to supraangular foramen; angular absent.

Color in life: Anolis limon is sexually dimorphic in color pattern. The dorsal surface of the body in both sexes is light green. Males have transverse dark green to black bands (five from the neck to the tail base, see Figure 1 ), whereas females have numerous dispersed dark green to bluish small blotches with a few additional small white blotches. The banded/blotched (male/female) pattern continues onto the dorsal surface of limbs and tail. Two aspects of the coloration, observed in the holotype, seem to be related to stress conditions, since they were not present when just caught. The first stress pattern is the brown and yellowish coloration in different parts of the head, and the second is some reticulated brown lines in trunk. The ventral surface of head, body, limbs, and tail is whitish with a diffuse light pattern of scattered bluish and greenish irregular small blotches in both sexes. Eyelids are bright yellow in their anterior and posterior margins, sometimes white at the very margin to the eye. The superior and inferior borders of eye are green like the rest of the body. The iris is light brown to reddish, the pupil is black. In males, the dewlap skin is uniform light tan or yellow near the throat and tan in the distal portion; the border scales are white, and has five transverse lines of light green scales. Females have white scales on the border of the dewlap, while the skin is green fading into yellow with rows of small white scales.

Color in preservative. The color of recently preserved specimens is darker than that of living specimens, but the banded/blotched pattern is conserved. Older specimens also conserve the pattern, but green surfaces turn into purple, and the ventral surfaces become grayish ( Figure 2 and 3 ).

Distribution and ecology. Anolis limon is only known from some localities in the northeastern slope of the Central Andes in Colombia between 1000 and 1800 m of elevation ( Figure 5 ). We found Anolis limon in secondary forest and forest edges, near streams and ponds, mostly sleeping on leaves at night.

Morphometric analysis. The principal component analysis shows a clear separation between females for each species ( Figure 6 ). The first two components explain 79.63% of variance in females ( Table 2 ). Head variables exhibited the highest loadings in the first component (IoD, HW, SL) and limb dimensions (HuL, UL, FL) exhibited the highest loadings in the second component (see Table 2 ). Females of both species show a clear separation in the first component with very few differences in the second ( Figure 5 ).

Phylogenetic relationships. Our search strategy resulted in 576 equally-parsimonious trees with length of 31889 steps and a consistency index of 0.12 and a retention index of 0.49. The 50% majority rule consensus of these trees is shown in Figure 7 (all non-dactyloid species were collapsed in this tree).

Etymology. The specific name limon makes reference to the resemblance of the body color of the females to the green color of the fruits of the lemon tree ( Citrus x lemon).

Our phylogenetic results show that Anolis limon is nested within the " Dactyloa " clade of Anolis ( Figure 7 ). The inclusion of species scored only for morphological characters probably reduces the support values for many nodes ( Huelsenbeck 1991). However, the inclusion of these taxa with a lot of missing data may increase the accuracy of recovered phylogenetic relationships ( Wiens & Tiu 2012). The results of our phylogenetic analysis reveal that although A. limon and A. chocorum are very similar morphologically they are nested in different subclades inside the “ Dactyloa ” clade. Instead, we found that A. limon is the sister taxa to A. ibanezi , although the nodal support is too low (below 50% of bootstrap replicates). However, we only included molecular data for Anolis chocorum and a further study (including molecular data) it is necessary to highlights the phylogenetic relationships of mainland green anoles ( Anolis limon , A. ibanezi and A. chocorum ). The recent phylogenies of dactyloid anoles (see Castañeda & de Queiroz, 2011, 2013) only have included the half of dactyloid taxa described (Castañeda & de Queiroz, 2011) and in some cases, taxa with many missing data, mostly for molecular data (Castañeda & de Quieroz, 2013). We considered that a better taxa sampling combined with a most complete character sampling (especially for molecular data) it is necessary to improve our understanding of the phylogeny of dactyloid anoles.

Our morphometric analyses suggested that the females of Anolis limon and Anolis chocorum differs mainly in head variables (see Table 2 and Figure 5 ). These morphological differences likely are associated to differences in diet and bite force (Herrel et al. 2001a; b), reflecting niche partitioning between species ( Harmon et al. 2005).

The distribution of Anolis limon is restricted to the middle Magdalena region of Colombia ( Figure 5 ). This restricted distribution provide additional support for the hypothesis that Magdalena region is an endemism area (Hernández-Camacho et al. 1992; Morrone 2001). Several species are known to be restricted to this region, like monkeys (e.g, Saguinus leucopus Günther 1877 ), birds (e.g., Capito hypoleucus Salvin 1897 ), frogs (e.g., Agalychnis terranova Rivera, Duarte, Rueda & Daza, 2013 ;, Allobates niputidea Grant, Acosta & Rada 2007 ; Dendrobates truncatus Cope 1861 ), turtles (e.g., Podocnemis lewyana Duméril 1852 ) and other anole species (e.g., A. ibague Williams 1975 ).

The discovery of this new species highlights the need for extensive work with Colombian anoles. Additional research in Colombian herpetological collections supplemented by extensive fieldwork at several sites across the country likely will allow the discovery of new anole taxa. With the description of Anolis limon we have added another species to the Colombian anole fauna for a total of 75 species ( Uetz & Hosek 2013). Despite limited sampling effort dedicated to anoles in Colombia, in comparison with other regions (e.g., Greater Antilles) Colombia has the highest anole diversity of any country ( Uetz & Hosek 2013). The high diversity of Anolis species in Colombia offers an excellent opportunity for addressing evolutionary and ecological questions (see Molina- Zuluaga & Gutiérrez-Cárdenas 2007; Velasco & Herrel 2007; Calderón-Espinosa & Barragán-Forero 2011; Calderón-Espinosa et al. 2013; Moreno-Arias & Urbina-Cardona 2013). We encourage herpetologists to conduct biological studies focused on Colombian anole species. Such studies will contribute to a greater understanding of the ecological and evolutionary causes of the high diversity in Colombia.

Figures

FIGURE 1. Anolis limon sp. nov. Top: male holotype (MHUA-R 11760); Bottom: female paratype (MHUA-R 10939).

FIGURE 2. Dewlap of Anolis limon sp. nov. and closest putative relatives. Top: Anolis limon sp. nov. (Photo: JPHG). Middle: Anolis chocorum (Photo: Omar Torres-Carvajal; QCAZ 4734). Bottom: Anolis ibanezi (Photo: Steven Poe).

FIGURE 3. Holotype of Anolis limon sp. nov. (MHUA-R 11760, adult male). A) lateral, B) dorsal, and C) ventral view of head; D) detail of dorsal scales at mid-dorsum of body, arrow indicate the middorsal scales; E) detail of ventral scales at middorsum of body; F) detail of flank scales at mid-dorsum of body; G) ventral view of cloacal region showing enlarged postcloacal scales.

FIGURE 4. Comparisons of head scales between Anolis limon sp. nov. and Anolis chocorum A) lateral, B) ventral, and C) dorsal view of head of A. limon sp. nov. (paratype, MHUA-R 11270); D) lateral, E) ventral, and F) dorsal view of head of A. chocorum (MHUA-R 10075; Colombia, Chocó, Nuqui, Estación Biológica El Amargal).

FIGURE 5. Distribution map for Anolis limon sp. nov. and closest putative relatives. Circles in white for A. chocorum correspond to specimens and observations checked by one of us (JAV). The locality information for the rest of occurrence records were taken from original descriptions (Williams & Duellman 1967, Poe et al. 2009) and recent literature (Lotzkat et al. 2013).

FIGURE 6. Dispersion of individuals (females) of Anolis limon sp. nov. (green) and Anolis chocorum (red) of the first (PC 1) and second (PC 2) components of PCA for 15 morphological traits.

FIGURE 7. A 50 % majority rule consensus showing phylogenetic relationships for dactyloid anoles including Anolis limon sp. nov. Values in the nodes correspond to support values above 50 % from 500 bootstrap replicates.

Tables

TABLE 1. Ranges of morphological measurements of the holotype, males and females of Anolis limon sp. nov. and Anolis chocorum. For abbreviations see materials and methods. Dimensions are given in millimeters.

	Anolis limon			Anolis chocorum
Character	Holotype	Paratype*	Females (n = 4)	Males (n = 7)	Females (n = 6)
SVL	78.60	74.50	71.21–81.78	71.92–80.64	58.61–74.27(n=8)
TL	193.00	182.00	180.97–201.92	179.17–203.55	124.82–202.87(n=7)
HL	20.10	18.70	19.37–21.5	17.56–21.34	17.22–18.89
HW	10.70	10.00	9.37–11.28	8.54–11.63	8.42–9.48
JL	18.20	15.60	16.96–18.53	15.89–18.3	15.06–16.70
IoD	3.40	3.70	3.05–3.39	2.41–2.94	2.23–2.74
AGL	35.90	33.70	34.16–39.56	32.42–38.15	30.01–34.14
InD	2.50	2.40	2.33–2.61	2.11–2.59	2.15–2.60
SL	9.70	9.10	9.26–10.51	8.33–10.65	8.15–9.29
HuL	11.00	10.50	10.00–12.09	10.13–13.27	9.34–12.10
UlL	10.10	9.80	9.22–11.21	9.31–12.16	8.67–11.10
FL	18.60	17.10	17.21–19.76	17.52–20.31	14.76–20.12
TiL	18.20	16.40	17.01–18.48	17.00–19.40	14.96–19.64
FoL	25.80	23.90	23.85–25.44	23.59–25.93	19.8–25.12
4tL	14.90	12.90	13.42–13.90	12.85–15.29	10.78–13.68

TABLE 2. Results of principal component analysis (the first two PC axes) for 15 morphological variables foradult females of Anolis limon sp. nov. and Anolis chocorum.

	PC 1	PC 2
% Variation	60.61%	19.00%
Eigenvalues	0.096	0.003
Loadings Head Length	0.322	0.006
Head Width	0.363	0.075
Jaw Length	0.281	-0.007
Internarinal Distance	0.097	-0.009
Snout Length	0.332	-0.109
Interorbital Distance	0.618	0.049
Snout Vent Length	0.237	0.130
Tail Length	0.135	-0.179
Axila Groin Length	0.249	0.259
Humerus Length	-0.116	0.521
Ulna Length	-0.040	0.470
Femur Length	-0.048	0.470
Tibia Length	-0.017	0.374
Foot Length	0.145	0.094
4th Toe Length	0.089	0.026
Discussion