Anolis nemonteae, Ayala-Varela & Valverde & Poe & Narváez & Yánez-Muñoz & Torres-Carvajal, 2021

Ayala-Varela, Fernando, Valverde, Sebastián, Poe, Steven, Narváez, Andrea E., Yánez-Muñoz, Mario H. & Torres-Carvajal, Omar, 2021, A new giant anole (Squamata: Iguanidae: Dactyloinae) from southwestern Ecuador, Zootaxa 4991 (2), pp. 295-317 : 298-311

Anolis nemonteae sp. nov.

( Figs 1 , 2 , 3 , 4 , 5 , 6 )

Proposed standard English name: Star anoles

Proposed standard Spanish name: Anolis de las estrellas

Holotype. QCAZ 14595 ( Figs 1 , 2 , 3 ), adult female, Ecuador, El Oro province, Buenaventura Reserve , 3.654 S, 79.777 W, WGS 84, 417 m, 30 January 2016, collected by Andrea Narváez, Sebastián Valverde, Keyko Cruz, and David Reyes.

Paratypes (N=12, Figs 3 , 4 ). ECUADOR: El Oro: QCAZ 14317 (adult female), 14318 (juvenile female), 14431 (juvenile female), 14432 (adult female), 13.2 km SW Piñas on highway, 3.662 S, 79.760 W, 754 m, 11 January 2016, collected by Fernando Ayala, Steven Poe, and Chris Anderson ; QCAZ 14596 (adult male), same collection data as holotype ; QCAZ 14597 (juvenile male), Buenaventura Reserve , 3.650 S, 79.780 W, 372 m ; QCAZ 14660 (female hatchling), Buenaventura Reserve , 3.653 S, 79.766 W, 578 m, 30 January 2016 ; DHMECN 4132 (juvenile male), Buenaventura Reserve , 3.645 S, 79.763 W, 800 m, 7 February 2006, collected by Mery Juiña ; DHMECN 7687 (adult male), same collection data as DHMECN 4132, 18 January 2010, collected by Marco Reyes-Puig, and Michael Harvey ; DHMECN 11543 (juvenile male), Buenaventura Reserve , 3.667 S, 79.766 W, 1,000 m, 31 December 2014, collected by Juan Carlos Sánchez, Karem López, Luis Oyagata, and Paúl Guerrero ; JMG 0484 (adult male), 0485 (adult female), Buenaventura Lodge , 3.653 S, 79.768 W, 520 m, 6 January 2017, collected by Paulina Romero.

Diagnosis. The new species belongs to the Megaloa clade of the latifrons series of Dactyloa ( Castañeda & de Queiroz 2013; Prates et al. 2020) based on the phylogenetic tree presented in this study. Anolis nemonteae sp. nov. differs from most species of the punctatus, heterodermus, and nasofrontalis series ( Castañeda & de Queiroz 2013; Prates et al. 2020) in having relatively smaller head scales; from the roquet series ( Castañeda & de Queiroz 2013) in possessing supraorbital semicircles separated from each other and the interparietal separated from the supraorbital semicircles; and from the aequatorialis series ( Castañeda & de Queiroz 2013; Prates et al. 2020) in having wider toepads and larger dorsal head scales.

The new species is most similar in external morphology to the other members of the latifrons series ( A. agassizi Stejneger 1900 , A. apollinaris Boulenger 1919 , A. brooksi Barbour 1923 , A. casildae Arosemena, Ibáñez & de Sousa 1991 , A. danieli Williams 1988 , A. fraseri , A. frenatus Cope 1899 , A. ginaelisae Lotzkat, Hertz, Bienentreu & Köhler 2013 , A. ibanezi Poe, Latella, Ryan & Schaad 2009b , A. insignis Cope 1871 , A. kathydayae Poe & Ryan 2017 , A. kunayalae , A. latifrons Berthold 1846 , A. limon Velasco & Hurtado-Gómez 2014 , A. maculigula Williams 1984a , A. maia Batista, Vesely, Mebert, Lotzkat & Köhler 2015 , A. microtus Cope 1871 , A. mirus Williams 1963 , A. parilis , A. princeps Boulenger 1902 , A. propinquus Williams 1984b , A. purpurescens Cope 1899 , A. savagei Poe & Ryan 2017 , and A. squamulatus Peters 1863 ). Anolis nemonteae can readily be distinguished from A. agassizi , A. apollinaris , A. casildae , A. frenatus , A. ginaelisae , A. ibanezi , A. latifrons , A. limon , A. maculigula , A. maia , A. princeps , A. purpurescens , and A. squamulatus by having shorter legs not reaching ear when adpressed against body (legs reaching to ear or beyond when adpressed against body); from A. purpurescens , A. ibanezi , A. maia and A. limon further by having a green-brown dorsal background (green); from A. danieli and A. propinquus by lacking elongated superciliaries (one elongated superciliary); from A. brooksi , A. insignis , A. microtus , A. savagei , and A. kathydayae , all from Costa Rica and Panama, by possessing weakly keeled ventral scales (smooth); from A. ginaelisae ( Panama) by lacking enlarged postcloacal scales in males (present); from A. kunayalae , A. mirus and A. parilis by having a wide toe pad on fourth toe (narrow toe pad), subdigital pad under phalanx III projecting above the proximal end of phalanx IV (subdigital pad continuous or indistinct), 21–23 lamellae under phalanges II and III of fourth toe (11–15 lamellae), and distal phalanx including claw equal or smaller than phalanges II and III combined (longer distal phalanx; see Fig. 1 of Williams 1963).

Anolis nemonteae sp. nov. is most similar morphologically to A. fraseri in having a large body size (SVL> 85 mm), a green-brown dorsal background, reddish brown iris, smooth head scales, weakly keeled ventral scales, and 21–23 (18–24 in A. fraseri ) lamellae under phalanges II and III of fourth toe. The new species can be distinguished from A. fraseri (character states in parentheses) by having a creamish white dewlap skin with black blotches longitudinally arranged along yellow stripes in females (female dewlap orangish yellow anteriorly, without black blotches); bluish white dewlap skin with yellowish white scales and gold apicogorgetal scales in males (creamish white skin with yellow or greenish white scales; Fig. 5 ); dark brown dots on neck laterally and dorsally (neck dots absent, large dark blotches might be present; Figs 3 and 5 ); 7–11, mean = 9.29±1.25 SD scales between second canthals, (6–10, 7.72±1.02, z = 2.737, p = 0.006); 3–4, 3.29±0.49 scales between supraorbital semicircles (2–4, 2.68±0.57, z = -2.281, p = 0.023), 7–10, 8.86±1.07 supralabials counted to a point below center of eye (7–9, 7.69±0.55, z = 2.845, p = 0.004); 21–23, 21.71±0.95 lamellae under phalanges II–III of fourth toe (18–23, 20.32±1.09, z = -2.799, p = 0.005), snout length/SVL, 0.116–0.122, 0.119±0.002 (0.112–0.133, 0.123±0.005, t = 2.664, p = 0.013) interparietal length/SVL, 0.016–0.028, 0.023±0.004 (0.011–0.027, 0.018±0.004, t = -2.750, p = 0.011), humerus length/ SVL, 0.131–0.184, 0.159±0.016 (0.155–0.204, 0.171±0.011, t = 2.380, p = 0.025), foot length/SVL 0.259–0.282, 0.272±0.009 (0.262–0.310, 0.287±0.014, t = 2.627, p = 0.014), and fourth toe length/SVL 0.151–0.177, 0.162±0.009 (0.168–0.203, 0.181±0.010, t = 4.287, p <0.001). Furthermore, Anolis nemonteae sp. nov. differs from A. fraseri in lacking enlarged postcloacals in males (present, sometimes inconspicuous), and genetic distances between these species range between 0.03–0.05 (ND2) and 0.05–0.06 (COI). In addition to the above diagnostic traits, the unique male and female dewlap color patterns of A. nemonteae sp. nov. distinguish it from all other Ecuadorian Anolis of the Megaloa clade ( Fig. 5 ).

Description of the holotype (scores for paratypes in parentheses). Snout to vent length 92.4 mm (88.4−115.2 mm); tail length 191.5 mm (200.6−263.1 mm); head length 23.9 mm (23.6−31.3 mm); head width 14.7 mm (14.8−16.9 mm); head height 11.9 mm (12.1−14.4 mm); snout length 11.3 mm (10.4−13.4 mm); interorbital length 4.8 (4.4−5.8 mm); interparietal length 2.3 mm (1.8−2.9 mm); ear height 2.1 mm (1.7−2.5 mm); femur length 22.6 mm (20.5−27.4 mm); tibia length 18.6 mm (17.1−22.7 mm); foot length 25.6 mm (24.2−29.8 mm); humerus length 17.0 mm (13.5−19.2 mm); ulna length 13.3 mm (11.6−16.0 mm); hand length 14.5 mm (13.7−16.5 mm); fourth toe length 16.4 mm (14.3−19.2 mm); fourth toe width 1.8 mm (1.9−2.6 mm); dewlap length 28.8 mm (29.5−49.9 mm); and dewlap height 9.8 mm (6.3−15.2 mm).

Head scales in supraocular disc and frontal region smooth (smooth or rugose); eleven (7−10) scales between second canthals; seven (6−9) scales bordering the rostral posteriorly; circumnasal separated by one (1−2) scale from rostral; supraorbital semicircles separated by three (3−4) scales; supraocular disc with four (3–4) enlarged scales; supraocular edge continuous; superciliaries in two series: first series without rectangular superciliary anteriorly (sometimes present) followed by gradually smaller scales, and second series with squarish scales; five (6−7) loreal rows;>15 loreal scales; midsnout without parallel scale rows (absent or weakly present); rostral with smooth dorsal edge; frontal region of head with a depression; rostral even with mental (even or slight overlapping); interparietal larger (smaller or larger) than ear opening, separated by three (1−3) scales from semicircles; ear oval with normal edge; transparent scales in lower eyelids absent; preoccipital scale absent; suboculars in contact with supralabials; ten (7−9) supralabials counted up to a point below center of eye; six (5−7) postmentals; no enlarged sublabials in contact with infralabials; mental divided partially; mental extending farther back posteriorly than rostral along edge of mouth (even or rostral extending farther than mental or mental extending farther back posteriorly than rostral); and posterior edge of mental straight (straight or slight concave).

Low nuchal crest formed by continuous series of small conical scales; low middorsal crest formed by continuous series of triangular scales (crest present in adults of both sexes); dorsal scales slightly keeled anteriorly and smooth posteriorly (smooth or keeled anteriorly and keeled or smooth posteriorly); two (absent or two) vertebral rows slightly larger than flank scales; eight (9−11) middorsal scales in a longitudinal segment representing 5% of SVL; flank scales smooth (smooth, rugose or weakly keeled), homogeneous in size, and barely separated by skin; ventral scales smaller than dorsals (ventrals larger than dorsals), slightly keeled, subimbricate, with round posterior edge (round or rectangular), and arranged in diagonal rows; ten (7−9) midventral scales in a longitudinal segment representing 5% of SVL; inconspicuous axillary pocket present (present or absent).

Toepads slightly overlapping distal phalanx in all toes; twenty-one (22−23) lamellae under phalanges II and III of fourth toe; supradigitals with multiple keels; tail crest absent; tail round (round or laterally compressed), with a single row of middorsal scales; insolitus tail ( Poe 2004) absent; enlarged postcloacal scales absent (in males and females); hindlimb reaching posterior to ear when adpressed against body.

Nuchal and dorsal folds present; dewlap large, extending posteriorly behind forelimbs (in males and females), with five (4−6) longitudinal rows of four (3–5) elongate scales each, smaller than ventrals, and separated by naked skin.

Inter- and intraspecific variation in morphological characters in Anolis nemonteae is presented in Tables 2 and 3 , respectively.

Color in life. Holotype, adult female QCAZ 14595 ( Fig. 3A, B, C , undisturbed color pattern): dorsum of head, body, limbs and tail pale yellowish green; dorsum of body with three broad, dark brown transverse bands extending onto flanks; dorsal surfaces of limbs and tail with dark brown transverse bands; palpebral scales yellowish green; flanks of neck and body with dark brown spots; ventral aspect of head, body, limbs, and tail cream; iris pale reddish brown; throat lining black; tongue yellow; edge of mouth including jaw hinges white; dewlap skin cream with black blotches, mostly arranged more or less longitudinally along yellow stripes ( Fig. 5B ); scales of dewlap yellowish white.

mean and standard deviation are given.

When stressed, adult females QCAZ 14594 and JMG0485 ( Fig. 3D ) turned dorsal background of head, body, limbs and tail yellowish brown or dark brown, respectively.

Juvenile female QCAZ 14431 ( Fig. 3E , stressed specimen): general color pattern similar to holotype, but dewlap skin dirty white with broad yellow stripes and elongate black blotches; gorgetals, sternals and marginals yellowish white; ventral aspect of head, body, limbs, and tail grayish cream with brown dots.

Hatchling female QCAZ 14660 ( Fig. 3F , stressed specimen): general color pattern similar to female QCAZ 14594, but dorsum of head, body, limbs and tail pale brown; dorsum of body with four dark brown transverse bands extending onto flanks.

Adult male QCAZ 14596 ( Fig. 3G, H, I , undisturbed color pattern): dorsum of body, limbs, and tail brown; dorsum of head light grayish turquoise with orange and red spots; dorsum of body with four broad, dark brown transverse bands extending onto flanks, of which the two posteriormost merge ventrally; second anteriormost broad band bordered anteriorly by yellowish cream line; dorsum of limbs and tail with dark brown transverse bands; palpebral scales yellow; flanks of neck and body with dark brown spots; ventral aspect of head, body, limbs, and tail cream; iris reddish brown; throat lining black; tongue yellow; edge of mouth including jaw hinges white; dewlap skin solid bluish white with yellowish white scales and golden apicogorgetals ( Fig. 5A ). When stressed, adult male JMG 0484 ( Fig. 3J, K ) turned background of body, limbs, and tail light brown.

Color in preservative. In preservative, the holotype (QCAZ 14595) has a light brown background ( Figs 1 , 2 ); otherwise, the color patterns in life (see above) and preservative are similar. Adult male QCAZ 14596 ( Fig. 4 A, B , left side): dorsum of body, limbs, and tail brown; dorsum of body with four dark brown transverse broad bands extending onto flanks; dorsum of limbs and tail with dark brown transverse bands; flanks of neck and body with dark brown spots; ventral aspect of head, body, and limbs grayish cream; tail dark brown with cream base; dewlap skin solid white with cream scales.

Adult males JMG 0484 and DHMECN 7687 ( Fig. 4 A, B , center and right side): general color pattern similar to male QCAZ 14596, but vertebral region of dorsum with dark brown spots; dorsum of DHMECN 7687 with three brown transverse bands of which the second one is bordered anteriorly by a cream stripe, which is discontinuous medially, where each half projects anteriorly.

Adult female JMG 0485 ( Fig. 4 C, D , center): dorsum of head, body, limbs and tail brown; dorsum of body with three broad, dark brown transverse bands extending onto flanks; vertebral region of dorsum with dark brown spots; dorsum of limbs and tail with dark brown transverse bands; flanks of neck and body with dark brown spots; ventral aspect of head, body, limbs, and tail dirty cream; dewlap skin creamish white with black blotches; scales of dewlap creamish white.

Adult female QCAZ 14432 ( Fig. 4 C, D , right side) differs from JMG 0485 in having faint dorsal transverse bands and small dark brown spots on limbs ventrally. Female hatchling QCAZ 14660 ( Fig. 4 C, D , left side) differs in having four dark brown transverse bands (discontinuous medially) on ventral aspect of head and dark brown transverse bands ventrally on limbs.

Hemipenis. Partially everted hemipenis small (7.3 mm total length, 2.9 mm truncus length) and slightly bilobate; sulcus spermaticus unforked, bordered by well-developed lips and opening into a single, smooth apical area; lobes with small calyces on asulcate side; fleshy projection on lobular crotch (crotch flap) on asulcate surface; truncus with transverse and lateral folds ( Fig. 6 ).

Distribution and natural history. Anolis nemonteae occurs on the Pacific slopes of the Andes in southern Ecuador, El Oro province, between 372−1,000 m ( Fig. 7 ). This species occurs in the Evergreen Foothills Montane Forest of Catamayo-Alamor (Ministerio del Ambiente del Ecuador 2013). Specimens of Anolis nemonteae were collected mainly in secondary forest and along the edge of roads ( Fig. 8 ). All individuals were found at night between 20:00 and 01:00 h sleeping horizontally on branches of trees, or leaves of bananas or Panama hat plants, 2.5–6.9 m above ground. A male and a female (JMG 0484, 0485) were found sleeping on banana leaves 10 m away from each other, 2.5 m above the ground. Anolis nemonteae occurs in sympatry with A. binotatus Peters 1863 and A. fasciatus at the type locality ( Yánez-Muñoz et al. 2013, Garzón et al. 2019).

A captive female ( QCAZ 14594 [tissue sample], SVL = 93.21 mm) that was subsequently released laid one egg (22.3 x 14.4 mm) on 30 January 2016. The egg was incubated in perlite at 19°C and 85% of relative humidity. After an incubation period of 129 days, a female ( Fig. 3F ; QCAZ 14660 , SVL = 32.9 mm, weight = 2.3 g) hatched .

Conservation. The known distribution area of Anolis nemonteae has suffered from dramatic deforestation ( Tapia-Armijos et al. 2015). However, most individuals of A. nemonteae were collected within the Buenaventura Reserve, which suggests that at least some of its populations are well protected. Because of the small known distribution ( Fig. 7 ) and lack of additional data, we suggest assigning A. nemonteae to the Data Deficient category according to IUCN (2012) guidelines.

Etymology. The specific epithet nemonteae is a noun in the genitive case and is a patronym for Nemonte Nenquimo, indigenous activist who led a successful campaign and legal action that protected 500,000 acres of Amazonian rainforest and Waorani territory from oil extraction in Ecuador. Nemonte means ‘many stars’ in Wao Tereo language. Nemonte Nenquimo’s work has been recognized worldwide. In 2020, she was awarded the prestigious Goldman Prize and was listed among the 100 most influential people of the year by the Time Magazine. Here we honor Nemonte Nenquimo for her braveness and determination to protect natural forests and their inhabitants.

Phylogenetic relationships. Data partitions and models of evolution are presented in Table 4 . Both ML and Bayesian analyses positioned Anolis nemonteae sp. nov. within a clade highly congruent with the Megaloa clade of Castañeda & de Queiroz (2013) with maximum support ( Fig. 9 ). The difference to the Megaloa clade as originally defined is that Anolis ibanezi , A. kunayalae , and A. parilis were also included ( Fig. 9 ). As expected, A. ginaelisae and A. maia , both described more recently, were also included in this clade ( Lotzkat et al. 2013, Batista et al. 2015). Both ML and Bayesian tree topologies for the Megaloa clade are identical, except for the sister species of A. maculigula ( A. casildae and A. apollinaris , respectively). The sister species of A. nemonteae sp. nov. is A. fraseri (PP = 0.98, BS = 65), and together they form a clade sister to A. parilis (PP = 1, BS = 84).

Interspecific genetic distances among sampled species of the Megaloa clade range from 0.02 ( A. fraseri / A. parilis , A. latifrons / A. princeps ) to 0.23 ( A. latifrons / A. microtus , A. microtus / A. princeps ) for ND2 and from 0.02 ( A. latifrons / A. princeps ) to 0.19 ( A. kathydayae / A. fraseri , A. maculigula / A. nemonteae , A. parilis / A. maculigula ) for COI. Genetic distances between Anolis nemonteae and A. fraseri are 0.03–0.05 (ND2) and 0.05–0.06 (COI).

Dewlap reflectance. The dewlap of Anolis nemonteae reflects light in the visible spectrum in both sexes ( Fig. 10 ). Reflectance starts increasing significantly at around 400 nm in males and 500 nm in females, and it reaches a peak (~50%) at ~ 530 nm. Light is also reflected near the ultraviolet spectrum (~15% at 320 nm) in females.

Remarks. Anolis nemonteae is most similar in morphology to its sister species A. fraseri . Even their hemipenes only seem to differ in relative size (smaller in A. nemonteae ) and in having more pronounced calyces on the asulcate side in A. fraseri ( Fig. 6 ), although the variation of these characters should be analyzed with a larger sample size. However, in addition to the differences presented above, the dewlap of males of the new species is different from both sexes of A. fraseri in lacking reflectance within the ultraviolet spectrum ( Fig. 10 ). The dewlap of both sexes of A. fraseri reflects light with a peak near the ultraviolet spectrum (~10% at 350 nm). Although it has been reported in only a few species of anoles (e.g., Fleishman et al. 2009; Torres-Carvajal et al. 2018), data on reflectance spectroscopy of dewlaps seems to be informative for species delimitation and should be explored in more detail.

Figures

FIGURE 1. Head of the preserved holotype (QCAZ 14595) of Anolis nemonteae sp. nov. in dorsal (top), lateral (middle), and ventral (bottom) views. Photographs by M. Masache. Scale bar = 10 mm.

FIGURE 2. Preserved holotype of Anolis nemonteae sp. nov. (QCAZ 14595) in dorsal (A), lateral (B), and ventral (C) views, with close-ups of dewlap (D), pelvic region (E), and right foot (F). Photographs by M. Masache. Scale bars = 10 mm (A, B, C) and 5 mm (D, E, F).

FIGURE 3. Variation of color in life of Anolis nemonteae sp. nov. Adult female QCAZ 14595 (holotype, A, B, C); adult female JMG 0485 (D); juvenile female QCAZ 14431 (E); hatchling female QCAZ 14660 (F); adult male QCAZ 14596 (G, H, I); adult male JMG 0484 (J, K). Photographs by AEN (A, B, C, G, H, I), FAV (E), P. Pintanel (F) and P. Romero (D, J, K).

FIGURE 4. Variation of color in preservative of Anolis nemonteae sp. nov. Dorsal (A) and ventral (B) views of males (SVL = 98.4 mm, QCAZ 14596 left; SVL = 104.6 mm, JMG 0484 center; SVL = 115.2 mm, DHMECN 7687 right); and dorsal (C) and ventral (D) views of females (SVL = 35.5 mm, QCAZ 14660 left; SVL = 88.4 mm, JMG 0485 center; SVL = 101.5 mm, QCAZ 14432 right). Photographs by M. Masache. Scale bars = 10 mm.

FIGURE 5. Dewlaps of males and females in five species of the Megaloa clade from Ecuador. Anolis nemonteae sp. nov. adult male (QCAZ 14596, A) and adult female (QCAZ 14595, B); A. fraseri adult male (QCAZ 6862, C) and adult female (QCAZ 11864, D); A. parilis adult male (QCAZ 15047, E) and adult female (QCAZ 15052, F); A. purpurescens adult male (QCAZ 4734, G) and adult female (QCAZ 10557, H); A. princeps adult male (QCAZ 16895, I) and adult female (QCAZ 6892, J). Photographs by AEN (A, B), FAV (C, J), D. Quirola (D, E, F), OTC (G, H), and D. Núñez (I).

FIGURE 6. Hemipenes of Anolis nemonteae sp. nov. (DHMECN 7687, SVL = 107.7 mm, left column) and A. fraseri (QCAZ 10212, SVL = 111.3 mm, right column) in sulcate (top), asulcate (middle) and lateral (bottom) views.Abbreviations: Ca = calyces, CF = crotch flap, SS = sulcus spermaticus. Photographs by MYM. Scale bars = 5 mm.

FIGURE 7. Distribution of Anolis nemonteae sp. nov. (red circles) and A. fraseri (blue circles) in Ecuador. The approximate location of the Jubones river basin is marked with a red ellipse.

FIGURE 8. Entrance to Buenaventura Reserve, type locality of Anolis nemonteae sp. nov., showing its general habitat. Photograph by AEN.

FIGURE 9. Phylogeny of the clade Dactyloa, with a close-up of the latifrons series as defined by Castañeda & de Queiroz (2013) and Prates et al. (2020). Maximum clade credibility tree obtained from a Bayesian analysis of 125 taxa and 3,221 characters. Numbers above branches are Bayesian posterior probability (PP) values and those below branches are ML bootstrap support (BS) values. GenBank accession numbers along with locality data are presented in Table 1 for newly sequenced specimens.

FIGURE 10. Reflectance of the gular sac in males and females of Anolis nemonteae sp. nov. and A. fraseri. Measured regions are gular sac base ‘DB’, center ‘DM’, and edge ‘DE’, as well as regions close to the head ‘DH’ and the abdomen ‘DA’. Photo- graphs by AEN (male and female of A. nemonteae sp. nov.), D. Quirola (female of A. fraseri) and FAV (male of A. fraseri).