Hyloxalus maculosus (Rivero 1991)

Páez-Vacas, Mónica I., Coloma, Luis A. & Santos, Juan C., 2010, Systematics of the Hyloxalus bocagei complex (Anura: Dendrobatidae), description of two new cryptic species, and recognition of H. maculosus 2711, Zootaxa 2711, pp. 1-75 : 39-44

Hyloxalus maculosus (Rivero 1991)

Colostethus maculosus — Rivero 1991:17–20.— Holotype: “ MCZ-A 99558 an adult male from Puyo , between Turingia and theatre, 950 m, Provincia Pastaza, Ecuador ”. Fig. 2B.

Hyloxalus fuliginosus — Andersson 1945:17.

Colostethus bocagei — Coloma 1995:23 (partim).

Hyloxalus maculosus — Grant et al. 2006:168.

Diagnosis. A species with (1) mean SVL in adult males 22.6 mm (19.5–24.9 SD = 1.6, n = 12) and in adult females 25.1 mm (22.4–29, SD = 1.5, n = 19); (2) disc of Finger IV expanded 1.5 times the width of adjacent phalange; (3) Finger II shorter than Finger III; (4) fringes present on fingers; (5) disc of Toe IV expanded slightly less than 1.5 times the width of adjacent phalange; (6) fringes present on toes; (7) outer metatarsal fold present; (8) extensive toe webbing, formula I 1—(2–2 +) II (1)—(2–3) III (1–1½)—(3–3 +) IV (3–3 +)—(1– 1½) V; (9) oblique lateral stripe present, complete but diffused anteriorly or incomplete; (10) dorsum with three large blotches and small scattered spots; (11) gular-chest region brown or gray in adult males, completely cream or brown with white spots in adult females; (12) venter uniformly brown or gray in adult males, cream slightly translucent in adult females; (13) sexual dimorphism in ventral coloration present; (14) tadpoles translucent with brown stippling and blotches, a longitudinal brown mark on dorsum of tail musculature and, in vivo, two pale spots at each side of the oral disc; (15) tadpole spiracular opening oriented laterally; (16) call is a long trill composed of paired pulsed notes.

Hyloxalus maculosus is similar to those species with extensive toe webbing and oblique lateral stripe complete or diffused anteriorly ( H. bocagei , H. fuliginosus , H. sordidatus ). It is distinguished from H. bocagei by having a large spot at sacral level (small spots in H. bocagei ). Hyloxalus fuliginosus is larger (SVL 27.8– 32.5 mm, mean = 29.9 mm in 12 adult females, U- Mann-Whitney, U= 0, p <0.001; SVL 23.6–24.3 mm, mean = 23.8 mm in 4 adult males, U- Mann-Whitney, U = 6, p> 0.001, Coloma, unpublished data) and has less extensive toe webbing (formula I 1½—2 II 1½—(2½–3) III 2—(3–3½) IV 3½—2 V). Hyloxalus sordidatus is larger (SVL 24.2–29.9 mm, mean = 25.7 mm in 8 males, t -test, t = 5.71, df = 16, p <0.001; SVL 31.8–36.1 mm, mean = 33.6 mm in 3 females, t -test, t = 12.43, df = 15, p <0.001) and gular-chest region in adult females is yellow, whereas in H. maculosus it is cream or light brown ( Duellman, 2004). Specimens of H. maculosus that lack an oblique lateral stripe, or it is reduced at groin level, are similar with H. leucophaeus , H. italoi and H. yasuni . Hyloxalus maculosus differs from H. italoi and H. yasuni by the ventral coloration; males of these two species have the throat dark brown with white spots, whereas, H. maculosus has the throat uniformly gray or brown without white spots. In H. leucophaeus, Finger II is longer than Finger III, outer metatarsal fold is absent, and there is no sexual dimorphism in ventral coloration.

Description. Variation in measurements is given in Table 4 (n = 44: 20 males, 24 females). Head slightly longer than wide; snout subacuminate in dorsal view, angular in lateral view; loreal region flat; nostrils slightly protuberant; supratympanic bulge weak, covering upper edge of tympanum.

Finger II shorter than Finger III; fingers unwebbed; fringes present but discrete; terminal discs 1.5 times diameter of adjacent phalange; subarticular tubercles round, those of Finger II slightly oval, distals of Fingers IV and V only visible under dissecting microscope; outer metacarpal tubercle large, round and slightly protuberant; inner metacarpal tubercle at base of thumb small, elliptical and less protuberant than outer; an indistinctive keel in outer edge of metacarpus. Outer metatarsal fold present; inner sigmoid tarsal fold present on distal half of tarsus; outer metatarsal tubercle round; inner metatarsal tubercle same size as outer, elliptical; protuberance between the two metatarsal tubercles; toes more than half webbed, toe webbing formula I 1—(2– 2 +) II (1)—(2–3) III (1–1½)—(3–3 +) IV (3–3 +)—(1–1½) V; extensive lateral fringes on toes; terminal discs expanded slightly less than 1.5 times the diameter of adjacent phalange; subarticular tubercles round, small; supernumerary tubercles absent.

Skin on dorsum, limbs, flanks and venter smooth; scattered tubercles on posterior dorsum and on flanks of some specimens; small and round tubercle inmediatly posterior to mouth; anal sheath conspicuous. Tongue more than twice as long as wide, thinner and broader posteriorly, posterior half not attached to mouth’s floor. Testis white.

Variation of color in preservative (~70% ethanol). Variation in color patterns is depicted on Figs. 5B – 7B. Dorsum of head and body brown; an interorbital blotch, a V-shaped blotch at scapular level, a blotch at sacral level, and small spots around scapular level blotch; flanks brown; diffuse dark brown stripe from snout to arm-body junction. Oblique lateral stripe present, complete but diffuse in anterior portion, or incomplete. Forelimbs brown with three transverse bars on elbow and forearm, transverse bars continue throughout fingers; dorsal surfaces of hind limbs brown with transverse bars darker brown (approximately 11 at leg and tarsus); ventral surfaces cream-colored. Venter uniformly brown in adult males, cream in adult females; gularchest region uniformly brown in adult males, cream or slightly brown with white dots in adult females; axillas translucent. Palmar and plantar surfaces brown; toe webbing cream.

Sixteen juveniles (EPN 1649, 8906; QCAZ 19968–19971, 19973, 20628, 20630–20631, 37157, 37160; USNM 282069, 282074, 282077, 282683) with SVL of 12.9–21.7 (mean = 17.5) have same coloration as adult specimens. However, blotches are more contrasting with brown dorsal coloration than in adults. Ventral surfaces are translucent. Five recently metamorphosed specimens (QCAZ 19978–19982) have SVL of 9.9– 10.6 (mean = 10.3).

Color in life. ( Fig. 3B). QCAZ 37156 (adult male, 2.6 km W of Puyo). Dorsum reddish-brown, posterior portion of dorsum and hind limbs more reddish; brighter reddish-brown spots posterior to eyes and on arm at arm-body junction. Ventrally translucent; gular-chest region uniformly gray, two thin band-like marks at each side of throat; venter white. Loreal region plain light brown. Tubercle posterior to mouth iridescent. Iris bronze (MIP field notes, 09 July 2007).

QCAZ 37158–37159 (adult females, 2.6 km W of Puyo, Fig. 4B). Gular-chest region white; hind limbs ventrally translucent ( MIP field notes, 09 July 2007) .

Variation. Twelve specimens from 2.6 km W of Puyo ( QCAZ 37156–37160 ), and also males from Santa Rosa ( QCAZ 42074–42084 ) are gray in preservative and the oblique lateral stripe is indistinctive; oblique lateral stripe to midflanks in females ( QCAZ 42078 , 42082–42083 ). Two males ( QCAZ 37156 , 37868 ) exhibit two band-like marks at gular-chest region; two females ( QCAZ 37158 and 37159) have the gular-chest region gray with white spots. Specimens from Puerto Misahuallí ( QCAZ 19968–19978 , 20628 , 20630–20631 , 20635 , 21186 ) are slightly lighter; transverse bars in hind limbs are very subtle and the oblique lateral stripe is reduced to a short cream band anterior to the groin. A male ( QCAZ 19972 ) has a cream longitudinal band in middle of the throat, and in two females ( QCAZ 19975 and 21186), the gular-chest region has brown stippling over a cream background .

Tadpole. The following description is based on a single specimen in Stage 28 (QCAZ 42086a, Figs. 11B, 15). Tadpole corresponds to a series of back-riding tadpoles from adult male QCAZ 42085, obtained in Santa Rosa, Provincia Pastaza, Ecuador. All measurements provided are in millimeters. Total length 26.7; body ovoid, depressed, narrower at anterior portion; body length 10.0 (37.5% of total length), width at spiracle 7.5, height taken posterior of eyes 5.5; snout round in dorsal and lateral views.

Nostrils very small, directed anterolaterally, openings circular; opening 2.5 from tip of snout; internarial distance (taken at internal edge of each nostril) 1.8; distance from narial opening to anterior edge of eye 1.0. Eyes directed dorsolaterally; eye length 1.0, width 0.9; interorbital distance from internal edge of each eye 1.8.

Spiracle sinistral 5.6 from tip of snout (56% of total length); inner wall free in its distal portion; length 1.2, width at base 1.3; opening directed laterally and with a diameter of 0.4. Vent tube totally bounded to ventral fin, length 1.2, width 1.2; opening circular and dextrally to ventral fin.

Tail length 17.8 (66.9% of total length); tail musculature narrowing gradually, tail musculature almost reaches tail terminus ( Fig. 15B); myotomes conspicuous from the posterior half of tail; muscle width at bodytail junction 2.7, muscle height 2.7; tail height at midtail 6.3; dorsal and ventral fin originate at body-tail junction; dorsal fin height 1.7, ventral fin height 1.0; distal margin of tail slightly round ( Fig. 15B). Lateral line system poorly developed; interorbital, supraorbital, and dorsal body lines hardly seen; dorsal body line not visible on the tail.

Oral disc located ventrally, emarginated on both sides ( Fig. 10B); transverse width 3.0 (40% of body width); border of disc surrounded with 104 marginal papillae: 65 ventral papillae and 39 located laterally (18 at one side and 21 at the other); submarginal papillae absent; alternate ventral marginal papillae are slightly displaced to opposite directions, emulating two rows; towards the sides of the oral disc, the ventral papillae are distributed irregularly; lateral papillae are aligned, but alternate papillae are oriented to opposite directions, also emulating two rows; single anterior gap of papillae 1.4.

Anterior and posterior jaw sheaths serrated through their entire length; serrations less profound as they move away from center; anterior jaw sheath transverse width, including lateral processes, 1.3 (43.4% of oral disc width); anterior and posterior edges of anterior jaw sheath convex; posterior jaw sheath V-shaped, transverse width 0.9 (30.3% of oral disc width).

Labia tooth row formula 2(2)/3; anterior tooth row A-1 length 2.1, number of teeth 197; A-2 length 1.0 and 75 teeth at each side of gap; A-2 gap length 0.1; a 1-tooth gap at P-1 row; posterior tooth row P-1 length 2.0, 142 teeth (71 at each side of small gap); P-2 length 2.0 and 168 teeth; P-3 length 2.0 and 189 teeth.

Color in preservative (~10% formalin). Dorsum and sides of body translucent with brown stippling. Ventrally, oral disc and immediate posterior region translucent. Region anterior to spiracle slightly stippled; posterior region of venter translucent leaving gut visible. Spiracle and vent tube translucent. Jaw sheath coppery brown.

Tail musculature white, translucent posteriorly; dorsally stippled from body-tail junction to two thirds of its length, forming a conspicuous blotch ( Fig. 15). Ventrally white. Laterally, scattered gray small blotches on the anterior two thirds. Fins translucent; dorsal fin with scattered small blotches on the anterior two thirds; ventral fin immaculate.

Color in life. ( Fig. 11). Dorsum brown with golden glitter; tail whitish with brown and golden spots on the anterodorsal portion, laterally white with brown flecks. Ventrally translucent, two pale spots at each side of the oral disc (photo of QCAZ 42086, taken by LAC).

Variation. Twenty (20) tadpoles in Stages 25–36 were examined; however, not every stage is represented in the sample. Variation of 17 measurements is given in Table 10.

Variation in tooth row P-1 consists of 83% of tadpoles in Stages 25–29 (n = 12) lack an evident gap. From Stage 33, gap is present in every specimen examined with the exception of two (n = 8). Specimens from the series QCAZ 37864–37865 differ in having a more pronounced oval body shape, posterior portion narrower; dorsum of body brownish and stippling in dorsal surface of tail is less visible. As development proceeds, the lateral line system becomes more evident; dorsal body, middle body, infraorbital, supraorbital and posterior supraorbital are visible from Stage 33. Dorsum of body and tail of tadpoles in early stages (25–29) is stippled. As development continues, the dots grow and blur to combine with other dots, resulting in a blotch pattern and, ultimately, in a uniform pattern of coloration.

Two metamorphs in Stage 42 (QCAZ 37864i, j) and one metamorph in Stage 44 (QCAZ 37865e) exhibit the same coloration pattern of adult specimens. Nonetheless, the transverse bars on limbs are more conspicuous. Gular-chest region slightly stippled and abdomen translucent. Dorsal tail blotch conspicuous and scattered spots throughout tail.

Comparisons. Tadpoles of Hyloxalus maculosus are notably similar to H. bocagei and H. sauli . They differ from H. bocagei in the following: (1) shape of dorsal fin ( Figs. 9B, 11A− B, 15B); (2) spiracular opening directed laterally (directed dorsoposteriorly in H. bocagei ); (3) oral disc narrower in relation to body width (t - test, t = 3.544, p <0.001); (4) labia immaculate (stippling on anterior and posterior labia in H. bocagei ); (5) anterior jaw sheath broader ( Fig. 10A− B). It differs from H. sauli in the following: (1) tail terminus is round in H. maculosus , pointed in H. sauli ; (2) spiracular opening directed laterally (dorsoposteriorly in H. sauli ); (3) anterior jaw sheath broader and the anterior edge is convex, whereas it is slightly winding in H. sauli .

Tadpoles of Hyloxalus maculosus are morphometrically different from H. italoi and H. yasuni (MANOVA, p <0.001, F = 15.437, df = 30, df2 = 361.705, n = 137). Additionally, the following differences are appreciable: (1) body less elongated in H. maculosus (t -test, t = 3.749, df = 59, p <0.001 with H. italoi ; t = 4.332, df = 33, p <0.001 with H. yasuni ); (2) dorsal caudal blotch present (absent in H. italoi and H. yasuni ); (3) spiracle directed laterally (dorsoposteriorly in H. italoi and H. yasuni ); (4) tail musculature does not reach tail terminus in H. maculosus ; (5) greater number of labial papillae (t -test, t = 6.163, df = 59, p <0.001 with H. italoi ; t = 5.229, df = 33, p <0.001, with H. yasuni ); (6) anterior edge of anterior jaw sheath is round in H. maculosus , winding in H. italoi and H. yasuni ( Fig. 10B− D); (7) labia immaculate (blotches in labia of H. italoi and H. yasuni ); (8) in life, H. maculosus has a pale mark at each side of oral disc, whereas H. italoi and H. yasuni also exhibit two pale marks at each side of body at spiracular level ( Fig. 11).

Comments. Rivero’s description of Hyloxalus maculosus (1991) is appropriate. Nonetheless, he points out that the holotype specimen corresponds to an adult male. Despite the presence of vocal slits, this specimen has juvenile appearance (SVL = 20.4 mm) and does not exhibit sexual dimorphism in ventral coloration. We have noticed that vocal slits can be open in juveniles as a result of manipulation. The presence of vocal slits in this specimen could be an artifact of previous manipulations. Thus, the holotype of H. maculosus is considered a juvenile. On the other hand, the specimen assigned as paratype (MCZ-A 104846) by Rivero (1991) corresponds to H. bocagei ( Fig. 16). See also comments in H. bocagei account. Hyloxalus maculosus is resurrected from H. bocagei ’s synonymia. These species differ in adult and tadpole morphometrics and external morphology. Additionally, call parameters of their advertisement call show statistically significant differences (see Call Comparisons section, and Tables 2 and 3 for patristic distances). Santos et al. (2003, 2009) assigned erroneously the name of H. maculosus to specimens from El Porvenir (= Reserva Hola Vida) and Kapawi in Provincia Pastaza, which belong to H. italoi . Further information is included under Phylogeny and Chronogram and Ancestral Area Reconstruction sections ( Tables 2 and 3; Fig. 1).