Colostethus trilineatus

NATURAL HISTORY: Colostethus trilineatus is a forest­dwelling species not closely associated with bodies of water. Numerous aspects of its ecology have been reported (usually under the name C. marchesianus) by Toft and Duellman (1979), Aichinger (1987), Rodríguez (1992), Duellman and Mendelson (1995), Wild (1996), and Parmelee (1999). VOCALIZATIONS

AMNH FS 8689 (16.0 mm SVL) was collected at Yurimaguas, the type locality. A recording of this frog (AMNH herpetology reel 272, made by Javier Icochea at 15: 18 h on 25 September 1993, 27 ° C) includes 27 calls in 3.08 min of continuous tape (0.15 calls per sec). The advertisement call (fig. 7) is a series of short, high­pitched peeps. Calls consist of 9 – 13 notes (n = 26, x = 11.2 ± 0.3 notes, mode = 10 notes; one obviously anomalous call of four notes is excluded). Call duration is 972 – 1550 msec (n = 26, x = 1260 ± 29.8 msec). Detailed data were taken from the first two calls on the tape, constituting 12 and 11 notes, respectively. In both calls, the first two notes are shortest (both 41.8 msec in call 1; 39.5 and 41.0 msec, respectively, in call 2). Similarly, internote duration between the first two notes of both calls is less than half of that of the other notes (25.8 msec in call 1; 29.9 msec in call 2). Video spectrographic scrolling revealed that in 17 of the 27 calls the internote duration between the first two notes is conspicuously less than between the remaining notes. For the remaining notes, note duration is 43.0 – 45.3 msec (n = 19, x = 43.79 ± 0.15 msec); internote duration is 71.1 – 88.7 msec (n = 17, x = 77.92 ± 1.25 msec). Each note weakly frequency modulated from lower to higher, with emphasized frequencies of the 23 notes between 4920 and 6040 Hz. Minor frequency modulation is detected among the notes of each call, in which notes are emitted at increasing frequencies, then decreasing frequencies, and again increasing frequencies, before terminating at a relatively high frequency.

Figures 2 – 7

MEASUREMENTS OF HOLOTYPE (in mm): BMNH. 1947.2.14.20 is an adult male with vocal slits and large, unpigmented (white) testes. SVL, 17.2; forearm length from proximal edge of palmar tubercle to outer edge of flexed elbow, 4.0; hand length from proximal edge of palmar tubercle to tip of Finger III, 3.8; shank length from outer edge of flexed knee to heel, 8.0; foot length from proximal edge of outer metatarsal tubercle to tip of Toe IV, 7.2; head width between angle of jaws, 6.0; head length diagonally from corner of mouth to tip of snout, 5.3; eye length from posterior to anterior corner, 2.5; eye to naris distance from anterior corner of eye to center of naris, 1.5; distance between centers of nares, 2.5; snout length from anterior corner of eye to tip of snout, 2.8; interorbital distance, 1.9; diameter of tympanum immeasurable (due to preservational artifact). REDESCRIPTION A composite redescription is provided based on 123 specimens from one Ecuadorian and 13 Peruvian localities. Many of these localities and / or their anuran assemblages have been described in detail (Toft and Duellman, 1979; Aichinger, 1987; Duellman and Koechlin, 1991; Rodríguez, 1992; Duellman and Mendelson, 1995; Duellman and Thomas, 1996; Wild, 1996; Parmelee, 1999). All localities are below 900 m. Given that several of the most crucial diagnostic characters are restricted to adult males, the four localities for which adult males were not available are marked with an asterisk and are only tentatively referred to Colostethus trilineatus (number of specimens examined in parentheses; see fig. 1 and appendix): Aguas Negras * (5); Río Alto Purús (1); Candamo * (2); Cocha Cashu (26); Río Curanja (4); Cuzco Amazónico (16); Explornapo * (1); Genaro Herrera (4); Limoncocha, Ecuador (3); Panguana (50); Río Santiago (1); Tambopata (2); Teniente López * (3); Yurimaguas (5). Colostethus trilineatus also has been reported from Bolivia (Morales, 1994; De la Riva et al., 1996; Köhler and Lötters, 1999; Gonzalez et al., 1999), but Bolivian material was not examined in this study. MORPHOLOGY: Adult males 15.0 – 17.7 mm SVL (n = 48, x = 16.45 ± 0.09 mm), adult females 15.2 – 19.3 mm SVL (n = 57, x = 17.09 ± 0.12 mm). The holotype is larger than the other two males from Yurimaguas (MUSM 15611 = 16.1 mm SVL; AMNH FS 8689 = 16.0; see fig. 3), but the difference in SVL is less than that observed within some other populations (e. g., Panguana). Testes unpigmented (white) in all males. Mature ova pigmented black or brown. Most of dorsal and ventral surfaces smooth, except variably expressed tubercles scattered over posterior part of body and dorsal surfaces of legs and a weak, low tubercle on each eyelid in well preserved specimens. A weak to strong postrictal bulge present, reminiscent of postrictal spicules or tubercles found in many Colostethus. Head width between angle of jaws 31 – 36 % of SVL, 1.02 – 1.25 times head length in males and 0.95 – 1.14 in females. Interorbital distance 27 – 38 % of head width. Snout sloped, rounded in dorsal aspect, sharply rounded in profile, protruding beyond jaws. Loreal region flat or weakly concave, not sloping outward to lip. Canthus rostralis sharply rounded and well defined. Eye length 39 – 53 % of head length. Eye­naris distance 50 – 64 % of snout length and 54 – 80 % of eye length. Nares directed posteriorly in profile, protuberant in dorsal aspect. Tympanum small; greatest diameter 33 – 48 % of eye length. Teeth on maxillary arch straight, moderate in length, not curved and fanglike. Hand length (fig. 4) 20 – 26 % of SVL, 0.89 – 1.15 times forearm length. Finger I> Finger II when appressed. Relative lengths of appressed fingers III> I> II> IV. Fingers weakly keeled distally. Metacarpal fold absent. A single, protuberant subarticular tubercle on each of Fingers I and II, two on Finger III, and one or two on Finger IV. Palmar tubercle well defined, elliptical or subtriangular. Thenar tubercle weak, elliptical. Digital discs weakly expanded. A pair of strong dorsal scutes on each disc. Finger III swollen in all adult males (contra Duellman and Mendelson, 1995: 338), not distally exaggerated. Degree of swelling somewhat variable, but strong and conspicuous along entire length of preaxial side of digit in all but a few adult males. Finger II also swollen along preaxial side between level of subarticular tubercle and finger disc (fig. 4) in five (of 11) adult males from Cocha Cashu, two (of six) from Cuzco Amazónico, and 12 (of 20) from Panguana (Finger II of several other specimens from these and other localities could not be unequivocally coded as swollen or not). Not all males from a locality had Finger II swollen, and no specimen had Finger II swollen and Finger III not swollen. Shank length and foot length 41 – 49 and 37 – 47 % of SVL, respectively. Relative lengths of appressed toes IV> III> V> II> I. Basal webbing between Toes II – IV (webbing formula II 1 ½ – 3 ½ III 2 ½ – 4 IV, following Myers and Duellman, 1982). Weak keels or fringes present on both edges of all toes. Outer metatarsal fold 3 present, often forming small tubercle. Tarsal keel on distal third of tarsus well defined, tuberclelike, arising roughly one­third to one­fourth tarsus length from the distal end of the tarsus, not extended distad to reach outer edge of inner metatarsal tubercle. Toe discs weakly expanded; each with pair of well­defined scutes on dorsal surface. One subarticular tubercle on Toes I and II, two on III and V, and three on IV. Outer metatarsal tubercle round; inner metatarsal tubercle elliptical; both tubercles well­defined and protuberant. COLOR IN PRESERVATIVE: The dorsal coloration (figs. 2, 3, 5) is tan to dark brown, either uniform or with small, dark spots scattered over the dorsum. Within­population variation in the expression of a narrow, pale vertebral stripe is as follows (present: absent): Aguas Negras (0: 5); Río Alto Purús (0: 1); Candamo (0: 2); Cocha Cashu (19: 7); Río Curanja (1: 3); Cuzco Amazónico (8: 8); Explornapo (0: 1); Genaro Herrera (0: 4); Limoncocha (0: 3); Panguana (0: 50); Río Santiago (0: 1); Tambopata (1: 1); Teniente López (0: 3); Yurimaguas (1: 4); total for all localities (30: 93). All specimens have a pale dorsolateral stripe from the posterior corner of the eyelid to almost the end of the urostyle, although it is inconspicuous in specimens that are dorsally very light (e. g., MUSM 9186 and 9195, both from Cocha Cashu). In one specimen (AMNH FS 8689 from the type locality; see fig. 3) the pale dorsolateral stripes broaden medially just behind the eyelids to form the outline of an hourglass pattern. The eyelid is blackish brown in all specimens. Ventral coloration among adult males is somewhat variable (figs. 3, 5). In most specimens, the throat and chest are stippled gray, but in some (e. g., MUSM 9196 and 15611) the stippling is much heavier, making the throat and chest dark gray or brown (but never solid black). In females, the throat, chest, and medial belly are immaculate or nearly so (very weak stippling often occurs on the chin). In all specimens examined, the belly is more strongly pigmented laterally than medially. In some specimens (e. g., MUSM 9184) the lateral belly ventral (medial) to the ventrolateral stripe is dark brown with whitish spots, whereas in others (e. g., KU 194916) it is stippled brown or gray with a variable number of elongate brown spots. Thigh coloration is highly variable (figs. 3, 5). Dorsally, thighs are tan or light brown, free of dark markings (e. g., AMNH FS 8689, fig. 3) or with numerous, irregular, small spots or blotches, one or more well­defined blotches, or one well­defined transverse band of variable width. In most specimens, the anterior surface of the thigh exhibits a diffuse pale brown, brown, or black (in dark specimens, e. g., MUSM 15611) stripe from the knee through the groin and continuous with the dark coloration of the flank. A few specimens (e. g., KU 194916) lack a dark anterior thigh stripe; in these, the anterior surface is the same color as the dorsal surface. A flash mark is absent from the groin. The posterior surface of the thigh is gray, pale brown, brown, or dark brown and invariably with minute, diffuse, whitish dots. The white spot on either side of the cloaca that Boulenger (1883) described is present in all well­preserved specimens, although it varies from a prominent, well­defined spot (e. g., AMNH FS 8689) to an inconspicuous narrow line (e. g., MUSM 9184; much of the variation in this character is shown in fig. 5). Thighs are usually ventrally immaculate, although they occasionally have a few diffuse gray or brown specks of pigment. The dorsal surface of the shank has one poorly to well­defined transverse band in most specimens, although in some (e. g., MUSM 9183) the shank is covered in irregular, dark brown blotches that fail to define a transverse band. Concealed surfaces of the shank are invariably pigmented pale brown or gray (i. e., flash marks absent). The inner surface of the foot is immaculate creamy white, free of melanophores. The plantar surface is brown or gray with creamy white blotches and spots; contact surfaces of tubercles are dark gray. Webbing between Toes III – IV is creamy white or brown. The arm is dorsally gray or tan with variably expressed darker brown blotches that extend from the anterior and posterior surfaces. The anterior and posterior surfaces of the upper arm have well­defined, dark brown, longitudinal stripes. The anterior stripe extends from near the base of the arm almost to the elbow; the posterior stripe extends from the axilla around the elbow, where it meets the dark brown mottling on creamy white ground of the outer and ventral sides of the forearm. Palmar surfaces are brown. The flank is dark brown or blackish brown with or without pale flecks and spots (fig. 6). The dark coloration of the flank is delimited ventrally by a moderately to well­defined ventrolateral stripe passing just dorsal to the arm, present in all specimens. Most specimens in all populations have a diffuse pale area anterior to the groin that extends anterodorsad to a point no further than half the distance to the arms (figs. 2 and 6). In some (e. g., MUSM 9201), this pale area includes several diffuse, whitish spots. In a few specimens (e. g., KU 194916), the area anterior to the groin is not obviously lighter than the rest of the flank, but this is probably a preservational artifact, as all well­preserved and living frogs have this pale region (e. g., fig. 2). The dark coloration of the flanks continues anteriad from the eye, through the loreal region, and around the snout (encompassing nares) to form a face mask. Below this, the face is creamy white with gray stippling or a blackish brown stripe along the upper lip (e. g., MUSM 15611). Dark lower lip line absent. COLOR IN LIFE: Color in life was described for specimens from Teniente López (Duellman and Mendelson, 1995) and Río Curanja (Duellman and Thomas, 1996), and color photographs of Bolivian specimens were published in Gonzalez et al. (1999). Photographs taken by LOR of material from Cocha Cashu (e. g., fig. 2) and Genaro Herrera agree with the published accounts except that the spots on either side of the cloaca and the vertebral stripe are yellowish bronze and the vertebral stripe is bordered by black.

DIAGNOSIS: A very small Colostethus (males to about 18 mm SVL; females to about 19 mm SVL); Finger III (and often Finger II) of adult males strongly swollen; throat evenly stippled gray in adult males; testes white (unpigmented) in adult males; Toes II – IV basally webbed; dorsolateral stripe present; oblique lateral stripe present as diffuse, inconspicuous, pale region or group of small spots extending from groin to midway along flank (see Remarks, below); ventrolateral stripe present; one or two subarticular tubercles on Finger IV; median lingual process absent; cloacal tubercles absent; anal sheath absent; black armband absent. Colostethus trilineatus most resembles six nominal species from the Amazon basin: C. beebei (Noble, 1923); C. brunneus; C. juanii Morales, 1994; C. marchesianus; C. peruvianus (Melin, 1941); and C. stepheni Martins, 1989. Colostethus beebei is most easily distinguished from C. trilineatus by the possession of a median lingual process. Adult male C. brunneus lack a dark throat, swollen Finger III, and ventrolateral stripe. Colostethus juanii is a larger species (tables 1 – 2) in which the gray stippling on the throat of adult males is concentrated into spots or mottling and Finger III of adult males is not swollen. Adult male C. marchesianus have an immaculate throat (Morales, 1994). According to Morales’s (1994) account and photographs of the holotype in the possession of TG, C. peruvianus has a complete oblique lateral stripe and lacks a ventrolateral stripe. Colostethus stepheni has a median lingual process, a well­defined, complete oblique lateral stripe, and lacks the dorsolateral and ventrolateral stripes.

REMARKS Colostethus brunneus and C. marchesianus have been reported from Peru (Duellman and Toft, 1979; Toft and Duellman, 1979; Schlüter, 1980; Frost, 1985; Rodríguez, 1992; Rodríguez et al., 1993; Rodríguez and Duellman, 1994; Wild, 1996; Parmelee, 1999). However, none of the material we examined is referable to those taxa, and we suspect that previous reports were based on erroneously determined specimens of C. trilineatus. The diffuse, pale region extending from the groin to midway along the flank is located in the same area as the oblique lateral stripe and is presumably homologous with it. However, this pattern does not conform to any of the previously delimited states (i. e., complete from groin to eye, e. g., C. nubicola [Dunn, 1924]; broken into series of spots, e. g., C. agilis Ruiz­Carranza and Lynch, 1985; partial or incomplete, e. g., C. kingsburyi [Boulenger, 1918]), and it is frequently overlooked. It is often difficult to code unambiguously, as it is hard to distinguish from chafing, fading, and other preservational artifacts, or from the white spots and flecks that are roughly uniformly scattered over the flank of many species of Colostethus. Nevertheless, all well­preserved and live exemplars of a number of similar species possess this diffuse, pale area on the flank, and we have not noticed it in any species west of the Amazonian slopes of the Andes. In the Amazon basin, we have observed this state in C. brunneus, C. juanii (in which it is usually quite prominent), C. trilineatus, C. melanolaemus (named below), and at least five unnamed species. The discovery of the swollen second finger in some specimens was initially taken as evidence for the recognition of two species. However, related evidence indicates that this interpretation was spurious. Specimens with the swollen second finger were all found in sympatry with specimens that exhibit swelling only of the third finger. Field notes and other data do not indicate differences in microhabitat selection, and the specimens are otherwise indistinguishable (e. g., fig. 5). Similarly, both conditions were found at localities separated by> 700 km (Panguana in the middle portion of the range, and Cocha Cashu and Cuzco Amazónico in the southern portion), and the swollen second­finger morphology was detected only in the three largest samples. The expression of swelling of the third finger is known to vary among males taken in large series (Myers et al., 1991; personal obs., TG), probably as a function of reproductive activity, and it is likely that the swollen second finger would serve the same function and undergo the same kind of variation. This claim is further supported by our observation of apparently continuous variation in the amount of swelling of the second finger (which prevented us from clearly assigning several specimens to either of the morphological classes). It should be noted, however, that swelling of Finger II does not appear to covary with age (inferred from SVL) or other secondary sex characters that often vary with reproductive activity (e. g., throat color; fig. 5). Several differences in temporal patterning are observed between the vocalizations recorded at the type locality and those reported for Panguana (Schlüter, 1980) and Cuzco Amazónico (Coloma, 1995; De la Riva et al., 1996). 4 Calls recorded at the latter two localities consist of couplets repeated at roughly 200 msec intervals; each note of the couplets has a duration of <30 msec. Rodríguez and Duellman (1994: 16) report a similar call of ‘‘ two chirplike notes produced at a rate of about 72 per minute’ ’, but no further data are provided. In contrast, the calls recorded at the type locality are composed of single notes (i. e., not couplets) of usually> 40 msec duration, repeated at <90 msec intervals. Although these differences in amplitude modulation could conceivably indicate the existence of two species, the calls of the three populations are spectrally identical and no significant morphological differences were detected among the specimens examined. 5 It has long been known that signal structure may vary greatly among populations, individuals, and even calls of the same individual (Bogert, 1960; see Junca´, 1998 and Myers et al., 1998, as well as the discussion of C. juanii, below, for examples of variation of temporal patterning in dendrobatids). When acoustic samples are small and the differences between them unaccompanied by morphological or other correlates, taxonomic interpretations should be conservative. For this reason, we continue to refer to all these frogs as C. trilineatus. In contrast to the above, another similar species occurs in the same vicinity as Colostethus trilineatus, but differs in both temporal and spectral call parameters as well as in morphology. Consequently, we name it

Holotype BMNH 1947.2.14.20 from ‘‘ Yurimaguas, [Departamento Loreto,] Huallaga River, Northern Peru. ’’