Gastrotheca pseustes Duellman & Hillis 1987

Carvajal-Endara, Sofía, Coloma, Luis A., Morales-Mite, Manuel A., Guayasamin, Juan M., Székely, Paul & Duellman, William E., 2019, Phylogenetic systematics, ecology, and conservation of marsupial frogs (Anura: Hemiphractidae) from the Andes of southern Ecuador, with descriptions of four new biphasic species, Zootaxa 4562 (1), pp. 1-102 : 79-85

Gastrotheca pseustes Duellman & Hillis 1987

Gastrotheca pseustes was described from 7.1 km by road north of San Lucas, 2940 m (03° 41' S, 79° 15' W), Loja Province, Ecuador, in the southern Andean Cordillera. The type locality is located about midway between San Lucas and Saraguro. Current assignment of specimens to this taxon is constrained because: (1) there is a high phenotypic similarity between G. pseustes and G. lateonota from the Cordillera de Huancabamba in Peru (compare both species in Fig. 10 with Duellman 2015: Fig. 12.21); (2). There is no genetic information for topotypic G. lateonota , thereby precluding comparisons with specimens from southern Ecuador; (3) according to Duellman (2015), variation in morphometrics, structural characters, and coloration within G. pseustes presents a geographic mosaic, except for the southernmost population, Saraguro. The frogs from Saraguro are somewhat more distinctive than the others in being larger in size, and in having broader heads and some consistent characteristics of color pattern, including dark flanks with pale spots and uniformly dark posterior surfaces of the thighs; and (4) new molecular phylogeographic data (not shown) suggest that there may be at least two species in what is now recognized as Gastrotheca pseustes .

While awaiting ongoing analyses of molecular data and a future report with a more detailed taxonomic and phylogeographic revision of Gastrotheca pseustes , we provide additional data of specimens (adults, tadpoles and metamorphs) from the type locality and surrounding areas in Loja and El Oro provinces.

The recognition of Gastrotheca lateonota in southern Ecuador (from El Oro and Loja provinces) by Blackburn & Duellman (2013), Duellman et al. (2014), Yáñez-Muñoz et al. (2014), and Duellman (2015) was based on specimens identified as that species by Carvajal-Endara and Coloma. Subsequent examination of the specimens from Chilla, El Oro Province, reveals that they do not differ from the holotype (KU 203443, Fig. 10G ) and additional specimens ( Figs. 10 D–F) of G. pseustes , from 3.7 km S Saraguro, 2800 m. Thus, we do not recognize G. lateonota to occur in Ecuador, and treat the specimens from Chilla as part of a series of populations we consider G. pseustes complex ( G. pseustes 1, G. pseustes 2, Fig. 33 ), occurring from the Equator south to high elevations of Podocarpus National Park in southern Ecuador (see also map in Duellman 2015: Figure 12.47). Conceivably, molecular data from topotypic G. lateonota from 31.5 km [by road] E Canchaque, 2770 m, Cordillera de Huancabamba, Región de Piura, Peru, ( Fig. 33 ), and additional populations from northern Peru would resolve by (1) placement of non-type populations in either G. pseustes or G. lateonota , or (2) placement of G. lateonota as a junior synonym of G. pseustes .

Castroviejo-Fisher et al. (2015) included in a phylogenetic analysis a specimen UINHM 94580 from San Rafael, Azuay, Ecuador under the name Gastrotheca riobambae , a species that does not occur in southern Ecuador. Their analysis places it in the G. pseustes complex. We also found a locality named San Rafael in Azuay Province, which is located between Cuenca and Cumbe, in Parroquia Tarqui at about 2700 m asl (not in the lowlands as was stated by Castroviejo-Fisher et al., 2015). This locality is well within the altitudinal and latitudinal range of G. pseustes 2.

Herein, we provide meristic data from specimens of Gastrotheca pseustes 1 and 2 ( Table 3), images depicting intrapopulation color pattern variation of metamorphs ( Fig. 34 ), of adults of G. pseustes 1 from the type locality ( Fig. 10G ) and from Chillacocha ( Figs. 10 D–F). Data for additional specimens of G. pseustes 1 are: QCAZ 45121, 45124 – 5, adult males, and QCAZ 45123 adult female from Chillacocha, ~ 8 km SW Chilla, El Oro Province (03° 30' 39.1" S, 79° 36' 52.92" W; 3163 m) collected on 18 August 2009. The frogs were on leaves of Gunnera sp. ( Gunneraceae ) near a small stream and adjoining marshland about 10 x 5 m. The water temperature was 9.6° C. Two individuals—CJ 201 adult female and KU 335386 adult male—are from Chillacocha, ~ 8 km SW Chilla, El Oro Province (03° 30' 15.37" S, 79° 37' 01.7" W; 3250 m) collected on 10 June 2011. They were in amplexus on a leaf of Gunnera sp. ( Gunneraceae ) approximately 90 cm above the ground and a small stream. Tadpoles were collected from a puddle next to the road in the vicinity of Chilla, El Oro Province (03° 27' 29.41" S, 79° 34' 52.07" W; 2452 m) on 11 June 2011; one of these was raised to be an adult male (CJ 399). Tadpoles were collected from a puddle next to the road at Manu, Loja Province (03° 33' 17.03" S, 79° 22' 6.02" W; 2876 m) on 11 June 2011; one of these was raised to be an adult female (CJ 400). Tadpoles were collected from the entrance of Parque Nacional Podocarpus, Loja Province (04° 05' 25.51" S, 79° 12' 09.97" W; 2456 m) on 14 June 2011; one of these was raised to be an adult female (KU 335387).

Tadpoles. Tadpoles belong to Type IV tadpole of Orton (1953), and the exotroph, benthic ecomorphological guild. All measurements are expressed in millimeters. The following description is based on a specimen in Stage 36, from a series (CJ 1949) obtained from a pond at Chillacocha, 8 km SW Chilla, 3250 m, El Oro Province, Ecuador, by Elicio E. Tapia, Sofía Carvajal-Endara, and Henry Grefa on 10 June 2011 ( Fig. 5E ). Total length 58.2; body length 22.7 (39% of total length). Body ovoid in dorsal and lateral views, slightly depressed; throat concave in lateral profile, sloping from anterior margin of snout to belly; body width at level of spiracle 15.3, and height at same position 12.9; head width at level of eyes 11.7. Lateral-line system present but barely visible, supraorbital and infraorbital lines both originating at tip of snout, running parallel to the eye and making contact immediately behind the eye; angular line descending vertically from just posterior of eye to throat; it dorsally contacts with post infraorbital line; post-supraocular present in form of a few stitches, anterior oral line descending vertically from oral disc level and behind nares level to throat, making a curve that parallels infraorbital line, forming a circuit continuous with angular and loreal lines; ventral line surrounds dorsally the spiracle; dorsal body and middle body lines not visible. Nostril medium sized (in proportion to body length), ovoid, protruding, with a fleshy annulus, its opening directed anterolaterally. Snout–nostril distance 3.9; internarial distance 3.6. Eye positioned and directed dorsolaterally, eye length 2.9, eye width 2.3; interorbital distance 7.1. Spiracle sinistral, located at midbody, spiracular opening oriented posteriorly; distance from tip of snout to spiracular opening 15.6; end of spiracle rounded, attached to body wall, inner wall of spiracle not evident; tube length 2.7, tube transverse width 3.0. Vent tube dextral, opening directed posteriorly, tube length 2.9, tube transverse width 2.8. Tail length 35.0, caudal musculature robust, narrowing gradually until tail terminus; caudal muscle height 4.5, caudal muscle width 4.3; caudal fins well developed and proportional, dorsal fin originating near tail-body junction, forming low hump; dorsal fin height 4.2, ventral fin height 3.8; maximum height of tail 12.3; tail terminus rounded, caudal musculature not reaching fin terminus.

Oral disc small, ventral, anteriorly reaching level of tip of snout, not protruding laterally beyond body, not visible dorsally; transverse width 5.9, surrounded by an uniserial row of small, marginal papillae, interrupted medially in upper lip; lower lip papillae alternating in orientation in and out, giving appearance of two rows; upper lip with 17 papillae on right side and 16 papillae on left side; lower lip with 52 marginal papillae; upper jaw sheath medium-sized, forming a finely serrated, smooth arch, with lateral processes, height 0.56, transverse width 3.7 (63% of oral disc width); lower jaw sheath V- shaped, finely serrated, width 2.9, height 0.68. Labial tooth row formula 2/3(1), tooth rows lengths: A1: 4.2, A2: 4.5, P1 right row 1.9, P1 left row 2.0, P1 gap 0.3, P2: 4.1, P3: 3.7. ( Fig. 6F ).

Color in preservative. Dorsum gray with darker gray areas on flanks, above eye and on throat; margin of snout paler than adjacent areas. Caudal musculature and fins with a profusion of medium-sized dots that are most dense on upper part of the musculature; fins otherwise translucent. Venter cream, speckled with white, guts not exposed; eyes lavender gray with irregular white markings, oral apparatus translucent.

Color in life. In dorsal view, body tan with black flecks. Flanks reticulated with black and tan; areas around the eyes and snout paler tan. Venter cream with black markings; throat translucent with small cream flecks; reddish gills evident. Caudal muscles reddish-pink, more evident on proximal half; myomeres barely visible; caudal muscles and fins having medium-sized cream dots, most dense on upper side of caudal muscles and near tail-body junction, forming a nearly conitnuous stripe along dorsolateral caudal musculature; otherwise caudal fins translucent. Legs cream with black markings on toes. Oral apparatus pale cream. Iris copper-yellow, with black reticulations.

Variation. Variation of 28 meristic characters of tadpoles in Stages 36–42 (CJ 1949) are shown in Table 10. Total length varies between 55.0 (Stage 40) and 58.2 (Stage 36) and tail length proportion varies from 60% to 70% until Stage 42. Number of marginal papillae varies among specimens and Gosner stages; number of lower lip papillae is high (43–52).

We documented changes in coloration during ontogenetic development of one, mostly pale brown individual (CJ 1953) ( Figs. 5E , 35 ). At Stage 41, the dorsum and flanks are yellowish-brown with a poorly defined pattern of brown-gray, elongated paravertebral marks and few blotches on dorsum of hind limbs. A diffuse brown-gray stripe borders the canthal and dorsolateral body, and is bordered above by a creamy-brown stripe. The iris has a reddishgold suffusion. By Stage 45, markings on the dorsum and flanks are better defined with brown markings darkest peripherally; scattered green ill-defined flecks are present on dorsum of head, limbs, and canthus rostralis; tip of fingers are yellowish-cream. At Stage 46, paravertebral green-brown markings on dorsum of body and green flecks on limbs are contrasting to surrounding light brown areas; flanks have a dark brown stripe. Color variation in 6 metamorphs (CJ 1949, 1953–56, QCAZ 45126) in Stage 46 is depicted in Figure 34 . They vary from dark brown to green with either well-defined paravertebral marks to a uniformly colored dorsum.

Comparisons. Tadpoles of Gastrotheca pseustes sensu stricto (in Loja and El Oro provinces) occur in sympatry with those of G. elicioi in the Saraguro region and with G. elicioi , G. lojana , G. psychrophila , and G. turnerorum in the Loja-Abra de Zamora region. Gastrotheca pseustes differs from G. elicioi by lacking a dorsal gray-pigmented fin that abruptly arises from the body; from G. lojana by having a reticulated pattern on flanks, and from G. turnerorum by having a less rounded tail terminus (compare in Fig. 5 ). For G. psychrophila , see remarks under G. elicioi tadpole account.

Vocalization. Four individuals of Gastrotheca pseustes were recorded from three locations in Loja Province (2 individuals from Bosque Washapamba, one from Vía Urdaneta-Tutupali, and 1 from Cerro de Arcos; see Appendix III). Because of the taxonomic problems related to the G. pseuste s complex we decided to use for the present analysis only the recordings obtained from populations situated nearby the type locality, south of the Jubones- Girón river valley in Loja Province (e.g. G. pseustes 1). Descriptive statistics of the acoustic variables are provided in Table 5. The advertisement call of G. pseustes is a complex call, composed of one to five long pulsed notes and followed (or not) by one to six short, single-pulsed notes ( Fig. 23 H–N). The long note had a mean duration of 0.878 s (SD = 0.188) and consisted on average of 32.72 (SD = 6.867) distinct pulses, partly fused, without silent intervals (amplitude modulation close but less than 100%). The amplitude of the long note increases gradually towards the end of the note after which it decreases a little by the end. The short notes had a mean duration of 0.080 s (SD = 0.046) and the inter-note interval is on average of 0.795 s (SD = 0.502). The mean dominant frequency of the call is 1359.0 Hz (SD = 37.981), with a mean 90% bandwidth of 1043.2–1483.4 Hz. The fundamental frequency is usually recognizable; when visible, 6 to 7 harmonics are distinguishable.

Comparisons: The advertisement call of Gastrotheca pseustes is most similar to that of G. yacuri , but G. pseustes has a much longer call duration, longer long notes duration, longer inter-note interval a lower dominant frequency and a lower 90% bandwidth frequency compared with the call of G. yacuri ( Table 5). Also, G. pseustes usually emits 4–6 short notes compared with the only two short notes that G. yacuri emits. The call of G. pseustes can be easily distinguished from that of G. lojana and G. testudinea by the amplitude modulation of the longer note, much longer call duration, lower short note rate, longer long notes duration, longer inter-note interval, larger number of pulses, higher pulse rate, a higher dominant frequency, and higher 90% bandwidth frequency. Also, G. pseustes emits a larger number of long and short notes compared with G. lojana and G. testudinea ( Table 5).

Figures

FIGURE 5. Live tadpoles of: (A) Gastrotheca cuencana (CJ 1945, Stage 37), from Cuenca, Azuay Province, (B) Gastrotheca litonedis (CJ 6813, Stage 37), from Laguna de Busa, San Fernando, Azuay Province, (C) Gastrotheca lojana (CJ 1948, Stage 35), from Oña, Azuay Province, (D) Gastrotheca elicioi (CJ 4312a, Stage 37), from Loja, Loja Province, (E) Gastrotheca turnerorum (CJ 1957, Stage 36), from Laguna Negra de Jimbura, Parque Nacional Yacuri, Loja Province, and (F) Gastrotheca pseustes 1 (CJ 1949, Stage 37), from Chillacocha, El Oro Province. Scales = 3 mm (A–D, F) (E). Photos by LAC (A, C, E) and MAM (B, D).

FIGURE 6. Oral discs of: (A) Gastrotheca cuencana (CJ 1945, Stage 38), from Cuenca (south control), Azuay Province, (B) Gastrotheca litonedis (CJ 5292, Stage 35), from from Laguna de Busa, San Fernando, Azuay Province, (C) Gastrotheca lojana (CJ 4309, Stage 37), from El Tablón, Loja Province, (D) Gastrotheca elicioi (CJ 4311, Stage 36), from Barrio Puntzará Grande, Loja, Loja Province, (E) Gastrotheca turnerorum (CJ 1959, Stage 39), from Laguna Negra de Jimbura, Parque Nacional Yacuri, Loja Province, and (F) Gastrotheca pseustes (CJ 1949, Stage 37), from Chillacocha, El Oro Province. Not to scale. Photos by LAC.

FIGURE 10. Live adults and brooding females of (A) holotype of Gastrotheca litonedis (KU 202690, SVL = 62.4 mm), of (B– C) G. litonedis (D–G) G. pseustes, G is the holotype (KU 203443, SVL = 55.2 mm) from 7.1 km N San Lucas, 2940 m, (H–I) G. elicioi, (J) G. turnerorum, (K) G. cuencana, (L) G. lojana, (M) female G. psycrophila (KU 164233, SVL = 63.5 mm) from 15 km E of Loja, 2850 m, and (N–O) G. yacuri, N is the holotype (CJ 5822, SVL = 57.4 mm). Not to scale. Photos A, G, M by WED; B–F, H–L by LAC, and N–O by PS.

FIGURE 23. Advertisement calls of Gastrotheca yacuri (A–G) and G. pseustes (H–N): (A) oscillogram of three consecutive calls, with the first call composed of two long notes and the next two calls composed of two long and two short notes, (B) oscillogram of a single long note, (C) spectrogram of a single long note, (D) power spectrum of a single long note, (E) oscillogram of a single short note, (F) spectrogram of a single short note, (G) power spectrum of a single short note, (H) oscillogram of two consecutive calls, with the first call composed of one long and five short notes and the next call composed of two long and five short notes, (I) oscillogram of a single long note, (J) spectrogram of a single long note, (K) power spectrum of a single long note, (L) oscillogram of a single short note, (M) spectrogram of a single short note, (N) power spectrum of a single short note. All spectrograms at Hanning window function, 512 bands resolution. See text for details.

FIGURE 33. Localities of known occurrence of Gastrotheca lateonota (red), G. pseustes 1 (green), and G. pseustes 2 (blue). See Appendix II for detailed locality data. Some nearby localities are represented by a single symbol.

FIGURE 34. Metamorph (Stage 46 of Gosner) variation in live Gastrotheca pseustes 1 from Chillacocha, El Oro Province, Ecuador: (A) CJ 1954, (B) QCAZ 45126, (C) CJ 1955, (D) CJ 1953, (E) CJ 1956, and (E) from Chilla–Saraguro (CJ 1956). Not to scale. Photos by LAC.

FIGURE 35. Ontogenetic changes in live Gastrotheca pseustes 1 (CJ 1953) from Chillacocha, El Oro Province, Ecuador. Stages of Gosner: (A) Stage 41, (B) Stage 45, and (C) Stage 46. Scale = 5 mm. Photos by LAC.