Gastrotheca antoniiochoai, Catenazzi, Alessandro & Lehr, Edgar, 2009

Catenazzi, Alessandro & Lehr, Edgar, 2009, The generic allocation of “ Hyla ” antoniiochoai De la Riva & Chaparro, 2005 (Anura), with description of its advertisement call and ecology, Zootaxa 2304, pp. 61-68 : 63-67

Gastrotheca antoniiochoai new combination ( De la Riva & Chaparro, 2005)

( Fig. 1 )

“ Hyla ” antoniiochoai De la Riva & Chaparro, 2005

Holotype. MHNC 0 0 68, a subadult female from near Quebrada Toqoryuoc, Wayqecha Research Center, Kosñipata Valley, Provincia de Paucartambo, Región Cusco, Peru, 13º11’21.0’’S, 71º35’05.5’’W, 2845 m, obtained on 4 March 2003 by Juan Carlos Chaparro.

Additional specimens. MUSM 27944–49, from the Wayqecha Research Center, near the Paucartambo– Shintuya road at 2950 m, 13º11’07.8’’S, 71º35’18.5’’W, obtained on 10 February 2009 by A. Catenazzi, A. Machaca and C. Quispe.

Genus reallocation. We assign “ Hyla ” antoniiochoai to the genus Gastrotheca because it shares with species of that genus the presence of a closed brood pouch, overall morphological similarity, and similar structure of the advertisement call.

Diagnosis. A small species of Gastrotheca characterized by (1) snout-vent length of 26.5 mm in males (n = 2) and 32.5 mm in a single female, tibia length 51.6% of SVL and 108.5% of foot length; (2) interorbital distance about 1.36x larger than width of upper eyelid; (3) skin on dorsum smooth to finely rugose, not coossified with skull, lacking transverse ridges; (4) supraciliary processes absent; (5) heel lacking calcar and tubercles; (6) tympanic annulus smooth; (7) Finger I<II, with discs from 1.1 (Finger I) to 1.6 (Fingers III and IV) wider than digits; (8) fingers unwebbed; (9) webbing extending maximally to point midway between preantepenultimate and antepenultimate subarticular tubercles on Toe IV, to point midway between antepenultimate and penultimate subarticular tubercles on Toe V; (10) in life, dorsum brown to golden tan with dark and green flecks; (11) head markings consisting dorsally of narrow dark flecks along eyelids and laterally of tan stripe extending from nares to posterior end of cilia; (12) pale dorsolateral stripe absent; (13) flanks beige with dark brown flecks; (14) venter gray-brown or beige with minute dark brown spots and diffuse pigmentation; (15) brood pouch paired, lateral.

The reallocation of “ Hyla ” antoniiochoai to Gastrotheca brings the number of Gastrotheca species known from southern Peru, Bolivia and northern Argentina to fourteen ( Duellman & Köhler 2005). The most striking features of G. antoniiochoai are its lateral, paired brood pouch, its small size (<30 mm in males, 32.5 mm in females) and a bromeliad life style. Paired brood pouches are known in only three species of Gastrotheca besides G. antoniiochoai : G. walkeri , G. williamsoni , and G. zeugocystis (Duellman et al. 2004, this paper). Gastrotheca williamsoni (SVL to 54 mm in females, based on the holotype and only known specimen) and G. walkeri (SVL 43.7–47.3 mm in males, 60.3–70.1 mm in females), both from northern Venezuela, are much larger than G. antoniiochoai and have a triangular calcar on the heel (absent in G. antoniiochoai ). Gastrotheca antoniiochoai is most similar to the central Peruvian G. zeugocystis . Both species lack interorbital or T-shaped marks on the dorsum, have unwebbed fingers and basal webbing between Toes III and V. However, G. antoniiochoai is smaller in size than G. zeugocystis (32.5 vs. 37.5 mm in brooding females and 26.8–27.0 vs. 28.2 mm in adult males, n = 1 female and 2 males for G. antoniiochoai , n = 1 female and 1 male for G. zeugocystis ), has Finger I shorter than Finger II (equal in size in G. zeugocystis ) and a relatively longer shank in proportion to SVL (51.6% vs. 46.9%) and to foot length (108.5% vs. 98.3%). None of the other species of Gastrotheca known to occur in the Andes of southern Peru and Bolivia has a lateral, paired brood pouch (see Duellman & Köhler 2005 for a list and comparison of diagnostic traits among these species).

Variation. The two males are smaller than the single female. Both males show well-developed, tan nuptial pads. The three juveniles are like the juvenile paratype by having dark bars on the limbs ( Figure 1 E). Moreover, in juveniles the tan stripe originating from the nares extends dorsolaterally to the midbody (only to the eyes in adults), and increases in width posterior to the tympanum, with an interruption at the point of arm insertion. In all juveniles the iris is reddish-bronze (bronze in adults) with black reticulations, the canthus rostralis is reddish-bronze, and the throat, chest, and belly are white. In adults all ventral surfaces are homogeneously gray-brown or beige with numerous minute black melanophores. The dorsum in one male (MUSM 27945) is pale beige, whereas the other male (MUSM 27948) has a golden-beige dorsum, and the female (MUSM 27949) has a darker, almost brown, dorsum. All adults have minute dark brown and green flecks from the interorbital region posteriorly to the sacral region.

* reported as “head: 8.9 (6.6)” in De la Riva & Chaparro 2005 **reported as “eye length” in De la Riva & Chaparro 2005

Vocalization and notes on reproduction. We analyzed the call of male MUSM 27948 (n = 15 calls, T = 20.0ºC). The advertisement call consisted of a long note 544.8 ± 27.5 ms (range 412–601 ms) in duration with 33.6 ± 1.9 pulses (range 26–38 pulses) and one, two, or three single-pulsed, short secondary notes 21.3 ± 1.8 ms (range 17–22 ms) in duration ( Fig. 2 ). The average call frequency was 32.2 ± 6.4 calls/minute (range 18– 40 calls/minute) and call length was 603.3 ± 70.3 ms (range 377–674 ms). The long note overall had little frequency modulation, and the fundamental frequency ranged between 2544–2968 Hz (median 2915 Hz). The dominant frequency in short notes was 1749–3445 Hz with maximum call energy between 3180 and 3445 Hz (median 3286 Hz). The average interval between long and short notes was 218.0 ± 22.8 ms (range 192–277 ms).

A male (MUSM 27948) and a female (MUSM 27949) were found inside the same bromeliad, and this male repeatedly attempted to mate with the female when placed in the same plastic bag after capture. The female contained six eggs ~ 6.5 mm in diameter in her lateral brood pouches ( Figure 1 C, D). This female was maintained in captivity for several weeks in a bromeliad filled with water, but the eggs slipped out of the pouches and did not complete development. Based on the small number and relatively large diameter of eggs, we suspect this to be a direct-developing Gastrotheca . Direct-developing species usually have fewer than 40 eggs 5–10 mm in diameter, whereas species that deposit tadpoles in water after they hatch usually have more than 70 eggs less than 4 mm in diameter ( Duellman & Köhler 2005; Duellman et al. 2001). This is the second Peruvian Gastrotheca known to possess paired lateral brood pouches; the other is G. zeugocystis (Duellman et al. 2004) .

Distribution and ecology. The species seems to have a patchy distribution in montane scrub and cloud forests between 2800 and 3300 m. The two types were collected at 2845 and 2817 m, but our specimens were captured in bromeliads 6–8 m above the ground in the cloud forest at 2950 m. In addition, we heard the species in cloud forest at 3300 m along the Ericsson trail connecting Acjanaco with Pillahuata, within Manu National Park, on 11 February 2009, and in montane scrub adjacent to our collecting site on 9 February 2009. Therefore, this Gastrotheca occurs in sympatry with G. excubitor throughout its elevational range (albeit G. excubitor becomes rare below 3200 m), and with G. ochoai at the lower end of its elevational range ( Catenazzi & Rodríguez 2001). Of these two species, the first is primarily found in grassland habitats dominated by Stipa ichu (puna) and montane scrub, whereas G. ochoai inhabits montane scrub and cloud forest. Interestingly, G. ochoai is also known to use bromeliads as microhabitats ( Duellman & Fritts 1972), although we never found this species in bromeliads at heights comparable to those used by G. antoniiochoai . Other sympatric frogs include Bryophryne hanssaueri , B. nubilosus , Centrolene sp., Hyloscirtus armatus , Noblella pygmaea , Oreobates lehri , Pristimantis pharangobates , Psychrophrynella usurpator and Telmatobius sp. (Catenazzi et al. 2009, Lehr & Catenazzi 2008, 2009a, b).

Discussion. Immature specimens have limited value for descriptions of species, because the absence of diagnostic characters can lead to supraspecific misallocations. De la Riva & Chaparro (2005) cautioned against introducing “taxonomic confusion” when describing “ Hyla ” antoniiochoai ; unfortunately, given the number of specimens available to them, they erroneously placed the species in Hyla . De la Riva & Chaparro (2005) found “immature white ovarian eggs, developed fat bodies, and undeveloped oviducts” in the holotype and considered the female to be an adult and “probably ready to lay eggs in the following days or weeks”. Because female Gastrotheca are unmistakable when they reach reproductive age (see Figure 1 for a picture of dorsal invagination in G. antoniiochoai ), we disagree with their assessment of the reproductive status and age of the holotype; we consider the holotype to be a subadult female. In support of this conclusion, we found the same color pattern reported in life for the holotype (white throat and chest and reddish-bronze eyes, De la Riva & Chaparro 2005) in all three juvenile specimens studied, but in none of the three adults. The new generic allocation also makes the species less unique with respect to congeners [e.g., vestigial webbing between toes, a character that according to De la Riva & Chaparro (2005) made the species distinct from other Peruvian and Bolivian Hyla ].

Concerning the reproduction of Gastrotheca antoniiochoai , the availability of water in bromeliads might not be necessary to complete its reproductive cycle, because females likely carry eggs until froglets hatch and emerge from the dorsal pouch. Direct development also would be in line with previous findings that in cloud forest Gastrotheca species, embryos complete development and hatch into froglets inside the dorsal brood pouch ( Duellman & Maness 1980; Wassersug & Duellman 1984).

We hypothesize that Gastrotheca antoniiochoai is related to G. zeugocystis , because both species share lateral brood pouches and are similar in general appearance and coloration. Both species inhabit cloud forest at similar elevations (around 2900 m) and use bromeliads as diurnal refuges. Additional research is needed to establish the relationship between these two species. The type localities are separated by 624 km in straight line and by the proposed biogeographic barrier of the deep valley of the Río Apurimac ( Lehr & Catenazzi 2008). This barrier seems to have isolated several anuran clades (e.g., strabomatind frogs), but its effect on the distribution of marsupial frog is presently unknown.

Although not a new description, this proposed new combination, as well as recent work pointing to past misidentification of species and genera in the Kosñipata valley (e.g., De la Riva et al. 2008 for the strabomantid frog Psychrophrynella usurpator ) shows that much work remains to be done to gain a better understanding of anuran diversity in southeastern Peru.

Figures

FIGURE 1. Upper row: Live adult male Gastrotheca antoniiochoai (MUSM 27944, SVL 27.0 mm) in lateral (A), and (B) ventral views; middle row: live adult female Gastrotheca antoniiochoai (MUSM 27949, SVL 32.5 mm) in lateral (C), and ventral (D) views; lower row: juvenile Gastrotheca antoniiochoai (MUSM 27947, SVL 13.4 mm) in lateral (E), and ventral (F) views. Photos by A. Catenazzi.

FIGURE 2. Spectrogram and oscillogram of the advertisement call of Gastrotheca antoniiochoai (MUSM 27948, SVL 26.0 mm) from the Wayqecha Research Station, Paucartambo, Región Cusco. Recorded on 16 February 2009 at 9 h 30, air temperature 20.0 ºC.