Ameerega panguana, Brown & Siu-Ting & May & Twomey & Guillory & Deutsch & Chávez, 2019

Brown, Jason L., Siu-Ting, Karen, May, Rudolf Von, Twomey, Evan, Guillory, Wilson X., Deutsch, Michael S. & Chávez, Germán, 2019, Systematics of the Ameerega rubriventris complex (Anura: Dendrobatidae) with descriptions of two new cryptic species from the East-Andean versant of Peru, Zootaxa 4712 (2), pp. 211-235 : 216-220

Ameerega panguana sp. nov.

Panguana poison frog

Phyllobates pictus (non Bibron): Silverstone 1976 p. 40–41, pattern 5 (partim), Texas Natural History Collections 36469, Río Pachitea near Bosque Nacional de Iparia, Nevati (Kansas University 144351–60, Los Angeles County Museum 92413).

Dendrobates pictus (non Bibron): Myers, Daly & Malkin 1978, p. 332 (by implication).

Ameerega picta ( Schlüter 2005) (by implication).

Ameerega altamazonica: Twomey & Brown 2008 . p. 56–62 (by implication).

Ameerega sp. “Panguana”: Siu Ting 2012. p. 20–22 (by implication); Guillory et al. 2020 p. 3–10.

Holotype. MUSM 26846 (field number KST263 ), an adult male collected by K. Siu Ting, S. Flechas and A. Crawford in Huánuco region, Peru, 4.1 km (via direct line) S of Puerto Inca along Río Pachitea at the Panguana Biological Research Station, 240 m elevation, 9° 36′ 49.3′′ S, 74° 56′ 7.8′′ W, 20 December 2007 ( Fig 4 ).

Paratopotypes. MUSM 26884 (field number KST301 ), collected by K. Siu Ting on 20 January 2008 (Supp. Fig. 1E ) . MUSM 24685–24687 collected between 10–16 November 2003 by W. Hödl, A. Amézquita, K. Siu Ting and A. Lima .

Paratypes. All from Huánuco region, Peru: MUSM 26963–26964 (field numbers JLB07-608 and 610), 11 km E of Puerto Inca along a trail to Cordillera El Sira, 298 m above sea-level, collected 25 April 2007 by E. Twomey and J.L. Brown, 9° 26′ 50.86′′ S, 74° 48′ 1.91′′ W . MUSM 26985 (field numbers JLB07-786 ), 4.5 km S of Puerto Sira along a trail to Cordillera El Sira, collected 3 September 2011 by J. L. Brown. 9° 18′ 44.78′′ S, 74° 51′ 5.83′′ W. AMNH 95663–95666 (field numbers CWM-13104-13107), “Río Llullapichis, nr. Llullapichis (town) on Río Pachitea”, C. Toft and R. L. Dressler, February 1975 (Supp. Fig 3A )

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Etymology. The specific epithet is in honor of the Koepcke family: parents, Drs. Hans-Wilhelm and Maria Koepcke, and their daughter, Dr. Juliane Diller (born as Koepcke). Hans-Wilhelm and Maria founded the Panguana Biological Research Station in 1968, which was named after the undulated tinamou ( Crypturellus undulates ), an inconspicuous, partridge-sized bird. The Koepcke family developed the Panguana Biological Research Station into a paragon for land conservation and biodiversity preservation. Under Juliane’s guidance, the station continues to serve as a cornerstone for biologists working in the Amazon Rainforest of central Peru and has become the country’s oldest biological station. Hans-Wilhelm, Maria, and Juliane also made substantial scientific contributions to the knowledge of Peruvian ornithology, botany, and mammalogy, respectively. On December 24th 1971, Maria and Juliane were passengers on LANSA flight 508. Midflight, the plane was struck by lighting and broke into several pieces, which crashed into the dense rainforests of the upper Pachitea drainage, ca. 120 km south-west of Pucallpa. Despite suffering a broken collar bone, a deep forearm cut, and a severe concussion, Juliane courageously made her way downriver towards the village of Tournavista—a trip that spanned 11 days. She was the sole survivor. The core of the distribution of Ameerega panguana contains the Panguana Biological Research Station, the site of the plane crash, and Juliane’s trek to Río Pachitea.

Definition. A small species of cryptically-colored frog assigned to Ameerega due to the presence of maxillary and premaxillary teeth, the first finger being longer than the second, and basal webbing occurring between toes II–IV. The species can be characterized by the following combination of characters: (1) mean SVL of adult males 19.0 mm (range 16.9–19.7 mm), mean SVL of adult females 19.8 mm (range 16.6–22.1 mm) ( Table 1 ); (2) dorsal skin granular, especially on the back and the dorsal surfaces of the legs, dorsal surfaces of forelimbs lightly granular, flanks and venter non-granular; (3) finger III expanded in adults; (4) absence of lateral fringes and basal webbing on fingers; (5) maxillary and premaxillary teeth present; (6) fingers and toes discs expanded, larger in toes II, III, and IV; (7) basal webbing between toes II–III and III–IV; (8) finger I longer than finger II; (9) toe III length reaches or surpasses the middle of the central sub-articular tubercle of toe IV; (10) metatarsal fold absent; (11) tympanum conspicuous and small; (12) in life, base dorsal coloration of the head, back, and limbs are dark brown mottled in subtle to conspicuous ovoid blotches variable in size and coloration ranging from gray to slate-blue to light olive green to chartreuse yellow; dorsal blotches often merge or are clustered on dorsum; in some individuals the dorsal blotches are mostly absent; (13) oblique lateral stripe absent; (14) usually with white dorsolateral stripes extending from loreal region to groin; (15) white labial stripe present, starting behind nares and ending at forelimb; (16) flanks black to dark brown, most individuals have bright white or cream, occasionally slate-blue, spotting or marbling extending from venter; (17) venter smooth, bright white to bluish-cream, with sparse black reticulation; (18) yellow to red spots present posterodorsally at the insertions of the forelimbs and hindlimbs, and on medial face of tibia; (19) limbs light to dark brown on dorsal surfaces, ventral surfaces of forelimbs are light blue distally, yellow proximally; underside of head pigmented as the venter but often darker (i.e. more black marbling), especially in males. (20) iris dark brown with golden ring around pupil; (21) in preservative, all lighter pigments and flash colors fade to white or gray; (22) advertisement call is a short ‘peep’ repeated 1.1–1.9 times per s for several min; each note is short (0.23 s, mean), with the dominant frequency from 4.9 to 5.5 kHz; (23) presence of exotrophic tadpoles carried to small terrestrial pools, where they are deposited in groups.

Diagnosis. Many Ameerega species possess white dorsolateral stripes and brown dorsal coloration, but only A. hahneli sensu stricto can have a similar white venter. However, A. hahneli has an advertisement call consisting of 6–10 notes per second for several minutes (versus 1–2 notes per second in A. panguana ; Figs. 5 & 6 ), the venter is typical finely marbled (coarsely reticulated in A. panguana ), the dark pigmentation on flanks is broad with venter coloration barely visible from profile (dark pigmentation narrow, ca. width, and venter coloration extends midway up obliques and is distinctly visible in profile in A. panguana ). The second similar species is Ameerega imasmari sp. nov. (described below), in which northern populations are the most similar, but can have golden dorsolateral stripes (white in A. panguana ) an advertisement call consisting of 3–4 notes per second with a dominant frequency 4.3–4.5 kHz (versus 1–2 notes per second with a dominant frequency 4.9–5.5 kHz in A. panguana ; Table 3 , Figs. 5 & 6 ). Other species similar in appearance to A. panguana include A. boliviana , A. ignipedis , A. simulans , A. petersi , A. pulchripecta (all of which have yellowish or green dorsolateral stripes and blue venters), A. picta sensu stricto (can possess a white venter, but has yellow dorsolateral stripes), A. shihuemoy (pink dorsolateral stripe and a blue venter), A. rubriventris (reddish-orange venter) and A. altamazonica (blue venter instead of a white venter in A. panguana ). Ameerega panguana is also similar in appearance to Allobates femoralis , however, it lacks an oblique lateral stripe (present in A. femoralis ) and finger I is longer than or finger II (finger II is longer than or finger I in A. femoralis ).

Measurements of holotype (in mm). SVL 17.3; FoL 7.6; TL 7.9; KK 15.6; FL 6.1; HaL 3.5; HL 4.1; HW 4.5; BW 4.0; UEW 2.9; IOD 2.4; IND 2.3; TD 2.4; ED 2.4; DET 0.5; L1F 2.8; L2F 2.4; W3D 0.5; W3F 0.4. For paratypes see Table 1 .

Description of adults. Little to no sexual dimorphism is apparent except for males being slightly smaller, possessing vocal slits and a subgular vocal sac. Tongue gray, ovoid, attaching anteriorly. Head widest at jaw articulations, slightly narrower than body in most individuals (head width at tympanum 71.3–126.0% of body width at axillae); head width 21.9–31.6% of SVL. Snout sloping laterally; bluntly rounded dorsally; truncate ventrally. Nares situated and directed posterolaterally to the tip of snout; nares visible from front and below but not from above. Canthus rostralis sloped, slightly rounded; loreal region nearly vertical and slightly concave. Interorbital distance nearly same width of superior upper eyelid. Eye large and prominent, with a maximum diameter of 14.9–17.3% of the snout vent length; pupil rounded and horizontally elliptical. Tympanum circular, partially concealed posterodorsally, lacking tympanic annulus; tympanum width 21.7–40.0% of eye diameter. Supratympanic fold absent.

Hands relatively small, length 18.9–29.3% of SVL. Relative length of appressed fingers: III> IV> II ≈ I. Discs moderately expanded, disc on finger III 1.3–1.7 times width of finger below disc. A large, circular outer metacarpal tubercle on median base of palm; a smaller inner metacarpal tubercle on base of finger I; one well developed and prominent subarticular tubercle on fingers I and II, two on fingers III and IV.

Hind limbs relatively small, femur 37.1–50.8% of SVL, tibia 40.7–55.1% of SVL. Relative lengths of appressed toes IV> III> V> II> I; first toe short, barely reaching bottom of subarticular tubercle on base of second toe, with unexpanded disc; toes II and III with barely expanded discs (much smaller than finger discs), and toe IV and V with discs expanded (disc 1.3–1.5 times broader than adjacent phalanx). Inner and a smaller outer metatarsal tubercle present, somewhat protuberant with rounded surfaces. One slightly protuberant subarticular tubercle present on toes I and II, two on toes III, IV, and V. Hands and feet lacking supernumerary tubercles, lateral fringes, and webbing. No toe fringes.

Vocalization. The advertisement call for A. panguana ( Table 1 , Figs. 5 & 6 ) is a short ‘peep’ repeated 1.1–1.9 times per second for several minutes. Each note is short (mean 0.23 s), with the dominant frequency from 4.9–5.5 kHz. This single-note advertisement call is given most frequently in the afternoon and evening as males chorus in small groups. We also note a second call type in A. panguana of two to three notes in quick succession (within 10 ms of each other), repeated once every 3-90 seconds. The latter call appears to function as an aggressive or territorial call and is most frequently heard in the early morning and early evening ( Schlüter 1980).

Distribution and Natural History. Ameerega panguana is distributed throughout the east-Andean versant, Cordillera Sira, and surrounding lowlands of central Peru at elevations of ca. 200–400 m ( Fig. 7 ). This species appears to be widely distributed throughout the region of Huánuco in lower elevations of the Río Pachitea drainage and foothills of Cordillera Sira, extending to both the western and eastern versant. This species is common and can be locally abundant in disturbed forested habitats (locally known as “Purmas”) that surround, or are nearby, small streams, which collectively provide refugia from the midday heat and habitat for reproduction. Ameerega panguana is less commonly found in secondary and old-growth forests. Male A. panguana were frequently observed calling on leaves 0.5-1m above ground. Populations of A. panguana observed at the Panguana Biological Research Station from December to February in 2003 and 2007 were most active between 05:00 to 09:00 and 16:00 to 18:00 (K. Siu- Ting, pers. obs.). This species commonly co-occurs with three other Ameerega species: A. trivittata , A. petersi , and A. hahneli sensu stricto. Ameerega hahneli sensu stricto is more easily detected than A. panguana at most surveyed sites ( Schlüter 1980).

Conservation status. Following the IUCN Red List criteria 3.1 (IUCN 2012), we suggest A. panguana be listed as Vulnerable (VU) under the following criteria: (1) we estimate its extent of occurrence at 9,370 km 2 (as pictured in Fig. 7 ), and part of this range lies in a protected forest (San Matías San Carlos) and two communal reserves (El Sira and Yánesha) and a private concession area (ACP Panguana); (2) it occurs in undisturbed habitat and disturbed areas; (3) population sizes are unknown, but assumed to be large given the abundant forested habitats and tentative large range; (4) populations do not appear to be declining; and (5) demand for the pet trade is presumed to be moderate to low.

Figures

FIGURE 1. Species in the Ameerega rubriventris species complex: A & B) Ameerega altamazonica, C) A. rubriventris dorsal view, D) A. rubriventris ventral view E) Ameerega panguana sp. nov. (photo T. Ostrowski), F) Ameerega imasmari sp. nov. (holotype)

FIGURE 3. Mirror phylogeny of A. rubriventris complex and outgroups. Left. Maximum-likelihood phylogeny reconstruct- ed from UCE genome-scale molecular markers. Right. Maximum-likelihood phylogeny reconstructed from mtDNA genome data (this tree was used a backbone constraint in Fig 2).

FIGURE 4. A–C) Holotype of Ameerega panguana in life (MUSM 26846), SVL=17.3mm. D–E) Holotype of Ameerega imasmari in life (CORBIDI 20575), SVL= 19.9 mm, see Fig. 1 for additional image.

FIGURE 5. Advertisement calls of: A) Ameerega hahneli from Panguana Biological Research Station at 25°C. B) A. rubriventris from type locality, Boqueron de Padre Abad, Peru at 24°C. C) A. altamazonica from type locality, near Tarapoto, Peru at 23°C. D) A. panguana from type locality at 24°C. E) A. imasmari from type locality at 23°C. Solid gray line depicts 5 kHz.

FIGURE 6. Advertisement calls of the A. rubriventris complex. The plot in center depicts the 2D call space occupied by each species with the x-axis representing advertisement call dominant frequency and y-axis representing individual note length (in seconds). Density plots extend from each axis and depict the relative frequency of each species’ values. Letters depict significant differences among taxa (ANOVA: dominant frequency, df=3, F= 22.55, p<0.001; note length, df=3, F= 8.55, p<0.001). Black lines in density plots on each axis depict median, upper-, and lower-quartiles for each species. The isopleths in center plot depict a 2D kernel density estimation of each species’ call space. White dots represent values for A. altamazonica.

FIGURE 7. Known distribution of species in the A. rubriventris complex. Each distribution was created by applying a 20 km buffer to a minimum convex polygon surrounding the known localities of each species. An asterisk indicates samples confirmed with genetic data. Gray dots represent frogs collected as either A. hahneli and A. picta over the past decades; in much of southern Peru it is impossible to positively ascribe these localities to either species based on observation alone. Thus, we have pooled them here to represent the joint distribution of these two similar looking species.