Bioacoustics of Ameerega altamazonica

Remarks on geographic variation. Individuals from near Chazuta closely resemble the individuals from the type locality in both colors and pattern. The Pampa Hermosa population from the west bank of the Ucayali has larger groin spots that are bicolored (orange and yellow). There seems to be a north-south transition in the Huallaga valley from northern frogs having a black dorsum with well-defined dorsolateral stripes to southern populations having a copper-brown dorsum with reduced (and in some cases absent) dorsolateral stripes. The population from near Tocache best demonstrates this shift; this population is described as follows: dorsal skin more granular (compared to conspecific populations to the north), color metallic copper- or rust-brown, dorsolateral stripes absent, pale blue-white labial stripes extending from the corner of the mouth to axillae. Some individuals possess faint tan stripes outlining the snout, though these stripes do not extend posterior past the eyes. In some individuals a faint dorsolateral ridge can be noted separating the dorsum from the flanks. Venter and flank coloration is identical: sky-blue with black reticulation. Bright-orange spots present ventrally under axillae, dorsally over groin, and on medial surface of shanks ( Fig. 2 , middle right and bottom right) Vocalizations. The advertisement call for A. altamazonica ( Fig. 3 ) is a ‘retarded trill’ (following the definitions by Lötters et al. 2003). Notes are repeated at a rate of 1.3–2 notes per second, duration of individual notes ranges from 60–80 ms. Dominant frequency is modulated; notes start at 4100–4300 Hz and end at 4600–4680 Hz. This single-note advertisement call is given most frequently in the evening as males chorus. We also noted a second call type in A. altamazonica consisting of two notes in quick succession (within 10 ms of each other), repeated once every 3–5 seconds. Unlike in the advertisement call, these notes are not frequency-modulated, though the first note is typically lower in frequency than the second by 100–150 Hz. This two-note call appears to function as an aggressive or territorial call and is most frequently heard in the early morning. Schlüter (1980) published spectrographs of A. altamazonica advertisement calls (as Phyllobates pictus ) from the Panguana region of central Peru , which had notes repeated at a rate of twice per second and were frequency modulated. Morales (1992) published a spectrograph of a call from a frog he referred to as Dendrobates sp. 2, which was from Tingo Maria, and has many similarities with the A. altamazonica advertisement call (i.e. 2–3 notes per second, note duration 42 ms). Since he made no mention of ventral coloration of this species, we assume the venter was ‘unremarkable’ (i.e. blue), and since the call did not have notes of alternating frequency (as in A. rubriventris ), we suppose that Morales’ Dendrobates sp. 2 can be referred to A. altamazonica . Lötters et al. (1997) presented advertisement call data for A. hahneli sensu lato from Tarapoto (= A. altamazonica ), noting the similarity to those of A. rubriventris , although the latter species has a call with notes of alternating frequency. The advertisement call of A. altamazonica is easily distinguished from that of A. hahneli sensu stricto , which consists of a train of notes repeated at a rate of 5–9 notes per second, each note with a duration of 11– 18 ms ( Schlüter 1980 , Morales 1992 , Haddad and Martins 1994, De La Riva et al. 1996 , Köhler and Lötters 1999 ). Dominant frequency ranges from 2700–7000 Hz and is not frequency-modulated. Ameerega yungicola , has an advertisement call resembling that of A. hahneli but differs in that it has a lower dominant frequency (3590–3719 Hz), slower repetition rate (4.5-5 notes/second), and longer note duration (31-34 ms) ( Lötters et al. 2005 ). The call of A. altamazonica is similar to the call of A. rubriventris , except the latter species has notes of alternating frequency whereas the former does not. Tadpole (measurements in mm). A stage 30 tadpole (ECU-F 102) was chosen for the description ( Fig. 4 ). It was free-living but species identity was confirmed by sequencing the 16S and cytochrome b gene regions. Total length 19.6, body length 7.2, maximum width 3.3, depth 2.8. Snout rounded when viewed from above; body ovoid and elongate in dorsal view. Eyes black, dorsal but angled laterally, pupils white in preservative. Nares not forming tube, situated half-way between eye and tip of snout, directed dorsally. Spiracle sinistral; vent dextral. Ventral tail fin begins at tail base, dorsal tail fin begins just posterior to plane of vent opening, deepest depth 1.4 measured 1/3 towards distal end. Caudal musculature deepest at tail base, musculature depth 0.77. The mouth is directed anteroventrally. Oral disc emarginate, anterior and posterior labia forming flaps free from body wall. Marginal papillae absent on anterior labium, present in one complete row on posterior labium. Papillae white, rounded; submarginal papillae absent. Jaw sheaths medium in longitudinal width, finely serrate. Anterior jaw sheath has a medial indentation with reduced serration, posterior jaw sheath Vshaped and has serration throughout. Lateral processes long, extending well past lower jaw. Labial tooth row formula is 2(2)/3. A-1 complete, A-2 with medial gap, same width as A-1. P-1, P-2, and P-3 complete; P-1 and P-2 equal width, P-3 shorter. In preservative, the head appears dark gray due to subdermal pigmentation. Dermal pigmentation on dorsum is uniform translucent white with small black melanophores. Ventral coloration is translucent gray; under a dissecting microscope the ventral skin appears white with large black melanophores concentrated around anterior half of body and over intestinal coils. Tail musculature white, fins white, melanophores are present in small, irregular clusters along length of tail. Life color was dark gray or black with two distinct white spots lateral to the mouth. While these spots are also present in other species (such as the sympatric A. bassleri ), in A. altamazonica the spots extend back almost to the eye; in other species the spots extend back only to the level of the nares. Two additional stage 30 A. altamazonica tadpoles (ECU-F 103, 104) were examined and agree with this description. Our examinations of A. hahneli tadpoles note the following differences from A. altamazonica : (1) dorsal and ventral skin (in preservative) uniform black with white marbling on rump and snout (versus translucent skin with black melanophores in A. altamazonica ), (2) lateral edges of anterior labium not forming free-flap (versus flap distinctly free from body wall in A. altamazonica ), (3) marginal papillae on posterior labium conspicuously large and somewhat pointed (versus reduced and rounded posterior marginal papillae in A. altamazonica ), (4) keratin on all three posterior labial tooth rows reduced or absent (versus present in A. altamazonica ), and (5) tail heavily mottled (versus white with irregular melanophore clusters in A. altamazonica ). Our examination of two A. hahneli tadpoles from Iquitos (ECU-F 105, 106) agrees well with the description by Haddad and Martins (1994) of an individual from Presidente Figueiredo, Brazil . The tadpole of A. altamazonica appears to be similar to that of A. rubriventris based on the sketches and description by Lötters et al. (1997) . Mouthpart formulas are identical in the two species, but the tadpole shape is slightly different in that A. rubriventris larvae are more elongate and have a slightly upturned tail near the tip.

Etymology. The specific epithet is composed of the Latin adjective ‘ altus’, meaning ‘high’, and the Spanish adjective ‘ Amazónica ’, meaning ‘pertaining to the Amazon’. Combined to signify ‘upper-Amazonian’, referring to the species’ distribution, being known from the upper Río Huallaga and Ucayali drainages, both major headwaters of Río Amazonas. Definition and diagnosis. A small species of Ameerega with an adult SVL of approximately 18–25 mm . Dorsal skin granular, black or brown, usually with white dorsolateral stripes extending from loreal region to groin. Yellow or orange spots present above groin, under axillae, and on shanks. White labial stripe present starting behind nares and ending at forelimb. Tadpole dark brown with large white spots lateral to mouth. The combination of white dorsolateral stripes and a blue venter with black marbling distinguish A. altamazonica from the multitude of Ameerega species possessing one but not both of these characteristics. Ameerega yungicola and A. hahneli sensu stricto are the only other species of Ameerega possessing both these characters. Ameerega yungicola has maxillary teeth (teeth absent in A. altamazonica ), red (versus orange or yellow in A. altamazonica ) flash marks, and an advertisement call consisting of 4.5–5.0 notes per second with a dominant frequency of 3590-3719 Hz (versus 2–3 notes per second with a dominant frequency of 4300– 5140 Hz in A. altamazonica ) . Ameerega hahneli sensu stricto is morphologically most similar to the new species but has an advertisement call consisting of 6–10 notes per second for several minutes. Its tadpole has enlarged and pointed (versus reduced and rounded in A. altamazonica ) marginal papillae on the posterior labium. Other species similar in appearance to A. altamazonica include A. boliviana , A. picta sensu stricto , A. petersi , A. pulchripectus , (all of which have yellowish or green dorsolateral stripes), and A. rubriventris (which has a reddish-orange venter instead of a blue venter in A. altamazonica ). The last mentioned species is the sister taxon to A. altamazonica , genetically distinct on the basis of 24 unambiguous nucleotide substitutions.

Ameerega altamazonica may serve as a (Batesian?) mimetic model for two species of Allobates with which it occurs sympatrically. Though we have no toxin information data on A. altamazonica , we suspect that it is ‘mildly toxic’ like other species of semi-aposematic Ameerega (see Summers and Clough 2001 ). In some areas of northern San Martín, A. altamazonica is sympatric with Allobates femoralis sensu lato , a complex of weakly- or non-toxic species which (here) share a similar pattern of a black dorsum and white dorsolateral stripes. In the central Huallaga valley, A. altamazonica is sympatric with an undescribed species in the Allobates femoralis complex (identifiable by a distinct advertisement call), which has a copper-brown dorsum and closely resembles the local A. altamazonica . Ameerega altamazonica may at the same time be a Müllerian mimic with the sympatric A. hahneli sensu stricto . Also, the possibility exists that a black dorsum with white dorsolateral stripes is an ancestral state in Ameerega and does not have any mimetic function in these two species. Conservation status. Following the IUCN Red List criteria (IUCN 2001), we suggest A. altamazonica be listed as Least Concern (LC) under the following criteria: (1) we estimate its area of occupancy at 48,300 km 2, and part of this range lies within two National Parks (Río Abiseo and Cordillera Azul), (2) it occurs extensively throughout suitable habitat and thrives even in disturbed areas, (3) population sizes are assumed to be large since it is common in several habitat types , (4) populations do not appear to be declining, and (5) demand for the pet trade is presumed to be low.