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ISSN 1175-5326 (print edition)

Copyright © 2009 · Magnolia Press

ISSN 1175-5334 (online edition)

ZOOTAXA

Redescription of Allobates brunneus (Cope) 1887 (Anura: Aromobatidae: Allobatinae), with a description of the tadpole, call, and reproductive behavior ALBERTINA P. LIMA1, JANALEE P. CALDWELL2,4 & CHRISTINE STRUSSMANN3 1 Coordenação de Pesquisas em Ecologia, Instituto Nacional de Pesquisas da Amazônia, Av. André Araujo 2936, 69011-970, Manaus, Amazonas, Brazil. E-mail: [email protected] 2 Sam Noble Oklahoma Museum of Natural History and Department of Zoology, University of Oklahoma, Norman, Oklahoma 73072, USA. E-mail: [email protected] 3 Departamento de Ciências Básicas e Produção Animal, Faculdade de Agronomia e Medicina Veterinária, Universidade Federal de Mato Grosso, Av. Fernando Correia da Costa s/n, 78060-900, Cuiabá, Mato Grosso, Brazil. E-mail: [email protected] 4 Corresponding author

Abstract Allobates brunneus, long known as Colostethus brunneus, was originally described by E. D. Cope in 1887. Specimens on which the original description was based were collected by H. H. Smith from the village of Chapada dos Guimarães, in the state of Mato Grosso, Brazil. Because of the brevity of the original description, new material of this species was collected from 1998–2001 for a redescription. In recent years, numerous undescribed species of Allobates have been identified throughout the Amazon region. Our redescription of A. brunneus includes many characters not given in the original description that are necessary to distinguish this species from other similar ones. We also include descriptions of the tadpole and vocalization. Allobates brunneus is a small frog, in which males range in snout–vent length from 14.8–18.3 mm, and females from 15.8–19.8 mm. The species typically inhabits swamp forests along small streams or rivers. Although the frog was once abundant, the construction of a hydroelectric dam and reservoir on the Rio Manso has inundated many of the localities where it was formerly known, greatly reducing the number of known populations. Key words: brunneus, Colostethus, Allobates, Dendrobatidae, Aromobatidae, Mato Grosso, Brazil

Resumo Allobates brunneus, que foi referida na literatura como Colostethus brunneus, foi originalmente descrita por E. D. Cope em 1887. Os espécimes sobre os quais baseou-se a descrição original foram coletados por H. H. Smith no vilarejo de Chapada dos Guimarães, no estado de Mato Grosso, Brasil. Tendo em vista a escassez de informações na descrição original, material adicional da espécie foi obtido entre 1998–2001, visando sua redescrição. Em anos recentes, numerosas espécies de Allobates ainda não descritas têm sido registradas em toda a Amazônia. Nossa redescrição de A. brunneus inclui diversos caracteres não fornecidos na descrição original, necessários para distinguir esta espécie de formas congenéricas semelhantes. Nós também incluímos uma descrição de seus girinos e da vocalização. Allobates brunneus é um anuro pequeno, cujo comprimento rostro cloacal varia de 14.8–18.3 mm em machos e de 15.8–19.8 mm, em fêmeas.. Indivíduos da espécie habitam florestas sazonalmente inundáveis ao longo de pequenos córregos e rios. As populações desse anuro, outrora abundante em sua área de ocorrência, parecem ter sido bastante reduzidas devido à perda de hábitats decorrente da construção de uma hidrelétrica e formação de um reservatório de grandes proporções no rio Manso, o qual inundou a maior parte das localidades onde a espécie havia sido detectada antes da construção do empreendimento.

Accepted by M. Vences: 22 Oct. 2008; published: 27 Jan. 2009

1

Introduction Allobates brunneus was originally described in 1887 by Edward Drinker Cope as Prostherapis brunneus. The frogs on which the description was based were collected by Herbert Huntington Smith during an expedition referred to as the Naturalist Brazilian Exploring Expedition. Smith traveled to Mato Grosso, Brazil, where he took up residence in the village of Chapada (incorrectly spelled as Chupada and now known as Chapada dos Guimarães), described as 30 miles northeast of Cuyabá (now known as Cuiabá) (Cope 1887). Cope noted that the specimens collected during this expedition were obtained at or near the village then known as Chapada. We were thus confident that we were returning to the type locality of this species as nearly as could be determined from the original description. At the time of the discovery of A. brunneus, it was common for authors to provide only brief descriptions. Thus, the original description gives the condition of only a few morphological characters, provides only a brief color description, and includes eight measurements of the frog (Cope 1887). A holotype was not designated, but 21 syntypes are present in the collection of the Academy of Natural Sciences of Philadelphia (ANSP 11241–61) (Malnate 1971). Edwards (1974a) examined these syntypes and concluded that their poor condition precluded comparison with material he had at hand. Edwards (1974a) provided a comparison of two topotypes of A. brunneus from University of Kansas Natural History of Museum (KU 93154–55) with the holotype of another Allobates (intermedius, now kingsburyi) and ultimately concluded that these two species are distinct. Morales (2002 “2000”) provided information on 12 characters and a stylized drawing of A. brunneus, based partly on the syntypes. Allobates brunneus and other closely related frogs were long considered to be dendrobatids in the genus Colostethus (sensu lato). A recent revision of dendrobatid frogs (now numbering about 245 species) confirmed that “Colostethus” was a paraphyletic group with genera in two families (Grant et al. 2006). As currently recognized, Allobates consists of 44 species, most of which are Amazonian in distribution. Allobates is grouped with Aromobates and Mannophryne in the family Aromobatidae (Grant et al. 2006). Our purpose in redescribing A. brunneus is to provide a more complete understanding of the morphology of this frog, including a description of the tadpole and the vocalization. Because this species was one of the first to be described from Brazil (Cope 1887), a detailed description will allow us and future workers to determine the limits of its distribution and to distinguish it from the many other similar species in this group, both described and undescribed. In light of current concern about declines of amphibian populations (Stuart et al. 2004; Pimenta et al. 2005), we provide a comment on the apparent current status of A. brunneus based on recent observations. One of us (CS) resides in the area and has conducted studies on the herpetofauna of the region for many years.

Material and methods Our work was conducted in the Brazilian state of Mato Grosso in the municipality of Chapada dos Guimarães, at 9 localities northeast of the town of Chapada dos Guimarães. These sites were located as near the type locality as possible. Specimens were obtained and observations on reproductive behavior were made from 14–19 December 2001 along an unpaved road from about 20–34 km north of Chapada dos Guimarães, at elevations from 360 to 380 m. Frogs were found along slow-moving streams, one called Ribeirão Invernada (15°16'00" S, 55°31' 52" W) and two that are unnamed (15°16'22" S, 55°34' 49" W; 15°14'31" S, 55°29'31" W). All these streams are small tributaries of Rio Casca, which flows into the left side of Rio Manso, which in turn is the main tributary of Rio Cuiabá and ultimately part of the upper Rio Paraguai basin.

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Additional observations were made and specimens collected approximately 55 km north of Chapada dos Guimarães, elevation about 297 m, in October and November 1998 and in January and March 1999. This work was done in similar forested areas, along banks of the slow-moving Rio Casca (14°56'45" S, 55°44' 33" W; 14°56'56" S, 55°44'52" W; 14°57'15" S, 55°42'33" W; 14°57'23" S, 55°41'41" W; 14°57'47" S, 55°41'31" W) where it conjoins with Rio Quilombo (14°57'23" S, 55°43'00" W). Since that work was completed, some of these study areas have been flooded by a reservoir constructed as part of the Manso Hydroelectrical Plant project. Thirty-eight adult specimens (20 males and 18 females) and 46 tadpoles of Allobates brunneus were collected. Adults and tadpoles were killed in a solution of lidocaine hydrochloride and epinephrine. Adults were fixed in 10% formalin for 72 hours and transferred to 70% ethanol for permanent storage. Specimens were deposited in the Herpetology Collection of the Instituto Nacional de Pesquisas da Amazônia (INPA) in Manaus, Brazil (Females, INPA-H 10111, 10114, 10116–19, 10121, 10123, 10125, 10127–29, 10131, 10133, 10140, 10143–44, 10146. Males, INPA-H 10112–13, 10115, 10120, 10122, 10124, 10126, 10130, 10132, 10134–39, 10141–42, 10145, 10147–48. Tadpoles were preserved in 10% formalin. Color in life is described from field notes and digital photographs of A. P. Lima. Sex was confirmed by dissection or presence of vocal slits. Color photographs and recordings of calls can be obtained from the Programa de Pesquisa em Biodiversidade website http://ppbio.inpa.gov.br/Port/acervo/amphibia/abrunneus/. Abbreviations and definitions of measurements for adults follow Caldwell & Lima (2003) and Grant et al. (2006). Measurements of adults and tadpoles were taken with digital calipers to the nearest 0.01 mm, or with a grid calibrated for the objective lens (nearest 0.01 mm) of a stereomicroscope. The following adult measurements were taken: 1) snout vent-length (SVL); 2) head length from the corner of mouth to tip of snout (HL); 3) head width at angle of jaws (HW); 4) snout length from anterior corner of eye to tip of snout (SL); 5) eye–nostril distance from anterior corner of eye to center of nostril (EN); 6) internarial distance (IN); 7) eye length from anterior to posterior corner (EL); 8) interorbital distance (IO); 9) diameter of tympanum (TYM); 10) forearm length from proximal edge of palmar tubercle to outer edge of flexed elbow (FAL); 11) hand length from proximal edge of palmar tubercle to tip of finger III (HAND III); 12) width of disc on finger III (WFD); 13) tibia length from outer edge of flexed knee to heel (TL); 14) foot length from proximal edge of outer metatarsal tubercle to tip of toe IV (FL); and 15) width of disc on toe IV (WTD). In addition, we measured the following: 16) length from proximal edge of palmar tubercle to tip of finger I (HAND I); 17) length from proximal edge of palmar tubercle to tip of finger II (HAND II); 18) length from proximal edge of palmar tubercle to tip of finger IV (HAND IV); and 19) arm length from the insertion with the body to outer edge of flexed elbow (AL). We used the distances from the base of the proximal edge of the palmar tubercle to the tips of each finger to compare length of fingers (Kaplan 1997) because it is difficult to determine the intersection of the palm and the finger for some fingers (Grant et al., 2006). A total of 46 tadpoles in 15 lots were used for descriptions (INPA-H 10025–10027, 10029–10030, 10032–10037, 10039, 10041, 10043, and 10044). The tadpoles were taken from the backs of one male and from three clutches found in the field and were raised to obtain a series of specimens. Those individuals were collected in December and preserved 30 December 2001 (INPA-H 10033, 10036, 10039), 03 January 2002 (INPA-H 10030), 05 January 2002 (INPA-H 10025, 10034, 10037), 14 January 2002 (INPA-H 10026, 10035), 20 January 2002 (INPA-H 10029, 10041, 10043, 10044), 31 January 2002 (INPA-H 10032), and 02 February 2002 (INPA-H 10027). Four groups of tadpoles of A. brunneus were reared in 40 x 60 x 10-cm plastic basins in a heavily vegetated suburban backyard in Manaus. Soil and leaf litter collected from margins of pools where A. brunneus was found provided substrate for the basins. We gave rabbit chow as a supplementary food source. Color in life was described from field notes of APL; color in preserved tadpoles was described from tadpoles in INPA-H 10043. Developmental stages of tadpoles were determined using Gosner's (1960) key. Terminology, diagnostic characters, and measurements follow Altig & McDiarmid (1999). We recorded the following tadpole mea-

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surements: 1) total length from tip of tail to tip of snout (TL); 2) body length from tip of snout to body–tail insertion (BL); 3) tail length from tip of tail to body–tail insertion (TAL); 4) body width at level of spiracle (BW); 5) body height at level of spiracle (BH); 6) width of head at level of the eyes (HWLE); 7) tail musculature, maximum width (TMW); 8) maximum tail height (MTH); 9) tail musculature, maximum height (TMH); 10) interorbital distance (IOD); and 11) internarial distance (IND). The calls of 8 males were recorded from 16 to 18 December 2001 at temperatures varying from 25.5 to 29.0 C. Calls were recorded using a Sony WM-D6C tape recorder and an AKG D-190-E microphone. We recorded 3 min of consecutive advertisement calls with the microphone positioned 90–100 cm in front of the frog. Tape recordings were digitized at 10 kHz, and spectral parameters of the calls were analyzed (Window type: Blackman; DFT size: 2048 samples; 3dB filter bandwidth: 20 Hz; Hot size: 16.4) with Raven 1.2 software (Charif et al. 2004). Each 3-min call was described by its temporal (note duration, inter-note interval, the silent interval between calls, and call duration) and spectral (maximum, highest, and lowest frequency) parameters. Upper and lower frequencies were measured at 20 dB below the peak intensity, the value at which the signal energy could still be clearly distinguished from background noise in our recordings. Results Redescription of Allobates brunneus (Figures 1–2) Adult definition and diagnosis: A small-sized Allobates (mean adult male SVL 16.7 mm; mean adult female SVL 18.3 mm); dorsum granular, heaviest posteriorly; Finger I slightly longer than Finger II, Finger II longer than Finger IV; Finger III on males not swollen (Fig. 3A). Dorsolateral stripe absent in both sexes; ventrolateral stripes absent in preserved specimens, present in life; oblique lateral stripe present but diffuse (Figs. 1C and 1F; Figs. 2A, 2B, and 2C); finger discs expanded; no webbing on hands (Fig. 3A); lateral fringes on fingers and toes absent (Figs. 2A and B); basal webbing present between Toes II and III and Toes III and IV (Fig. 3B); median lingual process absent (Grant et al. 1997); black arm-band absent (Grant & Castro 1998); white (unpigmented) testes extending half the length of the kidney; mature oocytes pigmented; teeth imperceptible under microscope at 50X magnification. Comparison with other species: Forty-four species are currently placed in the genus Allobates, many of which are known only from the vicinity of their type localities or have restricted ranges. We distinguish A. brunneus from other species that occur in the Amazon region of Brazil or in southern Brazil. Allobates brunneus has a distinct dark hourglass pattern on the dorsum, which distinguishes it from A. caeruleodactylus (Lima & Caldwell 2001), A. conspicuus (Morales 2002 “2000”), A. fuscellus (Morales 2002 “2000”), A. marchesianus (Melin 1941; Caldwell et al. 2002b), A. masniger (Morales 2002 “2000”), A. nidicola (Caldwell & Lima 2003), A. subfolionidificans (Lima et al. 2007), A. sumtuosus (Morales 2002 “2000”), and A. vanzolinius (Morales 2002 “2000”), all of which have plain dorsa. It is distinguished from two other Amazonian species of Allobates that have hourglass patterns on the dorsum by the following characters: A. crombiei has Fingers II and IV equal in length, a distinct dorsolateral stripe, no oblique lateral or ventrolateral stripes, and throat dark gray in males (Morales 2002 “2000”); A. gasconi is smaller than A. brunneus, dorsolateral and ventrolateral stripes are present, oblique lateral stripe is absent, and males have a swollen third finger and gray throat (Morales 2002 “2000”). Allobates olfersioides (including synonyms A. alagoanus, A. capixaba and A carioca; Lutz 1925; Verdade & Rodrigues 2007) differs from A. brunneus in having a pattern of intercrossing Xs on the dorsum (dark hourglass pattern in A. brunneus) and no oblique lateral stripe (diffuse oblique lateral stripe extending from groin to near midbody in A. brunneus). Adult description: Females are slightly larger than males (Table 1). Average female SVL is 1.5 mm greater than male SVL, but males have relatively wider heads [head wider than long; male HW 39% of SVL

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in males, 37% of SVL in females (t = 2.8, df = 36, P = 0.005)]. Snout blunt, broadly rounded to nearly truncate in dorsal view (Figs. 1A and 1D) and acutely rounded in lateral view (Figs. 1C and 1F), extending past lower jaw (Figs. 1B and 1E). Male SL 46% and female SL 47% of HL; IN in males and females 38% of HW; EN in males 74% and in females 73% of HW; tympanic membrane inconspicuous, round, TYM 46% of EL in both sexes; posterodorsal part of tympanum partially concealed by slip of m. depressor mandibulae; tongue attached anteriorly, longer than wide, slightly rounded posteriorly, median lingual process absent; teeth on premaxilla and maxilla imperceptible under light microscope at 50X magnification; dorsal skin granular, heavier posteriorly; dorsolateral stripe absent; ventrolateral stripe present in life, absent in preserved specimens; oblique lateral stripe present, consisting of a broad, diffuse area that interrupts the lateral dark brown band in several positions, most obvious from groin to midbody but extending to forearm in some specimens (Figs. 1 and 2). TABLE 1. Measurements (in mm) of adult males and females of Allobates brunneus collected from near the type locality. Abbreviations are defined in the text. Values are means ± standard deviation; maximum and minimum values are in parentheses. Character

Male (n = 20)

Female (n = 18)

SVL

16.7 ± 0.8 (14.8–18.3)

18.3 ± 1.2 (15.8–19.8)

HL

4.6 ± 0.2 (42.2–5.0)

5.0 ± 0.4 (4.2–5.6)

HW

6.5 ± 0.5 (5.6–7.0)

6.8 ± 0.4 (5.7–7.3)

SL

2.1 ± 0.2 (1.8–2.3)

2.4 ± 0.2 (1.9–2.7)

EN

1.6 ± 1.0 (1.4–1.7)

1.7 ± 0.1 (1.5–1.8)

IN

2.4 ± 1.0 (2.3–2.7)

2.6 ± 0.1 (2.3–2.9)

EL

2.1 ± 0.2 (1.9–2.5)

2.3 ± 0.2 (2.0–2.6)

IOD

5.1 ± 0.3 (4.6–5.7)

5.5 ± 0.3 (5.0–6.0)

TYM

1.0 ± 0.1 (0.8–1.1)

1.0 ± 0.1 (0.9–1.2)

FAL

4.0 ± 0.3 (3.3–4.5)

4.1 ± 0.2 (3.7–4.5)

HAND I

3.3 ± 0.33 (2.6–4.1)

3.3 ± 0.2 (2.9–3.7)

HAND II

3.1 ± 0.3 (2.2–3.4)

3.2 ± 0.2 (2.9–3.6)

HAND III

4.2 ± 0.4 (3.2–4.7)

4.4 ± 0.3 (3.7–5.0)

HAND IV

2.8 ± 0.1 (2.6–3.0)

2.9 ± 0.2 (2.6–3.1)

WFD

0.5 ± 0.1 (0.4–0.6)

0.6 ± 0.1 (0.4–0.7)

FL

7.9 ± 0.5 (6.8–8.7)

8.1 ± 0.5 (7.4–9.2)

WTD

0.7 ± 0.1 (0.5–0.8)

0.7 ± 0.1 (0.6–0.8)

TIL

8.6 ± 0.5 (7.8–9.6)

9.0 ± 0.2 (8.5–9.7)

AL

3.7 ± 0.3 (3.2–4.2)

3.9 ± 0.3 (3.5–4.3)

Forearm slightly longer than upper arm; ulnar fold absent; HAND III length in males 19.5% and females 18.4% of SVL; Finger I slightly longer than Finger II when fingers appressed; Finger III>I>II>IV (Fig. 3A); finger webbing absent; palmar tubercle nearly round, diameter 0.65 ± 0.08 mm in females, 0.56 ± 0.06 mm in males, 14.1% of HL in both sexes; thenar tubercle elliptic, one-third diameter of palmar tubercle (Fig. 3A); one subarticular tubercle present on Fingers I, II, and IV, two subarticular tubercles present on Finger III (Fig. 3A); basal subarticular tubercles on Fingers I and II largest, nearly equal in size, basal subarticular tubercle on finger IV very small; basal and distal subarticular tubercle on Finger III smaller, subequal. No fringes on fingers; all discs on fingers expanded; Finger III not swollen, width of disc on Finger III 0.55 mm, disc 62% wider than width of finger (hand characters in Fig. 3A).

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FIGURE 1. Dorsal (A), ventral (B), and lateral (C) view of male Allobates brunneus, INPA-H 10139; and dorsal (D), ventral (E), and lateral (F) view of female INPA-H 10119 in preservative.

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FIGURE 2. Dorsal views of males (A, B, and C) and females (D and E), showing variation in the dorsal patterns. (F) Ventral views of female (left) and male (right) in life showing the white throat in the female and the yellow throat in the male. (Photographs by A.P. Lima)

Hindlimbs robust; TL 50.4 % of SVL. Ratio of foot length to SVL in males (mean 0.47 ± 0.02 mm) significantly greater than in females (mean 0.45 ± 0.03 mm; t = 3.05, df = 36, P = 0.005); foot length 45% of SVL in males and 47% in females; relative length of toes IV>III>V>II>I; basal webbing between Toes III and IV present in all specimens; rudimentary webbing present between Toes III and IV only in 5 of 38 specimens; lateral fringes absent on all toes; Toe I reaching distal edge of subarticular tubercle of Toe II when appressed; REDESCRIPTION OF ALLOBATES BRUNNEUS

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discs on Toes I, II, III, and IV larger than adjacent phalanges; disc on Toe V nearly same width of phalanges; width of disc on toe IV 0.68 mm in adults; inner metatarsal tubercle oval; outer metatarsal tubercle round; medial metatarsal tubercle absent; metatarsal fold weak, present in 33 and absent in 5 specimens; tarsal keel distinct, short and curved; one subarticular tubercle on Toes I and II; two on Toes III and V; Toe IV with three subarticular tubercles, basal subarticular tubercle poorly defined in 33 and absent in 5 specimens (foot characters in Fig. 3B).

FIGURE 3. Ventral view of hand (A) and foot (B) of Allobates brunneus male INPA-H 10139.

Color in life: Ground color of dorsum generally varies from light grayish brown to orange brown with one to three dark brown, sometimes diffuse, triangular, diamond, or hourglass markings from between the orbits extending to the sacral region (Fig. 2A–2C). Upper surface of arm light orange-brown; upper surfaces of legs light gray with dark brown transverse bands on thigh, shank and foot in most specimens. Adult males with greenish-yellow throats with melanophores evenly dispersed on vocal sac; chest and belly lemon yellow to light lemon yellow; adult females yellow on outer edge of throat becoming white on central part of throat, blending with white chest and belly (Fig. 2D). Flank and undersurface of thigh greenish yellow; undersurface of leg and foot light gray; lower surface of arm light brown. Dorsolateral stripe absent; oblique lateral stripe pale tan to light orange brown, forming diffuse area variously extending from groin to midbody or sometimes to arm insertion; ventrolateral stripe consisting of a series of irregular, elongate white spots, extending from the anterior corner of eye to groin. Upper part of iris and pupil ring metallic gold with fine black reticulations; remainder of iris brown. Color in preservative: Ground color of dorsum uniform light brown with 1 to 3 chocolate brown triangular, diamond-shaped, or hourglass markings extending from between the orbits to the sacral region (Figs. 1A and 1D); upper surface of arms cream to yellowish in 35 specimens, brown in 3; posterior surfaces of arms and legs light brown with dark brown flecks. In 35 specimens, upper surfaces of leg light brown with a dark brown band on thigh, shank, and foot; in 3 specimens these bands diffuse. Dark brown band extending from the snout laterally around the body, to midbody in 35 specimens, or nearly to arm insertion in 3 specimens;

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this lateral dark brown band narrows before and after eye. Ventrolateral stripe not visible in preserved specimens; pale oblique lateral stripe interrupts lateral dark brown band at midbody in 32 specimens; in 6 specimens it consists of diffuse pale cream spots imbedded in the dark brown lateral band at level of groin (Fig. 1C and 1F, 2A–2C). Flank, belly, and upper lip plain white or very light yellow; adult male throat cream to yellowish with rows of spots formed by melanophores around lips; widely dispersed melanophores visible only under microscope on remainder of throat; chest and belly cream to yellowish (Fig. 1B). Female throat, chest, and belly cream (Fig. 1E); palms of hands and soles of feet brown; paracloacal mark absent (Fig. 1A–1F).

FIGURE 4. Waveform and spectrogram of one series of advertisement calls showing pulsed calls in groups (A) and continuous calls (B) of the advertisement call of Allobates brunneus (INPA-H 10). Indistinct harmonics can be seen in both types of calls.

Advertisement call Variation in environmental temperature can influence temporal features of advertisement calls (Ryan 1988; Gerhardt & Huber 2002). Temperature affected the temporal parameters of calls of Allobates brunneus. At temperatures above 28 C, males emitted notes in groups of 6 to 11. At temperatures below 27 C, the notes were not grouped, and the intervals between notes were not consistent throughout the 3-min recording. Call characteristics in temporal parameters: The calls of two males were recorded at temperatures above 28 C. These males emitted sequences of notes in groups of 6–11 notes separated by longer silent intervals (Fig. 4A). The notes within each sequence were separated by uniform intervals (Table 2). For these two individuals, the number of notes produced per minute was 47 and 48, and the number of sequences was 17 and

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19 per 3-min section. Thirty-four and 35 notes and inter-note intervals (2 per pulsed call) per male were measured per 3-min period. The mean note duration for the 2 males was 0.043 ± 0.007 and varied from 0.032 to 0.060 s. The inter-note intervals within sequences had a mean of 0.32 ± 0.05 s and a range of 0.24 to 0.44 s. The mean sequence duration was 2.7 ± 0.66 s, and varied from 1.7 to 4.2 s. The mean duration of intersequence silent intervals was 6.7 ± 2.6 s and varied from 2.8 to 13.1 s. TABLE 2. Mesasurements of acoustic parameters for male Allobates brunneus. Values for temporal parameters are means ± standard deviation; range in parentheses. Values of maximum frequency are median; lower and upper quartiles in parentheses. Individual INPA-H

Call duration (sec)

Interval between calls (sec)

Note duration (sec)

Interval between notes (sec)

10116-g2

3.12 ± 0.72 (1.68–4.18)

5.23 ± 1.61 (2.82–9.20)

0.039 ± 0.004 (0.032–0.051)

0.359 ± 0.041 (0.277–0.441)

10139-g1

2.35 ± 0.31 (1.92–3.06)

8.37 ± 2.51 (5.23–13.05)

0.047 ± 0.006 (0.032–0.06)

0.284 ± 0.039 (0.245–0.441)

10122-g8

------

------

0.045 ± 0.005 (0.034–0.057)

1.474 ± 2.057 (0.199–8.243)

10135-g5

------

------

0.045 ± 0.003 (0.037–0.049)

0.950 ± 1.105 (0.211–5.189)

10138-g7

------

------

0.053 ± 0.008 (0.039–0.065)

0.780 ± 0.797 (0.181–4.148)

10141-g4

------

------

0.044 ± 0.005 (0.037–0.055)

0.482 ± 0.312 (0.218–1.534)

10146-g3

------

------

0.042 ± 0.004 (0.029–0.054)

0.725 ± 0.622 (0.249–3.241)

10147-g6

------

------

0.051 ± 0.006 (0.039–0.068)

1.296 ± 1.269 (0.213–4.562)

Individual INPA-H

Number of notes/1 min

Maximum frequency (kHz)

Air temperature (oC)

Time of recording

10116-g2

56

4.85 (4.83–4.88)

28.1

16:30

10139-g1

46

4.88 (4.78–4.94)

29.0

14:30

10122-g8

66

5.12 (4.87–5.14)

25.5

17:30

10135-g5

138

5.367 (5.35–5.37)

26.4

18:30

10138-g7

115

5.04 (5.02–5.04)

25.5

17:01

10141-g4

126

5.48 (5.47–5.53)

26.5

17:51

10146-g3

106

4.74 (4.70–4.75)

26.6

17:10

10147-g6

35–56

4.95 (4.90–5.05)

26.0

18:53

continued.

At temperatures below 27 C, males did not emit sequences of notes, and the intervals between notes varied throughout the 3-min recording (Fig. 4B). The calls of six males were recorded at temperatures below 27 C. The mean number of notes produced per 1-min section was 110 ± 25, and varied from 66 to 138. Forty-one to 50 notes and inter-note intervals per male were measured per 3-min period. Notes and inter-note intervals were selected in intervals of 4 s throughout the 3-min recording. The mean note duration for the 6 males was 0.047 ± 0.007 and varied from 0.029 to 0.07 s. The inter-note intervals had a mean of 0.9 ± 1.2 s and a range of 0.2 to 8.2 s. However, variation in temporal parameters within and among individuals was high (Table 2).

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Call characteristics in spectral parameters: Because temperature did not affect the spectral parameters of calls, we describe the spectral parameters for the 8 males together. Large variation in the spectral parameters occurred within 3-minute intervals of individual calls. For most individuals, the frequency distribution was not normal. Therefore, we used the median, lower and upper quartiles, and maximum and minimum values to characterize the maximum, high, and low frequency traits for the 8 males. Because the maximum, low, and high frequency were highly correlated (maximum and lower: r = 0.87; maximum and high: r = 0.93; low and high: r = 0.92), we present only maximum frequency to illustrate individual variation in detail (Table 2). A sub-sample of 41–50 notes emitted in a period of 3 min was analyzed for each male. Notes were selected in intervals of 4 s. For the 8 males combined, the medians for low, high, and maximum frequency were 4.61, 5.25, and 5.01, respectively (Fig. 4). The upper and lower quartiles were 4.80 and 4.53 for low frequency, 5.60 and 5.10 for high frequency, and 5.34 and 4.60 for maximum frequency. The ranges of the low, high, and maximum frequencies were 4.20–5.80, 4.54–5.75, and 4.54–5.54 respectively. Three other Amazonian species for which calls are known produce only long trains of single notes (A. caeruleodactylus, Lima & Caldwell 2001; A. nidicola (Caldwell & Lima 2003); and A. subfolionidificans (Lima et al. 2007). All of these calls can be distinguished from A. brunneus by frequency or number of calls emitted per minute (see Lima et al. 2007).

Description of tadpole Figs. 5–6 Descriptive statistics for 11 meristic characters were based on 46 tadpoles of stages 25–42 (Table 3). The following description is based on a stage 39 tadpole from INPA-H 10043 (Figs. 5A–C). Tadpoles in this lot were collected in stage 25 from the back of a male and reared to stage 39 before preservation. The body is ellipsoid in dorsal view (Fig. 5A) and flattened in lateral view (Fig. 5C). TL 24.5 mm; body and tail 31% and 69%, respectively, of TL; body wider than deep; maximum BH 4.1 mm; maximum BW 6.0 mm; width of body at level of eyes 4.9 mm; snout bluntly rounded in dorsal and lateral views; distance from nostril to anterior edge of eye 1.0 mm; eye length 1.1 mm; eyes dorsal and directed laterally; IOD 2.6 mm, 53% of head width at level of eyes. Naris small, located dorsolaterally and directed anterolaterally; IND 1.3 mm, 27% of head width at level of eyes; spiracle a dorsolaterally directed free tube, 1.2 mm long, sinistral, easily seen approximately at mid-body and below lateral midline (Fig. 5C). Medial vent tube 2.0 mm, attached to ventral fin, opening in line with edge of ventral fin. Caudal musculature robust and deeper than fins, width 2.7 mm at body–tail juncture and 2.1 at midtail; upper fin 1.5 mm, lower fin,1 mm, at midtail. In lateral view, upper fin originates at junction of body and tail. Oral apparatus emarginate, located anteroventrally, 2.1 mm in width (Fig. 6); anterior labium with small papillae only on lateral margin, 5 on each side; posterior labium entirely surrounded by 22 papillae; papillae on posterolateral margin (5 on each side) smaller than the 12 posteromedial papillae (Fig. 6); lateral posteromedial papillae larger than medial; submarginal papillae absent; lower jaw sheath V-shaped, deeper than upper jaw sheath; transverse width of upper sheath 1.0 mm, or 48% of oral disc width; both upper and lower sheaths serrated; serrations extend entire length of sheaths, but do not include lateral processes; labial tooth row formula 2(2)/3(1); tooth row A-1 complete, 1.73 mm; tooth row A-2 interrupted medially, consisting of two widely separated sections at level of lower jaw sheath, each section 0.46 mm in length, medial gap, 0.63 mm. Lower tooth rows shorter than A-1; P-2 (1.5 mm) slightly longer than P-1 (1.4 mm) and P-3 (0.97) shorter in length than P-1 and P-2 (Fig. 6). P-1 gap very narrow. Tadpoles of A. brunneus are easily distinguished from those of A. marchesianus and A. caeruleodactylus (Caldwell et al. 2002a). The latter two species have an unusual arrangement of papillae on the margins of the oral disc and distinct but irregular stripes on the tail. Allobates brunneus has a more regular arrangement of

REDESCRIPTION OF ALLOBATES BRUNNEUS

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papillae on the margin of the oral disc and small, irregular blotches on the tail. The tadpole of A. subfolionidificans has more papillae surrounding the oral disc (Lima et al. 2007). The nidicolous tadpole of A. nidicola has greatly reduced mouthparts, yolk-filled intestines, no spiracle, and no external opening of the gut (Caldwell & Lima 2003). TABLE 3. Measurements (in mm) of 46 tadpoles of Allobates brunneus in different Gosner (1960) stages. Values are means ± standard deviation; range in parentheses; hyphenated numbers are measurements for 2 individuals. Character

Stage 25 (N = 11)

Stage 28 (N = 2)

Stage 30 (N = 8)

Stage 33 (N = 2)

TL

13.1 ±1.2 (11.2–14.6) 16.7–17.4

18.5 ± 1.1 (16.2–20.0) 21.1–22.3

22.0 ± 1.3 (20.7–23.7)

BL

4.8 ± 0.4 (4.2–5.3)

5.5–6.2

6.2 ± 0.2 (5.7–6.4)

6.9 ± 0.2 (6.7–7.2)

TAL

8.2 ± 0.9 (7.0–9.3)

10.4–11.3

12.3 ± 1.0 (10.4–14.0) 14.4–14.8

15.0 ± 1.0 (13.9–16.4)

BW

3.4 ± 0.3 (3.0–3.7)

4.2–4.5

4.5 ± 0.3 (4.1–4.8)

4.8–4.9

5.1 ± 0.2 (5.0–5.3)

BH

2.2 ± 0.3 (1.9–2.6)

2.1–2.7

2.9 ± 0.2 (2.6–3.4)

3.1–3.6

3.4 ± 0.3 (3.2–3.9)

HWLE

2.8 ± 0.2 (2.5–3.1)

3.4–3.9

3.9 ± 0.2 (3.6–4.2)

4.3

4.2 ± 0.2 (4.0–4.5)

TMW

1.0 ± 0.2 (0.7–1.2)

1.3–1.3

1.7 ± 0.1 (1.5–1.8)

2.0

2.1 ± 0.1 (1.9–2.2)

MTH

2.4 ± 0 .3 (1.9–2.9)

2.9–3.0

3.2 ± 0.3 (2.8–3.5)

3.6–3.9

3.9 ± 0.2 (3.6–4.1)

TMH

1.1 ± 0.2 (0.9–1.4)

1.5–1.6

1.7 ± 0.2 (1.5–1.9)

2.0–2.1

2.1 ± 0.1 (2.0–2.3)

IOD

1.5 ± 0.1 (1.3–1.8)

1.8–2.0

2.1 ± 0.1 (1.9–2.2)

2.4–2.8

2.3 ± 0.4 (2.0–3.0)

IND

0.8 ± 0.1 (0.7–0.8)

0.9–1.0

1.1 ± 0.1 (1.0–1.2)

1.0–1.1

1.2 ± 0.1 (1.1–1.2)

6.7–7.5

Stage 35 (N = 5)

continued. Character

Stage 37 (N = 3)

Stage 39 (N = 12)

Stage 41 (N = 2)

Stage 42 (N = 1)

TL

24.3 ± 0.3 (24.0–24.6)

24.6 ± 1.1 (21.6–24.6)

23.5–25.2

19.9

BL

7.9 ± 0.3 (7.7–8.2)

7.7 ± 0.5 (6.5–8.3)

6.5–6.8

7.7

TAL

16.5 ± 0.1 (16.4–16.5)

16.8 ± 0.9 (14.9–17.9)

16.7–18.7

12.0

BW

5.7 ± 0.4 (5.3–6.0)

5.9 ± 0.6 (4.7–6.6)

5.5–6.7

4.3

BH

3.9 ± 0.4 (3.5–4.2)

3.9 ± 0.4 (3.1–4.4)

3.7–4.0

3.9

HWLE

4.8 ± 0.2 (4.6–5.0)

4.7 ± 0.4 (4.0–5.1)

4.6–5.1

3.5

TMW

2.4 ± 0.6 (2.3–2.4)

2.6 ± 0.3 (2.0–2.9)

2.4–2.5

2.0

MTH

4.1 ± 0.2 (3.9–4.3)

4.2 ± 0.5 (3.3–4.8)

3.0–3.3

2.3

TMH

2.3 ± 0.3 (2.0–2.5)

2.6 ± 0.4 (2.00–3.30)

1.7–2.0

1.9

IOD

2.6 ± 0.1 (2.5–2.6)

2.7 ± 0.1 (2.50–2.90)

3.0–3.2

3.2

IND

1.3 ± 0.0 (1.3–1.3)

1.3 ± 0.01 (1.30–1.4)

1.3–1.4

1.4

Color of tadpole in life: Dorsal and lateral surfaces of body grayish-brown with scattered irregular brown and silver blotches. Ventral surface of body and tail musculature same as in preservative. At stage 36, fins transparent with scattered irregular brown and silver blotches. At stage 25, fins grayish-brown. Color of tadpole in preservative: Dorsal and lateral surfaces of body brown. Anterior area of ventral surface of body cream with diffuse brown melanophores. Posterior area of ventral surface transparent, not pigmented, with intestines visible though the skin. Tail muscle cream; fins transparent or pale with irregularly spaced brown blotches (Fig. 5A–C). Color of metamorph in life: Dorsal surface of recent metamorphs gray with scattered irregular brown and silver blotches. Dorsum with 1 to 3 dark brown markings that may form triangular, diamond-shaped, or

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hourglass patterns between the orbits and extending to the sacral region (Fig. 5D). Metamorphs otherwise resemble adults in coloration.

FIGURE 5. (A) Dorsal, (B) ventral, and (C) lateral views of a stage 39 tadpole of Allobates brunneus from lot INPA-H 10043. View of recent metamorph (INPA-H 10042); note that the dorsal pattern of the metamorph is similar to the adult pattern.

FIGURE 6. View of oral disc of a stage 39 tadpole of Allobates brunneus from lot INPA-H 10043.

Natural history Habitat and Reproduction Allobates brunneus occurs in swamp forests in lowlands of the Chapada dos Guimarães region in Mato Grosso, Brazil. Field observations of reproductive behavior were made between 16 and 19 December 2001 by REDESCRIPTION OF ALLOBATES BRUNNEUS

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APL. This species of Allobates is the first known to lay eggs on upper surfaces of leaves of understory vegetation (Figs. 7A and 7B). Some individuals oviposit in leaf litter on the ground (Fig. 7D). Of nine clutches that were observed, seven were found on upper surfaces of leaves from 10 to 60 cm above ground, and two were found in rolled up dead leaves on the ground. Only one clutch was found per oviposition site. Six recently laid clutches had 17 eggs each. Three other clutches had 13, 10, and 2 tadpoles. The proportion of clutches laid above ground is probably underestimated because two days were spent searching for nests on the ground before it was realized that the species deposits eggs on live leaves above the ground. Tadpoles develop in the leaf nest to about stage 25 (Fig. 7C) before being transported on the parent’s back to small pools near streams, where they remain until metamorphosis. Males called during the entire day but were most active in the early morning from 0600–0900 h and again in late afternoon from 1600 h until dusk. During heavy rainfall, males were active and could be heard calling anytime between 0600 and 1830 h. Three males were encountered in wrestling bouts.

FIGURE 7. Deposition sites of eggs of Allobates brunneus: (A and B) clutches on upper surfaces of leaves of herbaceous vegetation, (C) tadpoles in stage 25 on upper surface of a leaf, and (D) clutch in rolled dead leaves on the ground.

Discussion Adult specimens in this study conform well to Cope’s (1887) description, with only relatively minor exceptions. Cope considered the first finger equal to the second, but in our specimens Finger I is slightly longer than Finger II. Cope also reported that the tympanum was concealed; however, the condition in our specimens (and

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most closely related species) is that the tympanum is only partially concealed posterodorsally by a slip of the m. depressor mandibulae (Grant et al. 2006). Edwards’ (1974a) examination of two topotypes of A. brunneus agrees well with our redescription. Edwards (1974b) interpreted the light brown coloration on the dorsum of A. brunneus as forming two dorsolateral stripes. In our specimens in which the hourglass pattern on the back is incomplete, the light brown coloration does not form distinct lines, and we consider it part of the background color. Edwards (1974b) also reported fringes on the fourth toe. Although some of our specimens had basal webbing between Toes III and IV extending to the middle of the second phalange on both toes, none had fringes of the type described by Grant et al. (2006). The vocalization of A. brunneus is unusual in that above 28 C, pulsed calls were emitted in groups of 6 to 11 notes, whereas below that temperature, notes were emitted singly. We also reported that A. marchesianus at times produces irregular trains of notes and at other times produces a continuous train of notes (Caldwell et al. 2002b). Comparisons of the call of A. brunneus with other Amazonian Allobates for which calls are known indicate that each species has a distinguishable call. Tadpoles of many species of Amazonian Allobates are as yet undescribed, including A. conspicuus, A. fuscellus, A. masniger, A. sumtuosus, A. vanzolinius, A. crombiei, and A. gasconi. Known tadpoles of species of Amazonian Allobates, including A. marchesianus, A. caeruleodactylus, A. subfolionidificans, and A. nidicola, are readily distinguished from tadpoles of A. brunneus. Conservation concerns: In 2002, one of us (CS) conducted herpetological inventories at the National Park of Chapada dos Guimarães. These surveys revealed no evidence of the presence of A. brunneus in this or in other protected areas in Chapada dos Guimarães (pers. comm., CS). Thus, flooding of the swamp forests along the Rio Casca may have caused extirpation of Allobates brunneus in most of this region. Moreover, the sites where populations were last located, in December 2001, are outside of any of the government or private conservation units existing in that region. Special effort should be undertaken to ensure the conservation of these swamp forest habitats and the associated biota, including Allobates brunneus.

Acknowledgments We are grateful to William E. Magnusson for providing invaluable field assistance and comments on a draft of the manuscript. Collection of specimens by APL and CS was authorized by Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA, License # 006/2001, proc. 0200.008733/01-26 IBAMA/RAM to APL, and License # 131/98 IBAMA/DIREC, proc. 450/98-16-AC to CS). This research was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, proc. 300660/2005-7) and Instituto Nacional de Pesquisas da Amazônia (INPA, PPI - 05.70) to APL.

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