A new species of stream-dwelling frog of the genus Cycloramphus (Anura, Cycloramphidae) from the State of Rio de Janeiro, Brazil

Zootaxa 3407: 49–60 (2012) www.mapress.com / zootaxa/ Copyright © 2012 · Magnolia Press

ISSN 1175-5326 (print edition)

Article

ZOOTAXA ISSN 1175-5334 (online edition)

A new species of stream-dwelling frog of the genus Cycloramphus (Anura, Cycloramphidae) from the State of Rio de Janeiro, Brazil HELIO RICARDO DA SILVA & DAIANE OUVERNAY Universidade Federal Rural do Rio de Janeiro, Instituto de Biologia, Caixa Postal 74524, CEP 23851-970, Seropédica, RJ – Brasil. E-mail: [email protected], [email protected]

Abstract A new anuran species, Cycloramphus lithomimeticus sp. nov., of the C. granulosus species group is described from the Municipality of Itaguaí, in the State of Rio de Janeiro, Brazil (22°54'3.44"S; 43°53'34.59"W, 160 m). The new species is distinguished from all other species in the C. granulosus group (and many others in the genus) by lacking inguinal macro glands (on males). We also present data on its natural history, a few aspects of its osteology, tadpole, and discuss evidence for the relationships of the genus based primarily on the morphology of the tadpole. Key words: Atlantic Forest; Brazil; Cycloramphus granulosus group, tadpole, Cycloramphus relationships

Introduction The cycloramphid genus Cycloramphus Tschudi, 1838 comprises 27 species, all endemic to the Atlantic Forest of Brazil (Weber et al. 2011; Verdade & Rodrigues 2003) with a distribution extending from the State of Bahia in the northeastern (Heyer 1988) to the State of Rio Grande do Sul, in the south (Garcia & Vinciprova 1998). An unpublished phylogeny based on morphology recovered two groups within the genus (Verdade 2005). One associated with forest floor litter, with terrestrial eggs and endotrophic tadpoles that complete their development in terrestrial humid habitats (Heyer & Crombie 1979, Verdade & Rodrigues 2003). The other group is composed of species that lay eggs on logs or rocks in the splash zones of rivers and streams running in steep terrain and have tadpoles that feed and swim on films of water running alongside waterfalls (Lutz 1929; Heyer 1983, Giaretta & Cardoso 1995; Giaretta & Facure, 2003). A more traditional and phenetic approach to the taxonomy of Cycloramphus further subdivided the genus into five groups as presented by Heyer (1983) based on an early proposal by Bokermann (1951): C. bolitoglossus and C. eleutherodactylus species groups are forest litter dwellers, whereas C. ohausi, C. granulosus, and C. fuliginosus species groups are stream dwellers. Within the latter group, species in the C. granulosus group are recognized based on the absence of webbing between toes and granulose skin texture (Heyer 1983). While in the last nine years three new species of the terrestrial Cycloramphus eleutherodactylus species group have been discovered and described (Verdade & Rodrigues 2003; Brasileiro et al. 2007; Weber et al. 2011), no species has been described that belongs to the more aquatic groups of species. One possible explanation for that may relate to differential collecting efforts. While lots of new Atlantic forest localities have been inventoried with direct search and pitfall traps, which increases the chances of finding terrestrial forms, rivers running along scarped terrain, with many steep waterfalls have been less surveyed, possibly due to the risk of accidents associated with working at these sites. In a recent survey of frogs in a well preserved area of coastal forest in the metropolitan area of the city of Rio de Janeiro, a Brazilian city that has been surveyed for frogs for over two centuries, we found juvenile and tadpoles of species of Cycloramphus with free toes, belonging to the Cycloramphus granulosus group. The main river draining the surveyed area is called Itinguçu (or Itingussu). Although it runs on steep landscape, we had the opportunity to survey it, near some of its waterfalls, at night, and also collected additional adult specimens. Herein we describe this population as a new species.

Accepted by M. Vences: 15 Jun. 2012; published: 2 Aug. 2012

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Material and methods Specimens examined are listed in the Appendix. Although the specimen designated by Heyer (1983) as the lectotype for Cycloramphus granulosus is still available in the Museu Nacional, Rio de Janeiro, where the Adolpho Lutz collection is housed (AL-MNRJ 1537), it was not used for general comparison because of its poor preservation. Sex was determined by direct examination of gonads, via a small lateral incision on the abdomen or, in the case of the Cycloramphus granulosus, overall smaller size and the presence of the inguinal gland were used to identify males— larger specimens with no gland were considered females. The stomach of 10 individuals of the species described herein were removed and dissected, their contents were examined under stereomicroscope and identified to the level of order. Specimens measurements were taken with a digital caliper to the nearest 0.1 mm with the individuals under a stereomicroscope, using the standards presented by Duellman (1970) that are as follows: snout-vent length (SVL), head length (HL), head width (HW), thigh length (THL), tibia length (TBL), foot length (FL), and hand length (HaL), eye diameter (ED), interorbital distance (IOD), eye-nostril distance (END), and internarial distance (IND). Description of the snout shape was based on Heyer (1983). For finger numbering, we assume that the hypothesis presented by Alberch and Gale (1985) is correct, and therefore, that frogs lost their thumb (Finger I) and have only Fingers II to V. All adult specimens collected were euthanized with 5% xylocaine, fixed in 10% formalin, and transferred to 70% ethanol for permanent storage. Tadpoles were collected at night from rocks near were adults were collected, their identification was confirmed based on the finding of individuals on stage 42 that are already similar in color pattern to the adults. Tadpoles were euthanized the same way as adults, fixed and stored in 5% formalin. Standards for tadpole description and measurements follow Altig and McDiarmid (1999) and are as follows: total length (TL), body length (BL), body height (BH), body width (BW), tail length (TL), tail height (TH), dorsal fin height (DFH), ventral fin height (VFH), eye diameter (ED), internarial distance (IND), interorbital distance (IOD), eye-snout distance (ESD), eye-nostril distance (END), oral disc width (ODW). Developmental stages of tadpoles were determined following Gosner (1960). Geographic Information System data was collected by using a Garmin GPS map 60CSx with the datum South America 69. Abbreviations used for museums are as follows: CFBH (Universidade Estadual Paulista, Rio Claro, São Paulo), MNRJ (Museu Nacional, Rio de Janeiro), MZUSP (Museu de Zoologia da Universidade de São Paulo), and RU (Coleção Herpetológica da Universidade Federal Rural do Rio de Janeiro).

Results Cycloramphus lithomimeticus sp. nov. (Fig. 1) Holotype (MNRJ 80585) Adult male, obtained at Cachoeira de Itinguçu (also spelled Itingussu), Coroa Grande, Municipality of Itaguaí, State of Rio de Janeiro, Brazil (22°54'3.44"S; 43°53'34.59"W, near 160 m) collected upriver from the dam used by the State Water Company (CEDAE), by Daiane Ouvernay, Helio Ricardo da Silva, and Edicarlos Pralon in 30 August 2010. Paratypes. MNRJ 80586 ♀, MNRJ 80587 ♂, MNRJ 80588 ♂, MNRJ 80589 ♂, MNRJ 80590 ♂, MNRJ 80591 ♂, MNRJ 80592 ♂, MNRJ 80593 ♂, MNRJ 80594 ♀, MNRJ 80595 ♂, MNRJ 80596 ♀, MNRJ 80597 ♂, MNRJ 80598 ♂. All collected with the holotype. Diagnosis. The new species is placed in the genus Cycloramphus based on the presence of well developed menisci on upper irises and tadpole morphology, with characteristic mouth and reduced upper and lower fins on the tail, a bilobed terminated skin flap on the venter, and habitat (wet rock near waterfall). Additionally, the new species is placed in the Cycloramphus granulosus group because of the granular dorsal skin, free toes (no webbing), and heterotrophic larvae inhabiting steep wet rocks, near waterfall splash area. Cycloramphus lithomimeticus sp. nov. is a small sized species of Cycloramphus (adult males 24.6–31.0 mm, adult females 29.7–31.7 mm SVL) characterized by (1) snout round in dorsal and lateral views, (2) head wider than long, (3) eyes protruding, (4) white pigmented menisci on upper irises, (5) upper eyelid with small regularly spaced small granules; (6) dorsal skin granulose, covered by evenly spaced small granules; (7) tympanum not visible externally, but it can be observed after the skin is removed, (8) lack of vocal slits; (9) vocal sac indistinct, (10) dentigerous process of vomer round, (11) tibia and thigh of equal size, (12) toes free, (13) in life, dorsum brown and/or

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dark green, (14) in live specimens internal organs can be seen thorough the ventral skin and musculature (after fixation this area becomes cream and opaque), (15) lacking inguinal glands.

FIGURE 1. Cycloramphus lithomimeticus sp. nov. Holotype (MNRJ 80585). (A) dorsal view, (B) ventral view, (C) close up of the head in dorsal view, (D) lateral view of the head, (E) palm, and (F) sole.

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FIGURE 2. Cycloramphus lithomimeticus sp. nov. Live specimens, not collected, examples of two color variants (A) brown similar to the color after the specimens are fixed and (B) green dorsum that mimicries the gneisses and moss where the frog is sitting.

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FIGURE 3. Live Tadpole of Cycloramphus lithomimeticus sp. nov.

Comparison with other species of Cycloramphus. Cycloramphus lithomimeticus sp. nov. differs from all species of Cycloramphus except C. organensis Weber, Verdade, Salles, Fouquet, and Carvalho-e-Silva by the absence of externally visible inguinal macrogland on males. There are no glands internally or externally in C. lithomimeticus sp. nov. while in C. organensis such glands are present on the internal surface of the inguinal skin (see description in Weber et al. 2011). Because it has free toes, C. lithomimeticus sp. nov. can be readily distinguished from all the species with membrane between the toes (C. asper Werner, C. boraceiensis Heyer, C. brasiliensis (Steindachner), C. cedrensis Heyer, C. dubius (Miranda-Ribeiro), C. duseni (Andersson), C. fuliginosus Tschudi, 1838, C. izecksohni Heyer, C. juimirim Haddad and Sazima, C. lutzorum Heyer, C. mirandaribeiroi Heyer, C. ohausi (Wandolleck), C. rhyakonastes Heyer, and C. semipalmatus (Miranda- Ribeiro)). Because of the skin texture with granular appearance and small granules evenly distributed, C. lithomimeticus sp. nov.is similar to species in the C. granulosus group (C. catarinensis Heyer, C. granulosus Lutz, and C. valae Heyer) however, adult males of all these species have externally visible inguinal macroglands that are absent in C. lithomimeticus sp. nov. Both samples of C. granulosus from Serra da Bocaina (São Paulo) and Itatiaia (Rio de Janeiro) have vocal slits, C. lithomimeticus sp. nov. has only skin folds on the floor of the mouth lateral to the tongue. In Table 2 we present a comparison between samples of C. lithomimeticus sp. nov. and C. granulosus from Serra da Bocaina, São Paulo. Holotype description. Body robust, elliptical in dorsal view; head wider than long (Fig. 1) internarial distance smaller than eye-nostril distance and smaller than eye diameter; eye diameter larger than eye–nostril distance; menisci on upper irises evident, with round margin, and sprinkled with minute white dots; snout round in lateral and dorsal views (Fig. 1); nostrils elliptical and protuberant; loreal region slightly concave; eyes protruding; tympanum not visible externally; supratympanic fold discrete, but well marked, extending from tympanic region to shoulder; vocal sac indistinct; vocal slits lacking; tongue smooth and round; skin folds present on the month floor lateral to the tongue; dentigerous process of vomer elliptical, right vomer with five, left vomer with four teeth; choanae medium-sized, rounded. Pseudodontoid on the madibular symphysis, protuberant and conical. On the maxilla, a round space between the premaxillae lodges the pseudodontoid when the mouth is closed. Mandible with finegrained tooth-like serration. Arm robust; forearm slightly thicker, ulnar fold absent; fingers without webbing or fringes; finger lengths IV > V > II = III; palmar tubercle round, larger than thenar, which is elliptical, each finger with one supernumerary tubercle. With the exception of palmar surface of Finger II and III, the rest of the palm skin is dark. Tibia length similar to thigh length; tarsal fold absent; toes without webbing and lateral fringes; toe lengths IV > V ~ III > II > I; inner metatarsal tubercle elliptical and larger than round outer metatarsal tubercle. Toes I and II have one supernumerary tubercle each; Toes III and V with two, and Toe IV with three tubercles. Plantar surface dark. Inguinal glands absent. Dorsal skin densely granular, with small and round granules, all of similar size, covering the head, eyelid, trunk, dorsal surface of arms, thigh, and in smaller number the tibia.

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Color of holotype in preservative. Dorsal color pattern uniform dark brown, but near the flanks the brown is lighter. Dorsum with a central, irregular, cream spot, and an irregularly shaped, cream area over the scapulae. Near the inguinal region there are a few small, cream scattered spots. Head with a frontal triangular dark area. Laterally, face with two dark stripes, one from the eye to the lip, the other from the eye to the corner of the month; these stripes enclose white areas that are also marked by incomplete and lighter dark stripes (Fig 1). Dorsally, the head is mostly dark brown with an interorbital thin white to cream line. The thigh, tibia, and foot are barred with darker thick lines. The forearm and hand also have are crossed by to thick dark bars. Fingers are irregularly barred, with cream lines on the articulation and on the tips. The venter is cream, with a few scattered minute dark chromatophores on the gular region. The palm and foot sole are darker. Variation. Variation of measurements taken of adult males and females are given in Table 1. Variation in color pattern was described based on Heyer´s (1983) standards developed for species in the Cycloramphus fuliginosus group. Specimens of C. lithomimeticus sp. nov. vary in a similar manner (Fig. 2). The dorsum may fit patterns A, C, and D, thigh color may fit patterns A, B, and C, venter the patterns A, B, C, and E. The sample studied includes (1) specimens with a well marked dark X on the dorsum, that extends from the back of the eyes to the middle of the vertebral column and has a clear spot in the confluence of the lines that make up the X (Pattern A); (2) specimens with dark brown dorsum with cream and small irregularly distributed spots (Pattern C); and (3) with darker irregular marks on the brown dorsum (Pattern D). Specimens have uniformly dark (Pattern A), mottled (B), or spotted (Pattern C) posterior portion of the thighs. On the venter, although live specimens all have translucent abdominal wall and skin that permits observation of the internal organs, after fixation, the skin turned uniformly light cream, with scattered small melanophores, which may be more concentrated on the throat region, on the thigh and arm ventral skin. On the upper lip, between the eye and the nostril, three cream colored bars separated by three brown stripes are present in all specimens. The dark stripes may vary in length and darkness. TABLE 1. Measurements (in mm) of the type series of Cycloramphus lithomimeticus sp. nov. Abbreviations are as follows: Snout-vent length (SVL), head length (HL), head width (HW), eye diameter (ED), interorbital distance (IOD), eye-nostril distance (END), internostril distance (IND), thigh length (THL), tibia length (TBL), and foot length (FL). Boldface indicates the holotype. Number

SVL

HL

IOD

END

ED

IND

THL

TBL

FL

HL

MNRJ 80585

29.4

11.5

3.5

2.4

4.0

1.1

15.5

15.1

14.2

8.9

MNRJ 80586

29.7

11.1

3.5

2.9

4.1

2.6

15.2

13.4

13.5

7.3

MNRJ 80587

24.6

9.6

2.6

2.1

3.4

2.0

12.4

13.4

11.6

6.8

MNRJ 80588

29.6

11.6

3.4

2.1

3.9

1.5

14.5

12.8

10.8

6.6

MNRJ 80589

27.6

10.9

3.4

1.9

3.3

1.1

12.2

12.5

11.4

7.4

MNRJ 80590

26.9

10.5

2.8

1.9

4.1

1.4

14.2

13.1

11.2

7.2

MNRJ 80591

31.0

11.2

3.0

2.6

3.5

2.0

13.3

13.4

11.7

7.1

MNRJ 80592

29.7

10.8

3.1

2.6

3.4

1.4

13.7

14.0

11.5

7.8

MNRJ 80593

27.6

11.4

3.4

2.0

3.4

2.1

13.4

14.4

12.9

7.7

MNRJ 80594

31.0

11.9

3.5

2.8

3.9

2.0

15.9

15.6

14.6

9.2

MNRJ 80595

27.3

11.2

3.1

1.9

4.3

2.6

15.5

13.9

13.3

8.11

MNRJ 80596

31.7

11.7

3.2

2.1

4.1

2.3

14.7

14.1

12.3

7.9

MNRJ 80597

27.1

11.4

2.9

2.0

3.7

1.9

13.7

13.3

11.3

7.7

MNRJ 80598

27.0

10.7

2.6

2.1

3.7

1.7

13.2

13.7

12.0

7.0

Sex

♂ ♀ ♂ ♂ ♂ ♂ ♂ ♂ ♂ ♀ ♂ ♀ ♂ ♂

Tadpole (Figs. 3 and 4). Larval measurements for a sample of 11 tadpoles are presented in Table 3. The larvae are elongated, with the body and head, longer than wider and compressed dorsoventrally. Tail fins are low and restricted to the distal half of the tail, the ventral is more pronounced than the dorsal. The belly is flattened and has a shallow flap, which extends from the back of the mouth to the posterior end, over the vent tube and, in Stage 30, covers the limb buds and the vent tube, and has bilobed end. A spiracular tube is not present, but the skin that forms the ventral flap is pierced by a round opening, on the left side of the body. We injected water-diluted crystal violet through the spiracular opening and saw it spreading into a bag formed by the flap over the ventral body wall. The

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eyes are moderately large and dorsal and, in the Stage 30, already present menisci on the upper iris. Nostrils are minute and nearly round, with openings towards the front, and a little white-pigmented area in front of it. Ventrally, on the body and tail, there are no markings, and the general color is light cream. Dorsally, the body is dark brown, with the body part already resembling the adult color pattern, even in Stage 30. The tail is dorsally marked with dark outlined parentheses that may be either coincident on both sides or uneven, forming a general pattern that resembles a double helix. In live specimens, the dorsal color pattern is either pale salmon or green. The oral disk is ventral and relatively almost as broad as the head anteriorly. The anterior gap in the papillae is wide, and extends through entirely frontal part. The papillae are in a single row laterally and in two rows posteriorly. The tooth row formula is 2(2)/3(1). The two anterior tooth rows are larger than the posterior ones, and within each set the rows are of similar size. The keratodonts on each row are of different size, being A-2 the largest, A-1 ~ P-1, P-2 the next in size, and P-3 the smallest ones. The upper beak is longer than the lower one, and has the general shape of a moustache with the lateral ends thinner. The lower beak is in the shape of a pen tip, or a section of a cylinder. We were unable to identify lateral lines on the body or tail of the tadpoles. TABLE 2. Comparison of standard measurements (in mm) for samples of Cycloramphus lithomimeticus sp. nov. and Cycloramphus granulosus from near the type locality in Serra da Bocaina, São Paulo. Abbreviation are as follows: Snout-vent length (SVL), head length (HL), head width (HW), interorbital distance (IOD), eye-nostril distance (END), internostril distance (IND), thigh length (THL), tibia length (TBL), and foot length (FL). Cycloramphus lithomimeticus sp. nov.

Cycloramphus granulosus

Males (n = 11)

Females (n = 3)

Males (n = 7)

Females (n = 9)

Mean (SD)

Range

Mean (SD)

Range

Mean (SD)

Range

SLV

28.0 (+ 1.8)

24.6–31.0

31.0 (+ 1.0)

29.7–31.74

37.7 (+ 2.7)

34.0–41.1

HL

11.0 (+ 0.6)

9.6–11.6

11.6 (+ 0.4)

11.1–11.9

15.8 (+ 1.2)

IOD

3.1 (+ 0.6)

2.6–3.5

3.4 (+ 0.2)

3.2–3.5

4.1 (+ 0.8)

END

2.1 (+ 0.3)

1.9–2.6

2.6 (+ 0.4)

2.1–2.9

IND

1.7 (+ 0.5)

1.1–2.6

2.3 (+ 0.3)

Mean (SD)

Range

37.1 (+ 5.49)

24.0–42.2

13.2–17.1

15.4 (+ 2.73)

9.0–19.3

2.4–4.7

3.9 (+ 0.86)

2.4–4.9

2.2 (+ 0.2)

1.9–2.6

2.4(+ 0.51)

1.5–3.3

2.0–2.6

2.6 (+ 0.3)

2.2–3.1

2.0 (+ 0.54)

1.1–2.7

THL

13.8 (+ 1.1)

12.2–15.5

15.2 (+ 0.6)

14.7–15.9

18.0 (+ 1.3)

15.7–20.0

16.1 (+ 3.01)

9.6–19.2

TBL

13.6 (+ 0.7)

12.2–15.1

14.4 (+ 1.1)

13.4–15.6

16.1 (+ 1.4)

14.0–18.0

15.8 (+ 2.32)

10.3–18.1

FL

12.0 (+ 1.0)

10.8–14.2

13.5 (+ 1.1)

12.3–14.6

24.5 (+ 1.8)

22.3–27.2

19.6 (+ 5.94)

10.5–28.5

HL

7.5 (+ 0.7)

6.6–9.0

8.2 (+ 0.9)

7.3–9.2

9.6 (+ 0.7)

8.9–10.9

09.3 (+ 1.52)

5.9–10.8

TABLE 3. Measurements (in mm) of tadpoles of Cycloramphus lithomimeticus sp. nov. Stages follows Gosner (1960), total length (LT), body length (BL), body height (BH), body width (BW), tail length (TL), tail height (TH), dorsal fin height (DFH), ventral fin height (VFH), eye diameter (ED), internarial distance (IND), interorbital distance (IOD), eye-snout distance (ESD), eye-nostril distance (END), oral disc width (ODW), body fin distance (BFD), fin length (FL). Stage

LT

BL

BH

BW

TL

TH

DFH

VFH

ED

IND

IOD

ESD

END

ODW

BFD

37

24.3

6.6

2.6

3.4

16.6

3.0

0.3

0.2

0.9

1.0

1.5

0.7

0.8

2.2

11.2

5.4

30

23.0

5.8

2.4

4.0

16.9

1.7

0.3

0.2

0.9

1.0

1.3

1.0

0.8

2.1

7.0

8.2

30

19.6

5.2

1.7

3.1

14.1

0.9

0.2

0.1

0.7

0.6

0.9

1.1

0.7

1.9

7.7

7.2

30

22.3

5.5

1.9

3.1

15.6

1.3

0.3

0.3

1.1

1.0

1.0

1.0

0.7

1.8

8.5

8.6

30

21.3

5.3

1.5

3.1

15.0

1.1

0.3

0.3

1.0

0.7

1.0

0.9

0.5

1.8

7.2

8.0

30

21.5

5.4

1.6

3.2

15.4

1.1

0.2

0.2

0.8

0.8

1.0

0.9

0.8

1.6

7.9

6.7

30

22.2

5.7

1.7

3.1

16.5

1.3

0.3

0.4

0.8

0.9

1.0

0.9

0.6

1.9

6.4

9.2

30

20.8

5.1

1.6

3.2

14.4

1.0

0.2

0.2

1.1

0.9

1.0

1.0

0.6

1.7

7.0

7.3

30

20.6

5.1

1.6

3.1

14.5

1.0

0.2

0.2

1.0

0.8

0.8

0.9

0.7

1.7

6.4

8.4

30

21.1

5.1

1.7

3.1

15.3

0.6

0.3

0.2

0.7

0.8

0.6

1.0

0.6

1.9

6.2

8.9

30

21.9

5.6

1.5

2.9

16.9

1.0

0.2

0.2

0.9

0.6

1.0

1.2

0.7

1.9

6.7

8.7

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FL

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FIGURE 4. Morphological Features of a tadpole of Cycloramphus lithomimeticus sp. nov. Stage 37. (A) Dorsal pattern, (B) Extremity of the tail showing the ventral fin origin, (C) Body ventral, (D) Body lateral showing the extension of the skin flap, (E) Detail of the skin flap ventrally, (F) Body dorsal showing the extent of the skin flap, (G) Detail of oral disc and moth, and (H) Lateral of the body indicating the location of the spiracular opening.

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FIGURE 5. Type locality of Cycloramphus lithomimeticus sp. nov., Rio Itingussu, Municipality of Itaguaí, Rio de Janeiro (22º 13’ 14.6” S and 43º 26’ 02.1” W) yellow arrows point to three waterfalls where specimens have been taken.

Natural history. Individuals of Cycloramphus lithomimeticus sp nov. were observed only at night and are considered nocturnal. Males call from near crevices and cracks on the rocks in steep parts of the river, near waterfalls, in the splash zone. Tadpoles were found nearby, in permanently wet vertical or nearly vertical rock walls; sometimes, near the areas where adults were active. The analysis of stomach contents indicated that Hymenoptera was the main food item and that, in addition to vegetal matter, larvae of Lepidoptera, Diptera, Blattodea, Tricoptera, Coleopeta (larvae and adults), and Aranae were also found. In the river, C. lithomimeticus sp nov. occurs syntopic with the nocturnal Thoropa miliaris Boulenger (Cycloramphidae) and the diurnal Hylodes asper (Müler) and H. phyllodes Heyer and Cocroft (Hylodidae). Etymology. The specific epithet is a masculine adjective formed from the Greek words Lithos (meaning stone) and mimētikos (meaning to imitate) and is used in allusion to the species color pattern that serves as camouflage and makes individuals similar to the rock surface where they are at rest.

Discussion Recent surveying of new areas along the Atlantic Forest of Brazil resulted in the discovery of several new species of frogs from different genera and families, occupying the most diverse types of habitats within the biome (see Frost 2011 and SBH 2011 for a complete list). The most striking information regarding these new discoveries is that several of them were made near highly urbanized areas (e.g. Canedo & Pombal 2007, Pombal et al. 2008, Weber et al. 2011, Silva & Alves-Silva 2011), where herpetological collections have accumulated collecting efforts for more than two hundred years. Because of the conservation issues relating to the preservation of the Atlantic

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Forest and the fact that these areas represent potential for the expansion of the urbanized nucleus of the city of Rio de Janeiro, these findings reinforce the need for continuing survey and conservation efforts even in these areas. To our knowledge, C. lithomimeticus sp nov. represents the first species of frog endemic to the recently created State Park (2008)—Parque Estadual do Cunhambebe.

FIGURE 6. Map of the State of Rio de Janeiro, Brazil with the type locality Cycloramphus lithomimeticus sp. nov. Municipality of Itaguaí – 22º 13’ 14.6” S and 43º 26’ 02.1” W (modified from http://www.agritempo.gov.br/altimetria/RJ.html).

It is intriguing that the rate of anuran species discoveries in steep river habitats is low for Cycloramphus when compared to other taxa that use the same habitat, such as species of the genus Hylodes. We speculate that this may relate to the low investment in nocturnal surveys of these habitats and that many more species of these waterfall dwellers may still exist along the Atlantic Forest. Furthermore, we suggest that species of Cycloramphus may inhabit most of the rivers where species of Hylodes and Crossodactylus are found, since they usually have similar preferences, differing in that species of these hylodids are diurnal, while Cycloramphus is nocturnal and prefers steeper rock surfaces near waterfalls in the same rivers. Indeed, several species of these three genera are syntopic (Lingnau et al. 2008; Araujo et al. 2010, personal observation). However, records of at least one of these hylodids and species of Cycloramphus are not so common in the literature, indicating either the inexistence of proper habitats (Heyer 1988) in all localities where hylodids occur, or perhaps undersampling. The lower rate of species discovery in Cycloramphus when compared to these hylodids may be related to the fact that while the hylodids are diurnal and more easily detected when calling during the day, Cycloramphus are all nocturnal, active near waterfalls, secretive, and highly mimetic. All this features make sampling of species of Cycloramphus harder. The unique tadpole external morphology, with the skin flap and bifid posterior end, may represent a good source of evidence for the monophyly of Cycloramphus. However, because of the lack of knowledge of the tadpoles, mainly for the terrestrial endotrophic species, this information cannot as yet be evaluated properly. Finally, while revising the literature and examining available specimens of Cycloramphus granulosus, which is the species most similar to C. lithomimeticus sp. nov. we had the opportunity to compare specimens of the former species from two localities. C. granulosus was described by Lutz (1929) based on a sample from Serra da Bocaina,

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in the State of São Paulo. Later, Heyer (1983) attributed specimens from Itatiaia, Serra da Mantiqueira, in the State of Rio de Janeiro, to the same species. Heyer also mentioned two specimens of C. granulosus to the Municipality of Itaguaí, in the State of Rio de Janeiro, but we were unable to find them in the herpetological collection housed in the Museu Nacional in Rio de Janeiro. Although he has attributed the sample from Itatiaia to Lutz (1929) species, Heyer suspected that the two samples may actually represent two different species (Heyer 1983: 269). Our analysis of samples from these two localities deposited in the Collections of Museu Nacional, in Rio de Janeiro, and in the Museu de Zoologia da Universidade de São Paulo, in São Paulo, confirmed the view that they may represent distinct taxa. The two populations seem to vary in size, and the overall size and shape of the inguinal glands also seem to differ.

Acknowledgments In the field, we were helped by Edicarlos Pralon, and Geisa Alves de Souza. Dr. Vanessa Verdade (UFABC) indicated to us that this was a species worth studying and that it might represent a new taxon. Gabriela B. BittencourtSilva helped with macro photography. Dr. Nelson Papavero (USP) suggested the name of the new species. Dr. Leandro de Oliveira Salles (MNRJ) let us use his Leica stereomicroscope for multi-focus photography. DO received a fellowship from CNPq. Frogs were collected under the permit SISBIO number 10689-1 to HRS and a license to Collect in the Parque Cunhambebe was issued to DO by INEA (Rio de Janeiro State Environment Institute). André L.G. Carvalho (AMNH), Gabriela B. Bittencourt-Silva (UFRRJ), Dr. Mark Wilkinson (BMNH), anonymous reviewer, and Dr. M. Vences (TUB) made valuable contribution to early versions of the manuscript. We are also thankful to the Dr. José Perez Pombal Junior (Curator MNRJ–Rio de Janeiro) and Dr. Hussam Zaher (Curator MUZUSP–São Paulo) for their assistance and cordiality during museum visits.

References Alberch, P. & Gale, E.A. (1985) A developmental analysis of an evolutionary trend: digital reduction in amphibians. Evolution, 39, 8–23. Altig, R. & McDiarmid, R.W. (1999) Body plan: development and morphology. In: McDiarmid R.W. & Altig, R. (Eds.), Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago and London, pp. 24–51. Araujo, C.O., Condez, T.H., Bovo R.P., Centeno, F.C. & Luiz, A.M. (2010) Amphibians and reptiles of the Parque Estadual Turístico do Alto Ribeira (PETAR), SP: An Atlantic Forest remnant of Southeastern Brazil. Biota Neotropica, 10, 257–274. Bokermann, W.C.A. (1951) Sinopse das espécies brasileiras do gênero Cycloramphus Tschudi, 1838 (Amphibia, Salientia, Leptodactylidae). Arquivos do Museu nacional, Rio de Janeiro, 42, 77–105. Brasileiro, C.A., Haddad, C.F.B., Sawaya, R.J. & Sazima, I. (2007) A new and threatened island-dwelling species of Cycloramphus (Anura: Cycloramphidae) from southeastern Brazil. Herpetologica, 63, 501–510. Canedo, C. & Pombal, Jr., J.P. (2007) Two new species of torrent frog of the genus Hylodes (Anura, Hylodidae) with nuptial thumb tubercles. Herpetologica, 63, 224–235. Duellman, W.E. (1970) Hylid frogs of Middle America (Vol. 1-2). Monographs of the Museum of Natural History, The University of Kansas, Lawrence, 753 pp. Frost, D.R. (2011) Amphibian Species of the World: an Online Reference. Version 5.5 (31 January, 2011). Electronic Database accessible at http://research.amnh.org/vz/herpetology/amphibia/ American Museum of Natural History, New York, USA. (accessed 10 November 2011) Garcia, P.C.D.A. & Vinciprova, G. (1998) Range extensions of some anuran species for Santa Catarina and Rio Grande do Sul States, Brazil. Herpetological Review, 29, 117–118. Giaretta, A.A. & Cardoso, A.J. (1995) Reproductive behavior of Cycloramphus dubius Miranda-Ribeiro (Amphibia, Anura, Leptodactylidae). Revista Brasileira de Zoologia, 12, 233–237. Giaretta, A.A. & Facure, K.G. (2003) Cycloramphus boraceiensis (flattened waterfall frog) clutch attendance. Herpetological Review, 34, 50. Gosner, K.L. (1960) A simplified table for staging anurans embryos and larvae with notes on identification. Herpetologica, 16, 183–190. Heyer W.R. & Crombie, R.I. (1979) Natural history notes on Craspedoglossa stejnegeri and Thoropa petropolitana (Amphibia: Salientia, Leptodactylidae). Journal of the Washington Academy of Sciences, 69, 17–20. Heyer, W.R. (1983) Variation and Systematics of Frogs of the Genus Cycloramphus (Amphibia, Leptodactylidae). Arquivos de Zoologia, São Paulo, 30, 235–339.

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Heyer, W.R. (1988) A notable collection of Cycloramphus (Amphibia: Leptodactylidae) from Bahia, Brazil, with a description of a new species (Cycloramphus migueli). Proceedings of the Biological Society of Washington, 101(1), 151–154. Lingnau, R., Canedo, C. & Pombal, J. P. (2008). A New Species of Hylodes (Anura: Hylodidae) from the Brazilian Atlantic Forest. Copeia, (3), 595–602. Lutz, A. (1929) Taxonomy and biology of the genus Cyclorhamphus. Memórias do Instituto Oswaldo Cruz. Rio de Janeiro, 22, 5–25. Pombal, Jr., J.P., Siqueira, C.C., Dorigo, T.A., Vrcibradic, D. & Rocha,C.F.D. (2008) A third species of the rare frog genus Holoaden (Terrarana, Strabomantidae) from a montane rainforest area of southeastern Brazil. Zootaxa, 1938, 61–68. SBH (2011) Brazilian amphibians – List of species. Accessible at http://www.sbherpetologia.org.br. Sociedade Brasileira de Herpetologia (accessed 10 November 2011). Silva, H.R. & Alves-Silva, R. (2011) A new bromeligenous species of the Scinax perpusillus group from the hills of the State of Rio de Janeiro, Brazil (Anura, Hylidae). Zootaxa, 3043, 54–68. Verdade, V.K. (2005) Relações filogenéticas entre as espécies dos gêneros Cycloramphus Tschudi 1838 e Zachaenus Cope 1866 (Anura, Leptodactylidae). Unpublished PhD Thesis, Universidade de São Paulo, Brazil, 241pp. Verdade, V.K. & Rodrigues, M.T. (2003) A New Species of Cycloramphus (Anura, Leptodactylidae) from the Atlantic Forest, Brazil. Herpetologica, 59(4), 513–518. Weber, L.N., Verdade, V.K., Salles, R.O.L., Fouquet, A. & Carvalho-e-Silva, S.P. (2011) A new species of Cycloramphus Tschudi (Anura: Cycloramphidae) from the Parque Nacional da Serra dos Órgãos, Southeastern Brazil. Zootaxa (2737), 19–33.

APPENDIX I. Additional Specimens of Cycloramphus granulosus examined. São Jose do Barreiro, Bocaina, São Paulo MUZUSP 86567, MNRJ 2510-13 Campo de Fruticultura, Serra da Bocaina, São Paulo MUZUSP 86720-24, MUZUSP 87497-503, MUZUSP 88117-120, MUZUSP 96081-82, MUZUSP 88337, 8 MUZUSP 8343, MUZUSP 88345-48, MUZUSP 86566, MUZUSP 88435-470, MUZUSP 96087. Parque Nacional do Itatiaia, Maromba, RJ – MUZUSP 86911-915, MUZUSP 86917-919, MUZUSP 13628, MNRJ 75749, MNRJ 75751-52, MNRJ 75758, L 155, L 127-8 (These are specimens from the Adolpho Lutz collection Heyer, 1983 examined and used this L numbering system. They have not yet received official museum tags, but are housed in the Museu Nacioal Collection).

APPENDIX II. Additional Tadpoles of Cycloramphus examined. Cycloramphus boraceiensis: Picinguaba, Ubatuba, São Paulo CFBH 9017; 9020. Cycloramphus brasiliensis: Barreiras, RJ, Brasil CFBH 14031 Cycloramphus sp.: Ilha do Cardoso, Cananéia, São Paulo CFBH 21997

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