Article. A new, large species of Chiasmocleis Méhelÿ 1904 (Anura: Microhylidae) from the Iquitos region, Amazonian Peru

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1 Zootaxa 2247: (2009) Copyright 2009 Magnolia Press Article ISSN (print edition) ZOOTAXA ISSN (online edition) A new, large species of Chiasmocleis Méhelÿ 1904 (Anura: Microhylidae) from the Iquitos region, Amazonian Peru W. CHRIS FUNK 1,3 & DAVID C. CANNATELLA 1,2 1 Department of Biology, Colorado State University, Fort Collins, CO , USA. Chris.Funk@colostate.edu. 2 Texas Natural Science Center, University of Texas, Austin, TX 78712, USA. catfish@mail.utexas.edu. 3 Corresponding author Abstract We describe a new species of Chiasmocleis (Anura: Microhylidae) from lowland rainforests in the western Amazon basin of Peru (near Iquitos, Departamento de Loreto). The species differs from congeners in the Amazon basin by its large size (it is the largest known Chiasmocleis species), bright yellow iris, a grey dorsum with reddish blotches posteriorly and on limbs, and a creamy white venter with bold dark mottling with pale centers. The new species also differs from two other sympatric Chiasmocleis species at 12S 16S mitochondrial DNA (6.1% and 11.9% sequence divergence between the new species and C. ventrimaculata and C. bassleri, respectively). A comparison of the new species with other microhylids found in the western Amazon basin is provided. Key words: Anura; new species; terrestrial frog; Peru; mitochondrial DNA; Microhylidae; Chiasmocleis devriesi Resumen Describimos una nueva especie de Chiasmocleis (Anura: Microhylidae) de los bosques lluviosos de tierras bajas en la cuenca amazónica occidental (cerca de Iquitos, Departamento de Loreto). Esta especie se distingue de otros congéneres de la cuenca amazónica por su gran tamaño (es la especie más grande de Chiasmocleis conocida), iris amarillo brillante, un dorso de color gris con manchas rojizas en la parte posterior y en las extremidades, y un vientre de color blanco cremoso con patrones oscuros y centros pálidos. La nueva especie también se difiere de las otras dos especies simpátricas en ADN mitocondrial 12S-16S (6.1% y 11.9% de divergencia secuencial entre la nueva especie y C. ventrimaculata y C. bassleri, respectivamente). Se provee una comparación de la nueva especie con otros microhílidos encontrados en la cuenca Amazónica occidental. Palabras claves: Anuro; nueva especie; rana terrestre; Perú; ADN mitocondrial; Microhylidae; Chiasmocleis devriesi Introduction The 62 recognized species of New World microhylids are predominantly terrestrial (fossorial and semifossorial) inhabitants of lowland rainforest (AmphibiaWeb 2009). Eighteen microhylid species in 9 genera are found in the western Amazon basin (IUCN et al. 2008, Frost 2009). Relative to some frog families such as Hylidae, Leptodactylidae, and Strabomantidae, microhylids are fairly depauperate in the western Amazon. A few to several microhylid species are typically found at a single site in lowland Amazonia compared to a dozen or more from each of these other three families (Duellman 1978, 2005, Rodríguez & Duellman 1994). However, new microhylid species continue to be discovered in this region (Wild 1995, Duellman & Mendelson 1995, Campbell & Clarke 1998, Lehr et al. 2002, Lehr & Trueb 2007, Moravec & Köhler 2007, Peloso & Sturaro 2008), suggesting that the diversity of the group is currently underestimated. Accepted by M. Vences: 15 Sep. 2009; published: 6 Oct

2 Chiasmocleis Méhelÿ, 1904 is the most diverse genus of microhylids in the western Amazon and in South America with 23 described species (IUCN et al. 2008, Frost 2009). One new Chiasmocleis species was recently described from the Iquitos region of northeastern Peru (Moravec & Köhler 2007), another was described from Amazonian rainforests south of the Amazon River (Peloso & Sturaro 2008), and several new Chiasmocleis have been described in the last decade from non-amazonian regions in South America (Caramaschi & Cruz 1997, Cruz et al. 1997, 1999, 2007a,b, Caramaschi & Pimenta 2003, Canedo et al. 2004). In the course of research on Physalaemus petersi at the Amazon Conservatory for Tropical Studies (ACTS) near Iquitos in the Departamento de Loreto, Peru (Boul et al. 2007, Funk et al. 2007, 2008, 2009), we discovered a large, undescribed Chiasmocleis species which we describe here. Materials and methods We examined alcohol-preserved specimens from herpetological collections at the Smithsonian Institution National Museum of Natural History (USNM), Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru (MHNSM), and Texas Natural Science Center, Texas Natural History Collection (TNHC). The specimens examined in addition to the new species are shown in Appendix 1. If specimens were not available for direct examination, we relied on the literature. Observations of osteological characters of the holotype were made from a three dimensional Computed Tomography (CT) scan. Terminology of morphological characters generally follows that of Duellman (1970), Zweifel (1986), and Lynch and Duellman (1997). Morphological measurements were taken with digital calipers to the nearest 0.1 mm, as follows: (1) snout-vent length (SVL) = distance from tip of snout to posterior margin of vent; (2) head length (HL) = distance from tip of snout to posterior angle of jaw articulation; (3) head width (HW) = width of head measured at level of jaw articulation; (4) internarial distance (IN) = distance between nostrils; (5) eye nostril distance (EN) = distance from posterior margin of nostril to anterior margin of eye; (6) eye diameter (ED) = distance between anterior and posterior borders of eyes; (7) interorbital distance (IOD) = distance between upper eyelids; (8) thigh length (ThL) = distance from flexed knee to vent; (9) tibia length (TiL) = length of flexed leg from knee to heel; and (10) foot length (FL) = distance from proximal margin of outer metatarsal tubercle to tip of Toe IV. We also estimated sequence divergence between the new species and two sympatric Chiasmocleis species (C. ventrimaculata and C. bassleri). We analyzed 2253 bases of mitochondrial DNA genes 12S rrna, valinetrna, and 16S rrna for the holotype of the new species and one individual each of C. ventrimaculata and C. bassleri found at the same site as the holotype. Methods for DNA extraction, amplification, and sequencing follow the protocol of Pauly et al. (2004). Methods for sequence alignment and estimation of sequence divergence follow Funk et al. (2007). Briefly, initial alignment of DNA sequences was completed in ClustalX (Thompson et al. 1997). Manual adjustments were then made in MacClade 4.06 (Maddison & Maddison 2000) so as to minimize the number of changes required across taxa. Uncorrected sequence divergence was then estimated in PAUP* 4.0b10 (Swofford 2000). Species description Chiasmocleis devriesi Funk & Cannatella, new species Figs. 1, 2 Holotype. MHNSM 21540, adult female, collected at the Amazon Conservatory for Tropical Studies (ACTS) Field Station, Departamento de Loreto, Peru, 65 km NE of Iquitos, 1 km N of the Río Napo, and 1.3 km SSE of the ACTS Field Station (3 15'34" S, 72 54'10" W, 102 m elevation), 30 May 2004 by W. Chris Funk and Claudia P. Torres-Gastello. 38 Zootaxa Magnolia Press FUNK & CANNATELLA

3 FIGURE 1. Dorsal (above) and ventral (below) views of the holotype of Chiasmocleis devriesi in life (MHNSM 21540, adult female; SVL = 42.2 mm). Photos by W. Chris Funk. NEW SPECIES OF CHIASMOCLEIS Zootaxa Magnolia Press 39

4 TABLE 1. Geographic range and morphological characteristics of microhylid frogs found in the western Amazon lowlands (of Colombia, Ecuador, Peru, western Brazil, and Bolivia). Head shape is in dorsal view. * = sex of measured holotype was not specified in the original description of Chiasmocleis shudikarensis (Dunn 1949). Species Range SVL Adelastes hylonomos Zweifel 1986 Altigius alios Wild 1995 Chiasmocleis anatipes Walker & Duellman 1974 C. avilapiresae Peloso & Sturaro 2008 SVL Head shape F o ot webbing Occip. fold Tymp. No. toes State of Amazonas in southern Venezuela 25-29? Rounded None Departamento de Madre de Dios in 49.5? Rounded Extensive southeastern Peru and northeastern Bolivia Eastern Ecuador, northeastern Peru Rounded Extensive Amazonian Brazil south of Amazon River C. bassleri Dunn 1949 Amazonian Ecuador, Peru, Bolivia, and adjacent Brazil and Colombia C. devriesi sp. nov. Near Iquitos, Departamento de Loreto, northeastern Peru C. magnova Moravec & Köhler 2007 C. shudikarensis Dunn 1949 C. ventrimaculata (Andersson 1945) Ctenophryne geayi Mocquard 1904 Elachistocleis ovalis (Schneider 1799) Hamptophryne boliviana (Parker 1927) Otophryne pyburni Campbell & Clarke 1998 Synapturanus mirandaribeiroi Nelson & Lescure 1975 TERMS OF USE Near Iquitos, in Loreto, northeastern Peru Guyana, Surinam, French Guiana, and Amazonian Brazil Amazonian Ecuador, Peru, Bolivia, southeastern Colombia, and far western Brazil Amazonian Venezuela, Colombia, Ecuador, Peru, Bolivia, Brazil, and all of Guyana, Suriname, and French Guiana Panama and Colombia southward, east of the Andes, to Argentina; Trinidad Northern and western sides of the Amazon basin: State of Bolivar (Venezuela), French Guiana, Suriname, Guyana, Brazil, Ecuador, Peru, Bolivia, and Colombia Vaupés and Amazonas, Colombia, across Venezuelan lowlands through Guianan region to Amapás, Brazil Northern Brazil, eastern Colombia, and the Guianas Triangular E xtensive in males; basal in females Rounded None - - 5? 42 Moderately Basal in pointed females? Rounded Basal * 25* Truncate Extensive in males; basal in females Rounded Basal Truncate Extensive Ac u t ely rounded Basal Rounded None Pointed Basal Pointed None S. rabus Pyburn 1976 SE Vaupés, Colombia, adj. Ecuador Pointed None S. salseri Pyburn 1975 Vaupés, Colombia, Amazonas, Venezuela, Manaus, Brazil 24 26? Pointed None Syncope antenori Amazonian Ecuador and Peru Truncate None Walker 1973 S. carvalhoi Nelson Loreto, Peru, adj. southern Amazonian Truncate None Colombia S. tridactyla (Duellman & Mendelson 1995) Loreto, Peru, western Brazil? 12 Truncate None Zootaxa Magnolia Press FUNK & CANNATELLA

5 TERMS OF USE FIGURE 2. Computed Tomography (CT) scan of the holotype of Chiasmocleis devriesi (MHNSM 21540, adult female; SVL = 42.2 mm), showing dorsal (above) and ventral (below) views. Diagnosis. A member of Chiasmocleis based on: (1) no occipital fold; (2) clavicles reduced, not reaching the glenoid region; (3) quadratojugal and maxilla separate; (4) alary process of premaxilla tilted only slightly forward; shelf of premaxilla with moderately sized notch; (5) neopalatine not distinguishable (Parker 1934, Carvalho 1954, Zweifel 1986). The largest known species of Chiasmocleis distinguished from all other members in the genus by the following combination of characters: (1) large size, SVL 42.2 mm in female, body ovoid; (2) snout moderately pointed in dorsal view, rounded and projecting in lateral view; (3) canthus rostralis rounded; loreal NEW SPECIES OF CHIASMOCLEIS Zootaxa Magnolia Press 41

6 region flat, sloping smoothly to upper jaw; (4) skin on dorsum irregularly textured, almost smooth; (5) fingers IV and II the same length; fingers basally webbed, fringes present, lacking discs; finger tips rounded; (6) all toes with lateral fringes, basally webbed in females (males unknown); tips rounded, no discs; (7) subarticular tubercles prominent; inner metatarsal tubercle distinct, oval; (8) small pigmented eggs; (9) in life, dorsal surfaces dark gray with rusty red blotches posteriorly and on limbs; creamy mid-dorsal stripe from the level of the eyes to the vent; snout and eyelids silver-gray; (10) in life, ventral surfaces creamy white with large grayish brown blotches; blotches are largest on belly and chest, becoming smaller and more dense on throat and hindlimbs; blotches with light centers, particularly on belly and chest; (11) iris bright golden yellow in life. Comparisons. Chiasmocleis devriesi is distinguished from other genera of microhylids in the western Amazon basin by a combination of no occipital fold, no visible tympanum, and five toes (Table 1). These character states are also found in Adelastes hylonomos and Hamptophryne boliviana, but A. hylonomos has a rounded head in dorsal view (moderately pointed in C. devriesi), no webbing on feet (basal webbing in C. devriesi), dark brown dorsal coloration (gray with reddish splotches on limbs and posteriorly in C. devriesi), and venter light brown with no color pattern (creamy white with bold dark mottling with pale centers in C. devriesi; Zweifel 1986). Hamptophryne boliviana has a rounded head, no webbing, a black inguinal spot extending onto dorsum (no such marking in C. devriesi), and a distinct demarcation between a tan or gray dorsum and dark brown or black flanks (no distinct demarcation between dorsal and flank color in C. devriesi; Parker 1927, Duellman 1978, 2005, Rodríguez & Duellman 1994). Chiasmocleis devriesi is substantially larger than all other known Chiasmocleis species found in the Amazon basin (female SVL 42 mm in C. devriesi compared to female SVL mm in C. magnova; 20 mm in C. hudsoni; mm in C. jimi; 25 mm in C. shudikarensis; mm in C. bassleri; mm in C. anatipes; mm in C. ventrimaculata; and mm in C. avilapiresae; Table 1). Of these Chiasmocleis species, C. devriesi is most likely to be confused with C. ventrimaculata (Fig. 3; Andersson 1945, Duellman 1978, Rodríguez & Duellman 1994) and C. avilapiresae (Peloso & Sturaro 2008). However, C. ventrimaculata has a rounded head (moderately pointed in C. devriesi), a reddish brown iris (bright yellow in C. devriesi), white spicules present lateral and ventral to vent (spicules not present in C. devriesi), no reddish coloration on posterior surface of dorsum (reddish color present on posterior surface of dorsum in C. devriesi), and small black blotches or mottling on venter (larger black mottling with pale centers in C. devriesi). Chiasmocleis avilapiresae has dermal spines on dorsum and toes (no dermal spines in C. devriesi), a light horizontal line on the posterior surface of thighs which is always present (no such line in C. devriesi), venter varying from light with almost no dark markings, small scattered brown or black spots, a few large spots, or a reticulated pattern (creamy white venter with large black mottling with pale centers in C. devriesi), and a bronze iris according to Fig. 1 in Peloso & Sturaro (2008; iris bright golden yellow in C. devriesi). Chiasmocleis devriesi also differs from C. anatipes by basal webbing on feet (extensive webbing in C. anatipes; Walker & Duellman 1974); from C. bassleri by a gray dorsum with reddish coloration on limbs and a cream venter with large dark mottling with pale centers (cream canthal and postorbital stripe, black inguinal spot extending onto dorsum, and bluish white belly with large black spots in C. bassleri; Dunn 1949, Rodríguez & Duellman 1994); from C. hudsoni by a moderately pointed head, basal webbing, and a gray dorsum with reddish coloration posteriorly and on limbs (rounded head, no webbing on feet, and a brown dorsum with lighter stippling in C. hudsoni; Parker 1940); from C. jimi by a moderately pointed head, basal webbing, and a gray dorsum with reddish coloration posteriorly and on limbs (rounded head, no webbing on feet, and a brown dorsum with irregular white dots in C. jimi; Caramaschi & Cruz 2001); from C. magnova by normal finger and toe length (reduced fingers I and IV and reduced toe I in C. magnova; Moravec & Köhler 2007); and from C. shudikarensis by a moderately pointed head and a gray dorsum with reddish coloration on limbs (truncate head, gray dorsum with light flecking, and black inguinal spot extending onto dorsum in C. shudikarensis; Dunn 1949). 42 Zootaxa Magnolia Press FUNK & CANNATELLA

7 FIGURE 3. Dorsal (above) and ventral (below) views of Chiasmocleis ventrimaculata in life from the same site where C. devriesi was found, the Amazon Conservatory for Tropical Studies (ACTS) Field Station (MHNSM 21539, adult female; SVL = 34.4 mm). Photos by W. Chris Funk. NEW SPECIES OF CHIASMOCLEIS Zootaxa Magnolia Press 43

8 TABLE 2. Morphological measurements of Chiasmocleis devriesi and C. ventrimaculata from the Amazon Conservatory for Tropical Studies (ACTS), Departamento de Loreto, Peru. All measurements are in mm. Species MHNSM Sex SVL HL HW IN EN ED IOD ThL TiL FL no. Chiasmocleis devriesi F C. ventrimaculata F C. ventrimaculata F C. ventrimaculata F C. ventrimaculata F C. ventrimaculata F C. ventrimaculata M C. ventrimaculata M (subad) C. ventrimaculata M (subad) The remaining 15 non-amazonian Chiasmocleis species are also substantially smaller than C. devriesi, have different color patterns, and in some species, extensively webbed feet and dermal spines (Boettger 1885, Boulenger 1888, Dunn et al. 1948, Dunn 1949, Bokermann 1952, Caramaschi & Cruz 1997, Cruz et al. 1997, 1999, 2007a,b, Caramaschi & Pimenta 2003, Canedo et al. 2004). Description of holotype. Skin above irregularly textured, almost smooth; skin below smooth. Occipital fold absent. Head narrower than body. Snout moderately pointed in dorsal view, most similar to Chiasmocleis panamensis (Fig. 7C of Zweifel 1986); rounded and projecting in lateral view; nostrils positioned laterally and directed laterally, at level of tip of lower jaw. Loreal region flat, sloping smoothly to upper jaw. Canthus rostralis rounded. Eyes small. Tympanum not apparent externally; supratympanic fold well developed, extending from posterior corner of eye to insertion of forearm. Skin beneath supratympanic fold bulging laterally. Suprascapula and associated musculature bulging dorsolaterally behind head. Relative length of fingers 3 > 4 = 2 > 1, tips rounded, not flattened or expanded, circumferential grooves absent; all fingers with lateral fringes, most developed on finger 3, webbing basal between all fingers; subarticular tubercles prominent, round to oval, raised; inner metacarpal tubercle oval, raised, one-half size of outer metacarpal tubercle; outer metacarpal tubercle oval, prominent, raised. Ulnar fold absent. Relative lengths of toes 4 > 3 > 5 > 2 > 1, tips rounded, not flattened or expanded, lacking circumferential grooves; lateral fringe present on all toes, most prominent on toes 3 and 4; toes webbed basally; subarticular tubercles prominent, round to oval, raised, more prominent proximally than distally; inner metatarsal tubercle distinct, oval; outer metatarsal tubercle barely visible. Tarsal fold suggested by pale line on outer surface of tarsus. Vent opening directed posteriorly, with moderate dorsal fold; crease present from vent opening to venter. Osteology of holotype. Dorsal and ventral views of the skeleton of the holotype are shown in the Computed Tomography (CT) scan (Fig. 2). Maxillary arch incomplete, maxilla and quadratojugal not in contact; alary process of premaxilla narrow, long, tilted slightly forward; palatal shelf of premaxilla with moderately sized notch; premaxilla, maxilla, and mandible lacking teeth. Anterior vomer narrow and long, in contact with sphenethmoid; neopalatine not distinguishable. Posteromedial processes of hyoid ossified, straight, and expanded posteriorly. Pectoral girdle with thin clavicle reaching approximately two-thirds length of coracoids, not reaching glenoid region; large medial gap between anterior ends of clavicles; clavicles curved away from midline. Eight presacral vertebrae; sacral vertebra articulating with the coccyx; sacral diapophyses broadly expanded, the width of the lateral margin being approximately 3 times the width of the base. Pelvic girdle broadly U-shaped. Phalangeal formula of hand with slightly expanded terminal phalanges; formula of foot Humerus with anterior flange and a short, rounded posterior process on proximal half. Coloration of holotype. In life (Fig. 1), dorsal and lateral surfaces dark gray with rusty red blotches posteriorly and on limbs; thin cream mid-dorsal stripe from level of the eyes to the vent; snout and eyelids 44 Zootaxa Magnolia Press FUNK & CANNATELLA

9 silver-gray. Line of several raised, white spots extending from posterior margin of eye to above insertion of arm. White flecks on dorsal surfaces of limbs, increasing distally. Hidden surfaces of limbs brown with white blotches. Ventral surfaces creamy white with large grayish brown blotches; blotches are largest on belly and chest, becoming smaller and more dense on throat and hindlimbs; blotches with light centers, particularly on belly and chest. Iris bright golden yellow. In preservative, dorsum of body gray with reddish brown tinge posteriorly; limbs similar, but with prominent mottling dorsally on forelimbs and slightly weaker mottling dorsally on hindlimbs; thin cream middorsal line extending from behind eyes to venter; on flanks, dorsal coloration blending smoothly into ventral coloration; venter pale creamy yellow with bold black-brown blotches with pale centers; mottling denser and finer on throat and ventral surfaces of limbs; anterior concealed surfaces of thighs with finer reticulate pattern; posterior concealed surfaces of thighs almost uniformly brown-gray; palmar and plantar surfaces uniformly gray. Measurements of holotype (in mm). SVL 42.2; HL 10.9; HW 12.5; IN 2.8; EN 2.9; ED 2.8; IOD 4.2; ThL 15.7; TiL 15.4; FL Measurements of the holotype and sympatric Chiasmocleis ventrimaculata are shown for comparison in Table 2. Etymology. The specific name is a noun in the genitive case and a patronym for Philip J. DeVries, one of the most influential researchers in tropical ecology and the person responsible for introducing WCF to tropical biology and the Amazon basin. Appropriately, DeVries long-term studies of Amazonian butterfly diversity (e.g., DeVries et al. 1999, 2008, DeVries & Walla 2001) have highlighted the ubiquity and importance of rare species, such as Chiasmocleis devriesi, in lowland Amazonian rainforests. FIGURE 4. Map showing the known distribution of Chiasmocleis devriesi at the Amazon Conservatory for Tropical Studies (ACTS) Field Station (indicated by star). Color shows elevation (white = below 200 m; light gray = m; dark gray = above 500 m). NEW SPECIES OF CHIASMOCLEIS Zootaxa Magnolia Press 45

10 Distribution and natural history. Chiasmocleis devriesi is only known from the holotype, found at the Amazon Conservatory for Tropical Studies (ACTS) Field Station, 65 km NE of Iquitos, Departamento de Loreto, Peru (Fig. 4). The holotype was collected in unflooded (terra firme) primary rainforest approximately 1.3 km SSE of the ACTS Field Station at 102 m elevation. It was found at 21:25 hrs on the ground in a lindero, a linear clearing of forest (approximately 5 10 m wide) demarcating a boundary between properties. WCF and C. Torres-Gastello searched the forests surrounding ACTS for several hours each day and night for three weeks, but only found this single representative of C. devriesi; the species is thus apparently rare at this site. The female had many small (approximately 1 mm diameter) mature, pigmented eggs. No typical microhylid breeding sites, such as ponds, swamps, or lakes, were in the immediate vicinity. Some small (approximately 2 5 m diameter), empty indentations, however, were observed on the forest floor which may fill in the rainy season, potentially serving as breeding sites. Other microhylids found at the ACTS Field Station were Chiasmocleis ventrimaculata, C. bassleri, Syncope antenori, and S. carvalhoi. Sequence divergence. Uncorrected sequence divergence between C. devriesi and C. ventrimaculata was 6.1% and between C. devriesi and C. bassleri was 11.9% at 12S-16S mtdna genes. This level of sequence divergence is higher than that seen (in the same genes) between recognized species that are well differentiated by call and morphological characteristics, providing additional evidence that these are distinct species. For example, mean corrected sequence divergence at 12S-16S genes between Physalaemus petersi and P. freibergi is 4.6% (Funk et al. 2007). Molecular markers have been useful in delineation of other cryptic Amazonian frog species as well (Fouquet et al. 2007). Discussion An obvious limitation of our description of C. devriesi is that it is based on a single female. Thus it is not possible to describe morphological variation within the species, including morphological differences between males and females. For example, some characters such as ventral coloration and size can be highly variable in Chiasmocleis and the observed differences in these characters between C. devriesi and similar species (such as C. ventrimaculata and C. avilapiresae) could represent opposite sides of a continuous distribution. Nonetheless, the high sequence divergence between C. devriesi and sympatric Chiasmocleis (C. ventrimaculata and C. bassleri) and a unique combination of morphological traits demonstrates that C. devriesi is a new, previously undescribed species. The recent discovery of C. devriesi and other new microhylids from the western Amazon basin (Altigius alios, Wild 1995; Syncope tridactyla, Duellman & Mendelson 1995; Otophryne pyburni, Campbell & Clarke 1998; Melanophryne carpish, Lehr et al. 2002; M. barbatula, Lehr & Trueb 2007; C. magnova, Moravec & Köhler 2007) highlights our incomplete knowledge of microhylid diversity in the region. The small number of individuals found for these descriptions (median = 3 per species) suggests that many remaining undescribed species are rare and/or inadequately sampled. In addition to the rarity of some microhylids, their fossorial nature makes them difficult to find. As with the forest canopy (Guayasamin et al. 2006), fossorial habitats are often overlooked by herpetologists and other field biologists. Even some of the best herpetologists neglect this poorly surveyed microhabitat of tropical forests. As stated in Lynch and Duellman (1997; pp ), Lynch is guilty of spending too much time gazing at vegetation in quest of dainty centrolenids and small Eleutherodactylus and will always be thankful to Thomas J. Berger for showing him large toadlike frogs on the ground along the stream where he had just passed; search images sometimes are so powerful that a frog weighing a half kilogram somehow is not seen. Future amphibian surveys of tropical forests should make a special effort to thoroughly survey fossorial and terrestrial habitats. Pitfall traps may be a particularly effective means of sampling microhylids. 46 Zootaxa Magnolia Press FUNK & CANNATELLA

11 Acknowledgements TERMS OF USE We thank C. Torres-Gastello for her assistance in the field; P. Jenson and S. Madigosky (Amazon Conservatory for Tropical Studies, Explorama Lodges) for providing accommodations in the field; K. Ramírez (Peruvian Instituto Nacional de Recursos Naturales [INRENA]) and J. Córdova (MHNSM) for assisting with permits; C. Aguilar and J. Córdova (MHNSM), R. Heyer and R. McDiarmid (USNM), and T. LaDuc (TNHC) for curatorial assistance; B. Caudle (UT Austin) for sequencing; R. Symula for checking specimens; and A. Angulo and two anonymous reviewers for providing comments on the manuscript. INRENA provided research and export permit numbers INRENA-IFFS-DCB and AG- INRENA. We acknowledge the National Science Foundation for funding from the IRCEB Grant to DCC. This is publication number 201 of the Yanayacu Natural History Research Group. This paper is dedicated to the inspiration provided by Hannah Wilcox Handy who passed away during the field excursion in which Chiasmocleis devriesi was discovered. References AmphibiaWeb (2009) Information on Amphibian Biology and Conservation. Berkeley, California: AmphibiaWeb. Available from (accessed 27 May 2009). Andersson, L.G. (1945) Batrachians from east Ecuador collected 1937, 1938 by Wm. Clarke-Macintyre and Rolf Blomberg. Arkiv för Zoologi, 37A, Boettger, O. (1885) Liste von Reptilien und Batrachiern aus Paraguay. Zeitschrift für Naturwissenschaften, 58, Bokermann, W.C.A. (1952) Microhylidae da coleção do Departamento de Zoologia (Amphibia-Anura). Papéis Avulsos do Departamento de Zoologia, Secretaria da Agricultura S. Paulo Brasil, 10, Boul, K.E., Funk, W.C., Darst, C.R., Cannatella, D.C. &. Ryan, M.J. (2007) Sexual selection drives speciation in an Amazonian frog. Proceedings of the Royal Society B: Biological Sciences, 274, Boulenger, G.A. (1888) A list of batrachians from the province Santa Catharina, Brazil. Annals and Magazine of Natural History, ser. 6, vol. 1, Campbell, J.A. & Clarke, B.T. (1998) A review of frogs of the genus Otophryne (Microhylidae) with the description of a new species. Herpetologica, 54, Canedo, C., Dixo, M. & Pombal, J.P. (2004) A new species of Chiasmocleis Méhely, 1904 (Anura, Microhylidae) from the Atlantic rainforest of Bahia, Brazil. Herpetologica, 60, Caramaschi, U. & Cruz, C.A.G. (1997) Redescription of Chiasmocleis albopunctata (Boettger) and description of a new species of Chiasmocleis (Anura: Microhylidae). Herpetologica, 53, Caramaschi, U. & Cruz, C.A.G. (2001) A new species of Chiasmocleis Méhely, 1904 from Brazilian Amazonia (Amphibia, Anura, Microhylidae). Boletim do Museu Nacional, Nova Série, Zoologia, 469, 1 8. Caramaschi, U. & Pimenta, B.V.S. (2003) Duas novas espécies de Chiasmocleis Méhely, 1904 da Mata Atlântica do sul da Bahia, Brasil (Amphibia, Anura, Microhylidae). Arquivos do Museu Nacional, Rio de Janeiro, 61, Carvalho, A.L. (1954) A preliminary synopsis of the genera of American microhylid frogs. Occasional Papers of the Museum of Zoology, University of Michigan, 555, Cruz, C.A.G., Caramaschi, U. & Izecksohn, E. (1997) The genus Chiasmocleis Méhely, 1904 (Anura, Microhylidae) in the Atlantic rain forest of Brazil, with description of three new species. Alytes, 15, Cruz, C.A.G., Caramaschi, U. & Freire, E.M.X. (1999) Occurrence of the genus Chiasmocleis (Anura: Microhylidae) in the State of Alagoas, north-eastern Brazil, with a description of a new species. Journal of Zoology, London, 249, Cruz, C.A.G., Caramaschi, U. & Napoli, M.F. (2007a) A new species of Chiasmocleis (Anura, Microhylidae) from the Atlantic rain forest of northeastern Bahia, Brazil. South American Journal of Herpetology, 2, Cruz, C.A.G., Feio, R.N. & Cassini, C.A. (2007b) Nova espécie de Chiasmocleis Méhely, 1904 (Amphibia, Anura, Microhylidae) da Serra da Mantiqueira, Estado de Minas Gerais, Brasil. Arquivos do Museu Nacional, Rio de Janeiro, 65, DeVries, P.J. & Walla, T.R. (2001) Species diversity and community structure in neotropical fruit-feeding butterflies. Biological Journal of the Linnean Society, 74, DeVries, P.J., Walla, T.R. & Greeney, H.F. (1999) Species diversity in spatial and temporal dimensions of fruit-feeding butterflies from two Ecuadorian rainforests. Biological Journal of the Linnean Society, 68, DeVries, P.J., Austin, G.T. & Martin, N.H. (2008) Diel activity and reproductive isolation in a diverse assemblage of NEW SPECIES OF CHIASMOCLEIS Zootaxa Magnolia Press 47

12 Neotropical skippers (Lepidoptera: Hesperiidae). Biological Journal of the Linnean Society, 94, Duellman, W.E. (1970) Hylid frogs of Middle America. Monograph of the Museum of Natural History University of Kansas, 1, Duellman, W.E. (1978) The biology of an equatorial herpetofauna in Amazonian Ecuador. Miscellaneous Publications of the Museum of Natural History University of Kansas, 65, Duellman, W.E. (2005) Cusco Amazónico. The lives of amphibians and reptiles in an Amazonian rainforest. Cornell University Press, Ithaca, New York, and London. Duellman, W.E. & Mendelson, J.R. (1995) Amphibians and reptiles from northern Departamento Loreto, Peru: taxonomy and biogeography. University of Kansas Science Bulletin, 55, Dunn, E.R. (1949) Notes on South American frogs of the family Microhylidae. American Museum Novitates, 1419, Dunn, E.R., Trapido, H. & Evans, H. (1948) A new species of the microhylid frog genus Chiasmocleis from Panama. American Museum Novitates, 1376, 1 8. Fouquet, A., Gilles, A., Vences, M., Marty, C., Blanc, M. & Gemmell, N.J. (2007) Underestimation of species richness in neotropical frogs revealed by mtdna analyses. Plos Biology, 2, e1109. Frost, D.R. (2009) Amphibian Species of the World: an Online Reference. Version 5.3 (12 February 2009). American Museum of Natural History, New York, USA. Available from index.php (accessed 27 May 2009). Funk, W.C., Caldwell, J.P., Peden, C.E., Padial, J.M., De la Riva, I. & Cannatella, D.C. (2007) Tests of biogeographic hypotheses for diversification in the Amazonian forest frog, Physalaemus petersi. Molecular Phylogenetics and Evolution, 44, Funk, W.C., Angulo, A., Caldwell, J.P., Ryan, M.J. & Cannatella, D.C. (2008) Comparison of morphology and calls of two cryptic species of Physalaemus (Anura: Leiuperidae). Herpetologica, 64, Funk, W.C., Cannatella, D.C. & Ryan, M.J. (2009) Genetic divergence is more tightly related to call variation than landscape features in the Amazonian frogs Physalaemus petersi and P. freibergi. Journal of Evolutionary Biology, 22, Guayasamin, J.M., Ron, S.R., Cisneros-Heredia, D.F., Lamar, W. & McCracken, S.F. (2006) A new species of frog of the Eleutherodactylus lacrimosus assemblage (Leptodactylidae) from the western Amazon basin, with comments on the utility of canopy surveys in lowland rainforest. Herpetologica, 62, IUCN, Conservation International, and NatureServe (2008) An Analysis of Amphibians on the 2008 IUCN Red List. Available from (accessed 27 May 2009). Lehr, E., Rodríguez, D. & Córdova, J.H. (2002) A new species of Phrynopus (Amphibia, Anura, Leptodactylidae) from the Cordillera de Carpish (Departamento de Huánuco, Peru). Zoologische Abhandlungen Museum für Tierkunde Dresden, 52, Lehr, E. & Trueb, L. (2007) Diversity among New World microhylid frogs (Anura: Microhylidae): morphological and osteological comparisons between Nelsonophryne (Günther 1901) and a new genus from Peru. Zoological Journal of the Linnean Society, 149, Lynch, J.D. & Duellman, W.E. (1997) Frogs of the genus Eleutherodactylus in western Ecuador: systematics, ecology, and biogeography. Special Publication of the Museum of Natural History University of Kansas, 23, Maddison, D.R. & Maddison, W.P. (2000) MacClade 4: Analysis of phylogeny and character evolution. Ver Sinauer Associates, Sunderland, Massachusetts. Méhelÿ, L.v. (1904) Investigations on Paraguayan batrachians. Annales Historico-Naturales Musei Nationalis Hungarici, 2, Mocquard, F. (1904) Description de quelques reptiles et d un batracien nouveaux de la collection du Muséum. Bulletin du Muséum National d'histoire Naturelle, Paris, 10, Moravec, J. & Köhler, J. (2007) A new species of Chiasmocleis (Anura: Microhylidae) from the Iquitos region, Amazonian Peru, with possible direct development. Zootaxa, 1605, Nelson, C.E. (1975) Another new miniature 4-toed South American microhylid frog (Genus: Syncope). Journal of Herpetology, 9, Nelson, C.E. & Lescure, J. (1975) The taxonomy and distribution of Myersiella and Synapturanus (Anura: Microhylidae). Herpetologica, 31, Parker, H.W. (1927) The brevicipitid frogs allied to the genus Gastrophryne. Occasional Papers of the Museum of Zoology, University of Michigan, 187, 1 6. Parker, H.W. (1934) A monograph of the frogs of the family Microhylidae. Trustees of the British Museum, 8, London, Parker, H.W. (1940) Undescribed anatomical structures and new species of reptiles and amphibians. Annals and Magazine of Natural History, ser. 11, vol. 5, Pauly, G.B., Hillis, D.M. & Cannatella, D.C. (2004) The history of a Nearctic colonization: molecular phylogenetics and biogeography of the Nearctic toads (Bufo). Evolution, 58, Zootaxa Magnolia Press FUNK & CANNATELLA

13 Peloso, P.L.V. & Sturaro, M.J. (2008) A new species of narrow-mouthed frog of the genus Chiasmocleis Méhelÿ 1904 (Anura, Microhylidae) from the Amazonian rainforest of Brazil. Zootaxa, 1947, Pyburn, W.F. (1975) A new species of microhylid frog of the genus Synapturanus from southeastern Colombia. Herpetologica, 31, Pyburn, W.F. (1976) A new fossorial frog from the Colombian rain forest (Anura: Microhylidae). Herpetologica, 32, Rodríguez, L.O. & Duellman, W.E. (1994) Guide to the frogs of the Iquitos Region, Amazonian Peru. Special Publication of the Museum of Natural History University of Kansas, 22, Schneider, J.G. (1799) Historiae Amphibiorum naturalis et literariae. Fasciculus Primus continens Ranas, Calamitas, Bufones, Salamandras et Hydros in genera et species descriptos notisque suis distinctos. Frederici Frommanni, Jena, p. i-xiii Swofford, D.L. (2000) PAUP*: Phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Sunderland, Massachusetts. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D. (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, Walker, C.F. (1973) A new species and genus of microhylid frog from Ecuador. Occasional Papers of the Museum of Natural History, The University of Kansas, 20, 1 7. Walker, C.F. & Duellman, W.E. (1974) Description of a new species of microhylid frog, Chiasmocleis, from Ecuador. Occasional Papers of the Museum of Natural History, The University of Kansas, 26, 1 6. Wild, E.R. (1995) New genus and species of Amazonian microhylid frog with a phylogenetic analysis of New World genera. Copeia, 1995, Zweifel, R.G. (1986) A new genus and species of microhylid frog from the Cerro de la Neblina region of Venezuela and a discussion of relationships among New World microhylid genera. American Museum Novitates, 2863, NEW SPECIES OF CHIASMOCLEIS Zootaxa Magnolia Press 49

14 APPENDIX 1. Specimens examined Arcovomer passarellii: BRAZIL: RIO DE JANEIRO: Itaguaí, USNM Chiasmocleis albopunctata: PARAGUAY: AMAMBAY: Parque Nacional Cerro Cora, USNM , Chiasmocleis avilapiresae: BRAZIL: RONDÔNIA: USNM Chiasmocleis bassleri: BRAZIL: RONDÔNIA: Nova Brasilia, USNM , PERU: LORETO: Amazon Conservatory for Tropical Studies, MHNSM , Chiasmocleis jimi: BRAZIL: PARÁ: Reserva Biológica do Rio Trombetas, USNM ; Itaituba, USNM Chiasmocleis mehelyi: BRAZIL: MATO GROSSO DO SUL: Miranda, USNM Chiasmocleis panamensis: PANAMA: CANAL ZONE, USNM Chiasmocleis shudikarensis: GUYANA: EAST BERBICE: Kwakwani, USNM Chiasmocleis ventrimaculata: PERU: LORETO: Amazon Conservatory for Tropical Studies, MHNSM , , 15775, MADRE DE DIOS: USNM , , , Ctenophryne geayi: GUYANA: EAST BERBICE, Kwakwani, USNM Elachistocleis ovalis: BRAZIL: MATO GROSSO: Pontes e Lacerda, USNM COLOMBIA: META: Villavicencio, TNHC Hamptophryne boliviana: PERU: MADRE DE DIOS: Manu, USNM HUÁNUCO: Iparia, TNHC 44562, 44565, 44569, Myersiella microps: BRAZIL: RIO DE JANEIRO, Teresópolis, USNM Nelsonophryne aequatorialis: ECUADOR: AZUAY: Cuenca, USNM Nelsonophryne aterrima: COSTA RICA: GUANACASTE: Tilarán, UNSM Otophryne pyburni: VENEZUELA: AMAZONAS: Río Negro, USNM Otophryne robusta: GUYANA: MAZARUNI-POTARO: Mt. Roraima, USNM Relictivomer pearsei: COLOMBIA: USNM Synapturanus mirandaribeiroi: GUYANA: MAZARUNI-POTARO, Mabura Hill, USNM Synapturanus salseri: COLOMBIA: VAUPÉS: Timbo, TNHC Syncope antenori: PERU: CUZCO: San Martín, USNM LORETO: Amazon Conservatory for Tropical Studies, MHNSM Syncope carvalhoi: PERU: LORETO: Amazon Conservatory for Tropical Studies, MHNSM 21669; Río Lagarto, USNM APPENDIX 2. GenBank accession numbers for 12S-16S mtdna sequences Species Museum number GenBank accession no. Locality Chiasmocleis devriesi MHNSM GQ Peru: Loreto: ACTS C. ventrimaculata MHNSM GQ Peru: Loreto: ACTS C. bassleri MHNSM GQ Peru: Loreto: ACTS 50 Zootaxa Magnolia Press FUNK & CANNATELLA