Chiasmocleis devriesi Funk & Cannatella

Funk, Chris & Cannatella, David C., 2009, A new, large species of Chiasmocleis Méhelÿ 1904 (Anura: Microhylidae) from the Iquitos region, Amazonian Peru, Zootaxa 2247, pp. 37-50 : 38-46

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.

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 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 17–18 mm in C. magnova ; 20 mm in C. hudsoni ; 21–23 mm in C. jimi ; 25 mm in C. shudikarensis ; 20–28 mm in C. bassleri ; 25–30 mm in C. anatipes ; 21–34 mm in C. ventrimaculata ; and 24–38 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).

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 21540 F 42.2 10.9 12.5 2.8 2.9 2.8 4.2 15.7 15.4 14.8

C. ventrimaculata 21539 F 34.4 8.7 9.4 2.4 2.6 2.1 3.8 13.4 13.7 13.8

C. ventrimaculata 15697 F 27.8 8.1 8.4 2.2 2.4 2.1 2.9 11.4 11.3 11.2

C. ventrimaculata 15775 F 26.9 7.3 7.5 2.0 2.3 2.0 3.1 10.2 10.3 10.5

C. ventrimaculata 15698 F 26.3 7.6 7.4 2.1 2.6 2.2 2.9 10.6 10.1 10.7

C. ventrimaculata 15700 F 23.2 6.3 6.3 1.9 2.2 2.2 2.8 8.9 9.7 10.2

C. ventrimaculata 21538 M 23.2 7.6 6.9 1.9 2.0 1.6 2.8 10.2 10.1 9.7

C. ventrimaculata 15702 M (subad) 17.1 5.7 5.7 1.7 1.6 1.8 2.3 7.5 7.9 7.5

C. ventrimaculata 15701 M (subad) 16.5 5.1 5.6 1.4 1.6 1.8 2.1 6.6 6.9 6.9 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 2-2-3-3 with slightly expanded terminal phalanges; formula of foot 2-2-3-4-3. 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 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 14.8. 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.

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. f re i b e rg i 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).

Figures

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.

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.

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 = 200 – 500 m; dark gray = above 500 m).

Tables

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	3 SVL	Ƥ SVL	Head shape	F o ot webbing	Occip. fold	Tymp.	N o. toes
Adelastes hylonomos Zweifel 1986	St a t e o f A ma z on a s i n so u t h e r n Venezuela	25-29	?	Rounded	None	-	-	5
Altigius alios Wild 1995	Departamento de Madre de Dios in southeastern Peru and northeastern Bolivia	49.5	?	Rounded	Extensive	+	-	5
Chiasmocleis anatipes Walker & Duellman 1974	Eastern Ecuador, northeastern Peru	18–20	25–30	Rounded	Extensive	-	-	5
C. avilapiresae Peloso & Sturaro 2008	Amazonian Brazil south of Amazon River	22–27	24–38	Triangular	E xt e ns i ve i n m al es; b as al i n females	-	-	5
C. bassleri Dunn 1949	Amazonian Ecuador, Peru, Bolivia, and adjacent Brazil and Colombia	17–22	20–28	Rounded	None	-	-	5
C. devriesi sp. nov.	Near Iquitos, Departamento de Loreto, northeastern Peru	?	42	Moderately pointed	B a s a l i n females	-	-	5
C. magnova Moravec & Köhler 2007	Near Iquitos, in Loreto, northeastern Peru	?	17–18	Rounded	Basal	-	-	5
C. shudikarensis Dunn 1949	Guyana, Surinam, French Guiana, and Amazonian Brazil	25*	25*	Truncate	E xt e ns i ve i n m al es; b as al i n females	-	-	5
C. ventrimaculata (Andersson 1945)	Amazonian Ecuador, Peru, Bolivia, southeastern Colombia, and far western Brazil	20–23	21–34	Rounded	Basal	-	-	5
Ctenophryne geayi Mocquard 1904	Amazonian Venezuela, Colombia, Ecuador, Peru, Bolivia, Brazil, and all of Guyana, Suriname, and French Guiana	32–43	42–55	Truncate	Extensive	+	-	5
Elachistocleis ovalis (Schneider 1799)	Panama and Colombia southward, east of the Andes, to Argentina; Trinidad	24–33	33–44	A c u t e l y rounded	Basal	+	-	5
Hamptophryne boliviana (Parker 1927)	Northern and western sides of the Am az on bas i n: St a t e of Bo l i va r (Venezuela), French Guiana, Suriname, Guyana, Brazil, Ecuador, Peru, Bolivia, and Colombia	34–39	39–44	Rounded	None	-	-	5
Otophryne pyburni Campbell & Clarke 1998	Vaupés and Amazonas, Colombia, across Venezuelan lowlands through Guianan region to Amapás, Brazil	46–55	52–61	Pointed	Basal	-	+	5
Synapturanus mirandaribeiroi Nelson & Lescure 1975	Northern Brazil, eastern Colombia, and the Guianas	27–32	25–35	Pointed	None	+	+	5
S. rabus Pyburn 1976	SE Vaupés, Colombia, adj. Ecuador	16–17	18–19	Pointed	None	+	+	5
S. salseri Pyburn 1975	Va upés, Colom bia, Am az onas, Venezuela, Manaus, Brazil	24–26	?	Pointed	None	+	-	5
Syncope antenori Walker 1973	Amazonian Ecuador and Peru	11–12	13–14	Truncate	None	-	+	4
S. carvalhoi Nelson 1975	Loreto, Peru, adj. southern Amazonian Colombia	9–10	10–11	Truncate	None	-	-	4
S. tridactyla (Duellman & Mendelson 1995)	Loreto, Peru, western Brazil	?	12	Truncate	None	-	+	4