Slender Fingered Bladder Frog

Leptodactylus pentadactylus, the Smoky Jungle Frog, is a large frog. Adult males can reach 177 mm while the larger females can measure up to 185 mm (Savage 2002). This frog can be distinguished from other frogs by the presence of paired dorsolateral folds, paired lumbar glands, and a spotted or barred upper lip, as well as its large size (Savage 2002). This species has a smooth dorsum, definite inguinal glands, and large eyes and tympana (Savage 2002). The snout is rounded, almost semicircular when viewed from above (Savage 2002). Adult males have paired elongated vocal slits and a single internal subgular vocal sac (Savage 2002). In addition, adult males have extremely muscular forelimbs and a pair of black spines on the chest, plus a black spine on each thumb (Guyer and Donnelly 2005). Dorsolateral folds extend from each eye to the groin (Hero and Galatti 1990). The adult coloration has been described as either uniform gray to reddish brown, or with darker spots or bars on the ground color (Savage 2002), It has also been described as a dark purple and light brown reticulum (Guyer and Donnelly 2005). The underside is dark gray with white to yellow mottling or tiny white speckles (Savage 2002). The posterior thigh has small white spots on a black background. A dark interorbital bar is present (Guyer and Donnelly 2005). Young frogs are more brightly colored than adults and have toe ridges (Savage 2002). Tadpoles of this species are giant and elongate, growing up to 83 mm at stage 40 (Savage 2002; Hero and Galatti 1990). Dorsally, the tadpole is brown, with a lighter ventral surface (Savage 2002). The mouth is almost terminal, while the nostrils and eyes are on the dorsal side (Savage 2002). The spiracle is located laterally and sinistrally and the vent is medial (Savage 2002). This species has a long tail with low fins and a pointed tail tip (Savage 2002). The oral disk is complete and moderate, having two serrated beaks and 2/3 rows of denticles, with a broad gap in the row of denticles immediately above the mouth (Savage 2002). Labial papillae are lacking above the mouth, but are usually found in two rows lateral to the mouth and a single row ventral to the mouth (Savage 2002). The lateral line system is well-developed, particularly in comparison with larvae of other Leptodactylus species (Heyer et al. 1975).This species was featured as News of the Week on 12 February 2018:Heteromorphic sex chromosomes refers to sex chromosomes that differ in appearance and amount of genetic material. The traditional model of species exhibiting heteromorphic sex chromosomes is that they only have two pairs of sex chromosomes. While this is the common model in birds and mammals, amphibians are known to have a greater variation in sex determination from some species not exhibiting heteromorphic sex chromosomes at all to others with the traditional model of pairs. Gazoni et al. (2018) characterized the chromosomes of six female and seven male Leptodactylus pentadactylus, collected from the wild. They found that of the 11 pairs of chromosomes that the species has, more (six) pairs are sex chromosomes than autosomal. Among vertebrates, this is the largest number of sex chromosomes known in a species. Evidence also suggests that L. pentadactylus is part of a larger species complex and their findings may represent the effect of chromosomal rearrangements in the evolutionary process (Written by Ann T. Chang).

The Smoky Jungle Frog can be found from Honduras southward into South America. L. pentadactylus is widespread in lowland rainforest on both Atlantic and Pacific slopes of Costa Rica from sea level to 1,200 m (Leenders 2001). It prefers forest habitat near swamps and slowly flowing streams (Guyer and Donnelly 2005). It may also be found inhabiting areas distant from bodies of water (Galatti 1992).

These frogs can be long-lived and have a potential life-span of at least 15 years (Leenders 2001). Adults are nocturnal and stay in hiding during the day, sheltering in subterranean burrows, beneath logs, in the spaces between tree roots, or under houses (Savage 2002). Juveniles, however, are active during the day and can be found on top of the leaf litter (Savage 2002). This species prefers dimly lit forest (Jaeger and Hailman 1981). At the first sign of dusk, males of this species give off a loud "wrooop" (Leenders 2001). The call lacks pulses (Hero and Galatti 1990). Males are territorial and call sporadically from burrows located underneath a log or rock, often in densely vegetated areas (Leenders 2001). Mating is believed to take place throughout the rainy season months of May to November (Savage 2002). However, Hero and Galatti (1990) observed that males in the central Amazon region of Brazil began calling immediately after the first substantial rains, in late September, and that calling ceased after two to four weeks. Both calling and breeding take place at the water's edge; it is not known whether the same burrows used for shelter are also used as nest sites (Savage 2002). Amplexus is axillary in this species (Savage 2002). As the male hugs the female under the armpits with his robust forearms, he creates a large foamy mass around the eggs by rapidly moving his back legs through the jelly surrounding the fertilized eggs (Heyer and Rand 1977). This foam nest consists of a frothy mix of sperm, skin secretions, water, and air (Heyer and Rand 1977). Females lay about 1,000 light gray eggs, and the foam nests are constructed in dry cavities or depressions (Savage 2002). These hollows may be natural or possibly excavated by the males (Muedeking and Heyer 1976). Foam nests may be constructed near puddles, temporary pools or in seasonally flooded spots, such that rain washes the larvae out of the nests and into nearby small rain pools (Breder 1946). Alternatively, foam nests have been observed in open depressions at some distance from water, so that tadpoles develop within the nest until metamorphosis (Muedeking and Heyer 1976; Hero and Galatti 1990). In the latter case, Muedeking and Heyer (1976) noted both larvae and eggs in the nests, and inferred that eggs were being consumed by larvae. Leptodactylus pentadactylus larvae are unusually resistant to desiccation for anuran tadpoles, and can survive almost seven days out of water (Valerio 1971). Foam nests also provide protection to larvae from desiccation (Heyer 1969). Galatti (1992) observed that the strong seasonality in Leptodactylus pentadactylus reproduction in Brazil coincided with arthropod prey availability. He observed two peaks in arthropod abundance, one in late September (when the adults arrived at breeding sites), and the second in January and February, when tadpoles completed metamorphosis into juvenile frogs (Galatti 1992). These peaks did not completely correspond to rainfall, as the first peak in arthropod prey abundance occurred during the late dry season and the second occurred during the wet season (Galatti 1992). Leptodactylus pentadactylus is able to secrete huge amounts of mucus as an antipredator defense (Savage 2002). In addition to making the frog slippery and difficult to hold, the skin secretions are toxic (Savage 2002). Savage (2002) points out that this toxicity is evident both from direct contact (resulting in human skin rashes and stinging) and indirect contact, from being in the same room when the frog is handled (which results in sneezing and swelling of human eyes and mucus membranes). The residue from these skin secretions is lethal to other frogs which come in contact with it (Savage 2002). Leptodactylus pentadactylus also exhibits defensive behavior, which consists of facing the predator, inflating and elevating the body with all four limbs (Villa 1969; Savage 2002). This has the effect of raising the posterior, glandular surfaces above the level of the head since the hind limbs are longer (Villa 1969; Savage 2002). Initial elevation is followed by repeated raising and lowering of the body (Villa 1969; Savage 2002). These frogs are opportunistic feeders. Adults consume anything that they can swallow, including bird chicks, snakes, other frogs (particularly dendrobatids, despite their toxicity), and scorpions (Leenders 2001). Tadpoles initially feed on the foam produced by the male, but later will either eat algae (Vinton 1951) or become carnivorous, preying on eggs and tadpoles of their own species or other species (Muedeking and Heyer 1976; Heyer et al. 1975). Predators on Leptodactylus pentadactylus eggs include the ephydrid fly Gastrops willistoni, which lays its own eggs on L. pentadactylus clutches in Costa Rica and Brazil (Villa et al. 1982). Predators on the adult frogs include coatimundis, snakes, and caimans. When discovered, these frogs often remains still and easily approached. If caught, however, they will emit an extremely loud, high-pitched scream to startle potential predators (Leenders 2001). Research has shown that these frogs have an accurate visual image of their surroundings, though it is not known exactly what cues they use for orientation (Leenders 2001). Frogs taken from their burrows and displaced over short distances have managed to return to their burrow in a straight line (Leenders 2001). Adult Leptodactylus pentadactylus are negatively phototactic (avoid light), unlike most anurans (Kicliter and Goytia 1995).

Leptodactylus pentadactylus is not endangered. This species is fairly common (Savage 2002).

These frogs have been reported to be occasionally consumed by Amazonian people (Leenders, 2001)[3324]. The karyotype is 2N=22 (Bogart 1974).

Maximum longevity: 18.8 years (captivity)

Leptodactylus pentadactylus (Laurenti)

MATERIALS.—USNM uncatalogued (single specimen dissected, stage 34, SVL 18.4 mm). Collected from 6 km west of Turrialba, Cartago, Costa Rica. Specimen subsequently destroyed in SEM preparation.

REFERENCES.—External descriptions are in Heyer (1970, 1979). Discussions of ecology, habitat occurrence, and facultative carnivory are found in Heyer, McDiarmid, and Weigmann (1975) and Muedeking and Heyer (1976).

GENERAL

Leptodactylus pentadactylus (Laurenti), 1768

Rana pentadactyla Laurenti, 1768:32. [Type-locality: “Indiis.” Type: based on pl. 75: fig. 1 in Seba, 1734.]

Rana gigas Spix, 1824:25. [Type-locality: Amazon River, Brazil. Type: lost.]

Rana coriacea Spix, 1824:29. [Type-locality: Amazon River, Brazil. Type: lost.]

Leptodactylus goliath Jiménez de la Espada, 1875:57. [Type-locality: Archidona and Chinitambo, Sierra de Guacamayos, Oriente, Ecuador. Lectotype: Museo Nacional, Madrid, 328, adult female.]

Leptodactylus macroblepharus Miranda-Ribeiro, 1926:144. [Type-locality: Manaos, Amazonas, Brazil. Holotype: MZUSP 377, adult male.]

Leptodactylus pentadactylus dengleri Melin, 1941:51. [Type-locality: Roque, San Martin, Peru. Holotype: Naturhistoriska Muséet, Göteborg.]

Leptodactylus pentadactylus rubidoides Andersson, 1945:47. [Type-locality: Río Pastaza, Santiago-Zamora and Napo-Pastaza border, Ecuador. Holotype: Stockholm Royal Museum.]

DIAGNOSIS.—Individuals of L. pentadactylus have a distinctive pair of dorsolateral folds. Dorsolateral folds are also found in some or all individuals of fallax, flavopictus, labyrinthicus, kundseni, rhodomystax, rhodonotus, rugosus, and stenodema. Leptodactylus pentadactylus lack distinct light lip stripes; all flavopictus and rhodomystax individuals have distinct light upper lip stripes. Most rugosus lack dorsolateral folds; when present, the folds are interrupted, contrasting with the continuous folds found in pentadactylus. Leptodactylus pentadactylus is a large species (minimum adult SVL 106 mm) with a single thumb spine in males; rhodonotus is a moderate-sized species (maximum adult SVL 90 mm) with two thumb spines per hand in males; stenodema is a moderate-sized species (maximum adult SVL 100 mm) in which the males lack thumb spines. Leptodactylus pentadactylus most closely resembles fallax, labyrinthicus, and knudseni in the pentadactylus group. A fold from above the tympanum to the side of the body, usually dark outlined for the extent, is found in pentadactylus; this fold is absent in fallax, labyrinthicus, and knudseni.

ADULT CHARACTERISTICS (N=173).—Dorsum uniform, spotted, or barred (Figure 1, A–D, G, J); lip uniform or usually with dark triangular bars (Figure 2, A–C, E, J); posterior surface of thigh uniform or variously spotted and mottled (Figure 3, A–G, I-K, P, R, S); upper tibia distinctly or indistinctly broadly barred (Figure 4, A, C, E); 2 distinct, dark outlined dorsolateral folds from eye to sacrum; dark outlined fold from eye to over tympanum, dark outline continuing or not on continuation of fold to shoulder; dark outlined fold from above tympanum to side of body usually continuous, rarely interrupted in Middle American specimens; males with one thumb spine per hand, rarely a weakly developed second; upper tibia and distal tarsal surfaces smooth or with scattered to many white- or black-tipped tubercles; sole of foot smooth, rarely with scattered white tubercles; female SVL 148.1±14.7 mm, maximum 176.2 mm, male SVL 137.2±14.0 mm, 185.0 mm maximum; female interorbital distance/head length ratio 0.19±0.02, male 0.19±0.02; female eye-nostril distance/head length ratio 0.25±0.01, male 0.25±0.01; female head length/SVL ratio 0.37±0.01, male 0.38±0.01; female head width/SVL ratio 0.39±0.02, male 0.39±0.02; female femur/SVL ratio 0.42±0.03, male 0.42±0.02; female tibia/SVL ratio 0.45±0.02, male 0.44±0.02; female foot/SVL ratio 0.46±0.02, male 0.45±0.02.

DISTINCTIVE COLORS IN LIFE.—Posterior surfaces of thigh mottled black and white or black and gray, most distinctive in juveniles (Villa, 1972, from Nicaragua; R. W. McDiarmid color notes from Peruvian specimen).

LARVAL CHARACTERISTICS.—Eye diameter 7–13 percent head-body length; oral disk position anterior; oral disk entire; oral disk width 15–22 percent head-body length; anterior oral papilla gap 50–74 percent oral disk width; anterior split tooth row about ⅓ length of entire anterior tooth row; 45–67 denticles in split tooth row anterior to beak; tooth row formula head body length 28–39 percent total length; maximum total length, stage 40, 83 mm.

MATING CALL.—Dominant frequency modulated between 250–500 Hz (Figure 12); no harmonic structure in call; call barely pulsed (Costa Rica), partially pulsed (Panama, Barro Colorado Island), or pulsed (Ecuador), (Figure 13); call duration 0.22–0.33 s (Figure 13).

KARYOTYPE.—Diploid number 22, 2 pair median, 6 pair submedian, 3 pair subterminal (Heyer and Diment, 1974).

DISTRIBUTION (Figure 14).—Middle America from Honduras south into South America; in South America, the species occurs in coastal Colombia and Ecuador and the Amazon Basin.

BRAZIL. AMAZONAS: Benjamin Constant (MNRio 1743, 1751(2), 2559); Ducke Reserve (KU 129945); Fonte Boa, Alto Solimões (MNRio 796); Igarapé Belém, Rio Solimões (MZUSP 24897); São José (Jacaré), Rio Solimões (MZUSP 40303). MARANHÃO: Rio Aurá (CAS-SU 11830). PARÁ: Canindé, Rio Gurupi (MZUSP 25010–11); Furo do Panaquera (MZUSP 35677); IPEAN (KU 127400, 128336); Marambaia (KU 140094); Monte Cristo, Rio Tapajóz (MZUSP 38956); Óbidos (MZUSP 22126); Rio Mapuera, at Equator (AMNH 49482); Sudam Floral Reserve, 74 km SE Santarem (KU 129944).

COLOMBIA. AMAZONAS: Leticia (USNM 147053). ANTIOQUIA: Chigorodó, near Turbo (USNM 153914); Finca Chibiquí, 5 km W, Río Arquia (LACM 51211). CHOCÓ: Boca de Raspadura (AMNH 39792); Condoto (UMMZ 121418); Playa de Oro, 2 km above, upper Río San Juan (FMNH 54707). MAGDALENA: Parque Nacional Tayruna, trail between Canaveral and El Pueblito (USNM 200376). META: Río Guayabero, Angostura (USNM 150490); San Juan de Arama, Los Micos (FMNH 81329); about 30 mi WNW Vista Hermosa Caño Sardinata (UTA 5233–34). PUTUMAYO: About 15 km airline SW Mocoa, 1180 m (AMNH 84865). VALLE: Río Anchicaya, 8 km W Danubio, 300 m (KU 169090); Río Calima (USNM 150756); lower Río Calima (USNM 145094); Río Raposo, Virology Field Sta, (USNM 151460–61). VAUPÉS: Río Ariari and Río Guaviari (UTA 2719, 5232).

COSTA RICA. CARTAGO: La Suiza (KU 25713–14, 28188); Moravia de Turrialba (KU 30407, 65709, UTA 1395); 2.7 mi NE Río Reventazon Bridge, Peralta Rd, 3100’ (UMMZ 117274–76); Tunnel Camp, near Peralta (KU 33165, 33167); Turrialba (AMNH 54485, 62251, FMNH 57532, 101800, 101802, KU 30408–11, 65707–08, USNM 29953–54); 10 mi S Turrialba (USNM 192577). HEREDIA: Puerto Viejo and vicinity (KU 33135–39, 33144–52, 65710–12). LIMÓN: Guapiles (MCZ 7981–84); La Lola (KU 34967, UMMZ 117277); Los Diamantes (FMNH 101797, 101799, KU 25716–18, 30405–06(3), 65706); Puerto Viejo (KU 35924); Suretka (KU 35927, UMMZ 124019, 135387, 135392); Tortuguero (AMNH 75098–5100, MCZ 29134). PUNTARENAS: Agua Buena (KU 34965, 35928–29); Esterillos Oeste, 15 km SE Jacó (KU 33153, 34968–69, 65715–17, TCWC 19305–06); Gromaco (UMMZ 123320); Rincón de Osa and vicinity (LACM 116317, USNM field 1628, 1630–31, 1634, 1641, 1663, 1666–68, 1682); Villa Neily and vicinity, 75 m (KU 65713–14, 100338–39, 100354). SAN JOSÉ: El General (KU 25715); San Isidro del General 2½ mi E (FMNH 101801); 13 mi WSW San Isidro del General on Dominical Rd, 710 m (KU 34966, 35925–26, LACM 114334).

ECUADOR. COTOPAXI: Region of Sigchos (USNM 196743). ESMERALDAS: Hacienda Equinox, 30 km NNW Santo Domingo de los Colorados, 1000’; (USNM 196739). MORONA-SANTIAGO: Cusuime, 320 m (AMNH 93705–06). NAPO: Dureno, 320 m (KU 104714); Lago Agrio, 340 m (KU 126258–59, UMMZ 129062); Limoncocha (KU 99040, LACM 92128–31); Puerto Libre, Río Aguarico, 570 m (KU 122579); Santa Cecilia (KU 104713, 104715, 104717–18, 109152–53, 111405, 111408–09, 122574–75, 122577, 122580, 126257, 146176–80, 149354–58; MCZ 57944–46, 57948–52, 57954–56, 57959–60, UMMZ 129280–81). PASTAZA: Andoas (AMNH 71025); Canelos (USNM 196742); 2 km E Puyo (USNM 196741(2)); headwaters of Río Arajuno, tributary of Río Napo (USNM 196744); Río Pindo (USNM 196747); Río Rutuno, tributary of Río Bobonaza (USNM 196746). PICHINCHA: Espinosa, 9 km W Santo Domingo de los Colorados, road to Chone (CAS-SU 10453–54); 18 km W Santo Domingo de los Colorados, Ramsey Farm, km 19 Chone Rd. (USNM 196740(2), 196745).

FRENCH GUIANA. Sophie (MCZ 44562).

GUYANA. Rupununi, N of Acarahy Mts (KU 69685); Shudi-kar-wau (AMNH 70118–20).

HONDURAS. COLON: Belfate (AMNH 45704, 45722).

NICARAGUA. BLUEFIELDS: 6 mi W Rama, 50’ (TCWC 19307). GRANADA: N Granada (LACM 37870). MATAGALPA: 10.5 km N Finca Tepeyac, 9 km E Matagalpa, 960 m (KU 85146). RÍO SAN JUAN: San Juan del Norte (Greytown) (USNM 19765). ZELAYA: Bonanza (KU 85147–48, 101168); Camp Corozo, Río Huahuashan (AMNH 54980–81); Camp Santa Ana, Río Huahuashan (AMNH 54999); Cara de Mono, 50 m (KU 112673–75); Masawas, Waspuk R (AMNH 58435); El Recreo, 25 km W Rama (KU 112666–72, LACM 13945, 20475); 10 mi above Recreo, Río Mico (UMMZ 79751–52).

PANAMA. BOCAS DEL TORO: Almirante (KU 79992, USNM 142334); Boca del Drago (USNM 142318); Punta de Peña (USNM 38714). CANAL ZONE: Barro Colorado Island (AMNH 52878–79, 69728, FMNH 175986, KU 76568, MCZ 15266, UMMZ 64594, 124019, 135387, 135392, USNM 161151); Candelaria and Peluca Stas, near Boqueron (AMNH 53747); Cave A, Chili Brillo (AMNH 62338); Frijoles (USNM 196303); Las Cruces trail near Corozal (AMNH 38977); near Madden Dam (AMNH 87143, KU 155306, UMMZ 78481). CHIRIQUÍ: Progreso (UMMZ 58221). COCLÉ: El Valle, 560 m (AMNH 59590, KU 76575, 107229, 116825.) DARIÉN: Camp Creek, Camp Townsend (AMNH 40785–88, 40793, 41061, 41765); Casita (USNM 141783); Jaqué (USNM 161215); Laguna, 820 m (KU 76570–72); along Río Canglón, near mouth (UMMZ 123160–61); across from mouth of Río Canglón, along Río Chucunaque (UMMZ 123158–59); Río Chucunaque, about 7 km above Río Mortí, 150 m (KU 107230); Río Silugandí (UMMZ 124018); Río Tuira at Río Mono (KU 115308); Río Ucurgantí, about 7 km above mouth, 30 m (KU 97014–17), 107231–32); Tacarcuna, 550 m (KU 76573–74). LOS SANTOS: Guánico Arriba, 60 m (KU 107228). PANAMÁ: Altos de Maje (AMNH 88743); Cerro Campana (KU 76569); Ciricito (CAS 71514–16); Juan Mina, Chagres R (USNM 129908); Tapia (AMNH 18920, 18922–23). SAN BLAS: Armila (USNM 150090); Camp Sasardí, 12 m (KU 108688–89); Quebrada Venado (USNM 150089). VERAGUAS: Mojara (UMMZ 123320); mouth of Río Concepción, 1 m (KU 11537).

PERU. AYACUCHO: La Mar, Candalosa (FMNH 39720). HUANUCO: Ganzo Azul (FMNH 45145); Río Llullapichis, 4–5 km upstream from Río Pachitea (KU 171901). LORETO: Cashiboya (AMNM 42404); Iquitos (AMNH 42002, 42560); Peru-Brazil border, upper Utoquinea (AMNH 42751, 43371); 61 mi SE Pucallpa, 500’ (TCWC 4967); Río Pisqui (AMNH 43539); Río Ucayali, Yarinacocha (FMNH 56293, 56300). SAN MARTÍN: Upper Biabo Valley (AMNH 42656); Pachisa (AMNH 42001); Tocache Nuevo, Río Huallaga (AMNH 42562).

SURINAM. Godo Drai (TCWC 23561–63); King Frederick William IV Falls (FMNH 30912–13).

The smoky jungle frog (Leptodactylus pentadactylus) is a species of frog in the family Leptodactylidae. It is found in Bolivia, Brazil, Colombia, Ecuador, Costa Rica, Panama, French Guiana, and Peru. Its natural habitats are tropical and subtropical moist broadleaf forests, subtropical or tropical swamps, subtropical or tropical moist montane forest, rivers, freshwater marshes, intermittent freshwater marshes, and aquaculture ponds.