A small dendrobatid species (18-22 mm) with granular skin (Savage 2002). The typical color of the back and the upper arms is bright orange (Savage 2002). The belly, lower arms and the hind legs are green to blue-green (Savage 2002). Calling males have a black vocal pouch (Goodman 1971). In the area of Quepos, Costa Rica, this species has an olive-colored dorsum (Meyer 1996).
A stage 28 tadpole was collected after deposition was observed and was described by van Wijngaarden and Bolaños (1992). Total length at stage 28 was 17.8 mm and body length was 5.8 mm. For a different specimen at stage 39 the total length was 25 mm and the body length was 8.5 mm. Tail length was consistently 67% of body length from stage 25 to stage 39. The tadpole has a depressed body. The snout is rounded in dorsal view at all stages, but different specimens varied in profile from "edge-shaped" at stage 25 to rounded at stages 26-34, to truncate in stages 27 and 39. Nostrils are dorsal and are directed laterally. Eyes are dorsal and directed dorsolaterally. Mouth is anteroventral. Oral disc is not emarginate. Dental formula is 1/1. Labial teeth are present in a single anterior row (A1) and single posterior row (P1); A1 is irregularly interrupted while P1 is continuous and longer than A1. Anterior jaw sheath is widely arched with slender marginal processes and finely serrated; the posterior jaw sheath is also arched and finely serrated. Jaw sheath keratinization was incomplete at stages 25-27. Single row of large marginal papillae borders the posterior labium. The spiracle is low and sinistral and the vent is medial. Tail fins are equal in height; the dorsal tail fin does not extend onto the body. Tail tip is attenuated in the specimen described by van Wijngaarden and Bolaños 1992, but has been reported as rounded by other workers (Silverstone 1975; see van Wijngaarden and Bolaños 1992). Meyer (1993) observed that the tadpoles have epidermal tubes at the tail base, the function of which is unknown, but van Wijngaarden and Bolaños (1992) did not report this feature.
According to van Wijngaarden and Bolaños (1992), the only sympatric congener of O. granulifera is Dendrobates auratus and the larger tadpoles of D. auratus have a denticle formula of 2(1)(2)/3 and two rows of smaller papillae, in contrast to those of O. granulifera, where the denticle formula is 1/1 and there is a single row of large papillae. Myers et al. (1995) also reported Oophaga pumilio to be in sympatry with O. granulifera.
In life and in preservative, tadpole coloration is suffused with gray that lightens from the dorsum to the venter (van Wijngaarden and Bolaños 1992).
Distribution and Habitat
Country distribution from AmphibiaWeb's database: Costa Rica, Panama
Oophaga granulifera occurs mainly in southwestern Costa Rica, on low mountains near Puntarenas, Costa Rica, at elevations from 20 m - 100 m above sea level (Meyer 1992, 1993; Savage 2002; Stuart et al. 2008). Its range extends down into the adjacent southwestern region of Panama (Young et al. 1999; Ibañez et al. 2000). It has also been found in much smaller numbers along the Atlantic Coast, in a region of southeastern Costa Rica adjacent to Panama (Myers et al. 1995). It occurs in humid lowland forest, near streams, and has been reported from both undisturbed primary forest (Meyer et al. 1993; Miller and McFarlane 2008) and secondary forest (van Wijngaarden and Bolaños 1992; Miller and McFarlane 2008) as well as plantations (Stuart et al. 2008) and bamboo habitat (Miller and McFarlane 2008). However, it appears to be far more common in primary forest (Meyer et al. 1993; Miller and McFarlane 2008).
Life History, Abundance, Activity, and Special Behaviors
Like most other dendrobatid frogs, the Granular Poison Frog is diurnal and terrestrial, protected from predation by its aposematic coloration. This species is highly territorial (Goodman 1971; Crump 1972; Bolaños 1990; van Wijngaarden and van Gool 1994), showing male-male physical aggression (Goodman 1971; Crump 1972). Territoriality in this species involves defending calling sites and oviposition sites (Bolaños 1990), and is vocally mediated (van Wijngaarden and van Gool 1994). Color recognition may not be a key factor in male-male or intraspecies recognition in O. granulifera, since an O. granulifera male was observed to attack both a female O. granulifera and a similar-sized but cryptically-colored Eleutherodactylus that were positioned near a loudspeaker during the playback of male vocalizations (van Wijngaarden and van Gool 1994).
Although Myers and Daly (1976) characterized this species as calling "incessantly," Bolaños et al. (1990) found a bimodal calling pattern, with the most active calling period in early morning and a second calling period in the last hour before dusk. Males observed in a three-week study by van Wijngaarden and van Gool (1994) had one to three fixed calling sites and occupied those sites more frequently between the hours of 5 am and 10 am than after 10 am. Calling sites are elevated, 0.7 m to 1.5 m above the ground (van Wijngaarden and van Gool 1994; Crump 1972; Goodman 1971). Meyer (1993) states that the courtship call is distinguished from that of other dendrobatid species by its long notes, while Myers and Daly (1976) describe the advertisement call as a "chirp" call rather than the buzz call used by some other species of dendrobatids. According to Myers and Daly (1976), chirp calls are a series of harsh and not well-modulated notes, with rapid pulses that cannot be resolved on wide-band sound spectrograms. Meyer (1996) noted differences in advertisement call structure among south to central Costa Rican populations
of this species.
During the rainy season, receptive females approach calling males, who then lead the females to an oviposition site (Crump 1972; van Wijngaarden and van Gool 1994). Males sometimes continue to call softly while leading the female (van Wijngaarden and van Gool 1994). Eggs are laid on dead, curled-up leaves that are elevated and covered by other leaves; oviposition sites were observed to be in twig forks at 0.15-0.2 m above ground, between stones on a boulder at 0.5 m, and in a bromeliad leaf axil, about 2.5 m above the calling site on a tree (van Wijngaarden and van Gool 1994). Clutches laid by members of the D. histrionicus species group usually consist of 3-4 eggs (Crump 1972; van Wijngaarden and van Gool 1994). Males attend the clutch and perform hydric brooding on a daily basis, moistening the eggs periodically with water from the bladder (Meyer 1992; Meyer 1993). Females continue to lay small clutches of fertilized eggs until the first clutch hatches (Meyer 1993). At that point the female transports her tadpoles to water-filled sites in plants (Meyer 1993). Tadpoles are usually transported one at a time but occasionally a female will transport two tadpoles at once (van Wijngaarden and Bolaños 1992). Tadpole brooding sites observed in the wild by van Wijngaarden and Bolaños (1992) included a leaf axil of a Heliconia plant, 0.15 m above the ground; the broken stem of a palm tree, 0.8 m above ground; leaf axils of various species of Dieffenbachia plants, 0.6-0.95 m above ground; the broken stem of a shrub, 1.5 m above ground; and in a bromeliad (Guzmania sp.), 3.0 m above ground. For the six observed Dieffenbachia tadpole brooding sites, the mean water volume was found to be 2.4 ml (van Wijngaarden and Bolaños 1992). Tadpoles were generally found singly (n=10), but on one occasion two tadpoles were found in the same brooding site (van Wijngaarden and Bolaños 1992).
Larvae are oophagous; the female visits each plant axil and lays unfertilized eggs to provide nutrition for the growing tadpoles (Meyer 1993). The tadpoles perform a complicated swimming behavior that appears to signal the female to lay the nutritive eggs (Meyer 1993). In the wild, under natural conditions, development takes approximately 80 days; in captivity when fed with chicken egg yolk, development requires about 200 days, and some of the captive larvae are only able to metamorphose when also fed thyroxin (Meyer 1993).
During the dry season (January to April) it is difficult to find any individuals. Bolaños et al. (1990), during a one-year study, found that O. granulifera left the study area in the dry season but returned in the wet season.
Trends and Threats
Although Oophaga granulifera is still relatively common in southwestern Costa Rica, its population is declining (Stuart et al. 2008). In southeastern Costa Rica it is considerably less common than its congener O. pumilio, with Myers et al. (1995) observing only four individuals of O. granulifera for every hundred O. pumilio. The habitat of this species is fragmented, and is under threat of becoming further fragmented due to forest destruction (Stuart et al. 2008). Logging, agriculture, and expanding human settlement thus present the greatest threats (Stuart et al. 2008). Although Meyer et al. (1993) did not find this species outside of closed primary rainforest or away from fast-flowing streams, it has been reported from secondary forest (van Wijngaarden and Bolaños 1992) and plantations as well (Stuart et al. 2008). However, Miller and McFarlane (2007) reported that densities were considerably lower in secondary forest and considered secondary forest likely to be unsuitable habitat. The range overlaps with several protected areas, including Parque Nacional Corcovado (Summers 2000) and the Firestone Reserve (Miller and McFarlane 2008) in Costa Rica.
Relation to Humans
Oophaga granulifera is captured for the pet trade, despite the toxicity of its skin (see Daly et al. 1978 and numerous other publications by Daly and Myers for toxins found in this species). Captive breeding of O. granulifera was accomplished for the first time in 1992 (Meyer 1992).
Possible reasons for amphibian decline
General habitat alteration and loss
Habitat modification from deforestation, or logging related activities
A Spanish-language species account can be found at the website of Instituto Nacional de Biodiversidad (INBio).
The karotype is 2n=20 (Rasotto et al. 1987).
This species was transferred to the genus Oophaga by Grant et al. (2006) and subsequently back to the genus Dendrobates by Santos et al. (2009). In 2011, the genus Dendrobates was subdivided into seven genera, including the new genus Oophaga by Brown et al (2011).
Bolaños, F. (1990). 1990): Actividad de Canto y Territorialidad en Dendrobates granuliferus Taylor 1958. Thesis. Universidad de Costa Rica, Sistema de Estudios de Posgrado, Ciudad Universitaria , Costa Rica.
Brown J.L., Twomey E., Amézquita A., De Souza M.B., Caldwell J.P., Lötters S., Von May R., Melo-Sampaio P.R., Mejía-Vargas D., Perez-Peña P., Pepper M., Poelman E.H., Sanchez-Rodriguez M., and Summers K. (2011). ''A taxonomic revision of the Neotropical poison frog genus Ranitomeya (Amphibia: Dendrobatidae).'' Zootaxa, 3083, 1-120.
Crump, M. (1972). ''Territoriality and mating behavior in Dendrobates granuliferus (Anura: Dendrobatidae).'' Herpetologica, 28, 195-198.
Daly, J. W., Brown, G. B., and Mensah-Dwumah, M. (1978). ''Classification of skin alkaloids from neotropical poison-dart frogs (Dendrobatidae).'' Toxicon, 16, 163-188.
Goodman, D. (1971). ''Territorial behavior in a neotropical frog, Dendrobates granuliferus.'' Copeia, 1971, 365-370.
Grant, T., Frost, D. R., Caldwell, J. P., Gagliardo, R., Haddad, C. F. B., Kok, P. J. R., Means, D. B., Noonan, B. P., Schargel, W. E., and Wheeler, W. C. (2006). ''Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae).'' Bulletin of the American Museum of Natural History, (299), 1-262.
Ibañez, R., Solís, F., Jaramillo, C. and Rand, S. (2000). ''An overview of the herpetology of Panama.'' Mesoamerican Herpetology: Systematics, Zoogeography and Conservation. Johnson, J. D., Webb, R. G. and Flores-Villela, O. A., eds., The University of Texas at El Paso, El Paso, Texas, 159-170.
Meyer, E. (1992). ''Erfolgreiche Nachzucht von Dendrobates granuliferus Taylor, 1958. Cría exitosa en cautividad de Dendrobates granuliferus Taylor, 1958.'' Herpetofauna, 14, 11-21.
Meyer, E. (1993). ''Fortpflanzung und Brutpflegeverhalten von Dendrobates granuliferus Taylor, 1958 aus Costa Rica (Amphibia: Dendrobatidae).'' Veröffentlichung - Naturhistorisches Museum Schleussingen Btholdsbrg, Schleusingen, 7/8, 113-142.
Meyer, E. (1996). ''Eine oliv-gelbe Variante von Dendrobates granuliferus aus dem zentral-pazifischen Tiefland Costa Ricas: erste Beobachtungen zur Fortpflanzungsbiologie. .'' Herpetofauna (Weinstadt), 18, 21-27.
Meyer, E. (1996). Ökologie und Biogeographie des zentralamerikanischen Pfeilgiftfrosches Dendrobates granuliferus TAYLOR. Dissertation, University of Ulm, Ulm, Germany.
Miller, J. R. B., and McFarlane, D. A. (2007). ''A preliminary investigation into Hayne estimates of poison dart frog (Anura: Dendrobatidae) densities in recovering tropical forest habitat in Costa Rica.'' Herpetological Conservation and Biology, 3(2), 289-294.
Myers, C. W., Daly, J.W., Garraffo, H.M., Wisnieski, A., and Cover, J.F., Jr. (1995). ''Discovery of the Costa Rican poison frog Dendrobates granuliferus in sympatry with Dendrobates pumilio, and comments on taxonomic use of skin alkaloids.'' , 14(3144), 1-21.
Rasotto, M. B., Cardellini, P., and Sala, M. (1987). ''Karyotypes of five species of Dendrobatidae (Anura: Amphibia).'' Herpetologica, 43(2), 177-182.
Santos, J. C., Coloma, L. A., Summers, K., Caldwell, J. P., Ree, R., and Cannatella, D. C. (2009). ''Amazonian amphibian diversity is primarily derived from late Miocene Andean lineages.'' PLoS Biology, 7(3), e1000056.
Savage, J. M. (2002). The Amphibians and Reptiles of Costa Rica. University of Chicago Press, Chicago and London.
Silverstone, P. A. (1975). ''A revision of the poison-arrow frogs of the genus Dendrobates Wagler.'' Natural History Museum of Los Angeles County, Scientific Bulletin, 21, 1-55.
Summers, K. (2000). ''Mating and aggressive behaviour in dendrobatid frogs from Corcovado National Park, Costa Rica: a comparative study.'' Behavior, 137, 7-24.
van Wijngaarden, R., and Bolaños, F. (1992). ''Parental care in Dendrobates granuliferus (Anura: Dendrobatidae), with a description of the tadpole.'' Journal of Herpetology, 26(1), 102-105.
van Wijngaarden, R., and van Gool, S. (1994). ''Site fidelity and territoriality in the dendrobatid frog Dendrobates granuliferus.'' Amphibia-Reptilia, 15, 171-181.
Written by Kellie Whittaker and Ketti Augusztiny (kwhittaker AT berkeley.edu), UC Berkeley
First submitted 2004-12-02
Edited by Kellie Whittaker, Brent Nguyen (2011-11-09)
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