Diagnosis: Bufo holdridgei can be diagnosed by the following combination of characters: It is a moderate-sized toad, black to light brown in color with reddish parotoids and some reddish warts on the dorsal and lateral surfaces. The head bears low cranial crests except for a prominent supratympanic crest, This species completely lacks all elements of the outer and middle ear apparatus (tympanum, pseudocolumella, Eustachian tubes, ostia pharyngea). Hands and feet are fleshy and pad-like. Upper surfaces of the back and limbs have smooth beadlike warts (Savage 2002).
Description: Adult males are usually 32 to 46 mm in SVL but can reach up to 51.7 mm, while adult females range from 38 to 53 mm SVL (Savage 2002). Dorsal surfaces have bead-like warts, both large and small in size. A distinct lateral series of smooth conical warts is present. The venter is pustulate. Head is broader than it is long. Snout is subovoid in dorsal view. Skin on upper surface of the head is co-ossified to the skull. Canthal, supraorbital, postorbital, and parietal crests are low; in contrast, the supratympanic crest is thickened. Parotoid gland is smooth and globular and is less than two-thirds the area of the upper eyelid. Exostosis is present (a well-developed narrow temporal plate with ornamentation, continuous with the supratympanic crest posterior to the orbit). No vocal slits or sac observed in males. Limbs are short. Fleshy hands and feet are pad-like and lack subarticular, accessory, palmar, and plantar tubercles. Forelimbs are hypertrophied in adult males. Fingers I and II are equal in length. Fingers are webbed but not fringed. Legs are short and do not have large pointed warts. Toes are moderately webbed and the webbing is fleshy. Inner metatarsal tubercle is obsolescent and round, and smaller than the outer metatarsal tubercle. No tarsal fold is present. Males have a light-colored nuptial pad on the thumb (Savage 2002). Males also have unusually hypertrophied testes (Blair 1972).
The dorsum is black or brown (may be dark or light brown). There are some reddish warts on the body and limbs. The supratympanic crests are also black or brown. The venter is whitish and some dark mottling is present on the chest. The iris is black. (Savage 2002).
Similar species: B. holdridgei can be distinguished from the similar Costa Rican species B. fastidiosus by its relatively unremarkable cranial crests (vs. massive light-colored cranial crests in B. fastidiosus) and lacking large pointed warts on the upper tibial surface (vs. large pointed warts present on the upper tibial surface in B. fastidiosus). B. holdridgei can be distinguished from the closely related B. peripetates of western Panama by having a smaller adult size (32-52 mm in B. holdridgei, vs. 54-96 mm SVL in B. peripetates), less developed cranial crests (vs. massive and elevated cranial crests in B. peripetates), and an ornamented, exostosed temporal plate (vs. no temporal plate in evidence). B. holdridgei can also be distinguished from the similar species Crepidophryne epiotica by moderately webbed toes (vs. extensively webbed toes in C. epiotica) (Savage 2002).
Tadpoles are small, with a stage 36 tadpole measuring 23 mm in total length. The body is ovoid-shaped, with the tail having a caudal fin that is rounded at the tip. The spiracle is sinistral and lateral, while the vent tube is medial. Nares and eyes are dorsal. The mouth is anteroventral and directed ventrally. The oral disc is small and entire, with beaks and 2/3 rows of denticles, and bordered laterally by a single row of large papillae. The A2 row of denticles shows a median gap above the mouth (Savage 2002; Novak and Robinson 1975).
The tadpole body is heavily pigmented with dark brown, as are the upper tail musculature and dorsal fin. The venter is lighter in color (Savage 2002; Novak and Robinson 1975).
Distribution and Habitat
Country distribution from AmphibiaWeb's database: Costa Rica
Bufo holdridgei was originally found on the Volcán Barva, Cordillera Central, Costa Rica from 200-2,200 m asl, in lower montane rain forest. This species was considered to be extinct (Stuart 2008), but has been recently rediscovered (Abarca et al. 2010). The current known population was found in Alto del Roble, in the Cordillera Central, in secondary forest dominated by oak trees (Abarca et al. 2010).
Life History, Abundance, Activity, and Special Behaviors
This species is seasonally fossorial (Stuart et al. 2008), and is active during the daytime when it is above ground (Savage 2002). During periods of heavy rain (March to November), Bufo holdridgei is found under forest floor debris (Savage 2002). During dry periods, it inhabits mossy stream banks (Stuart et al. 2008).
B. holdridgei lacks tympana and vocal slits and thus does not have a breeding call (Novak and Robinson 1975). Sexual maturity is attained at about 3 years of age (Savage 2002). This species is an explosive breeder, laying small clutches of large eggs in forest floor pools as well as in drainage ditches made by humans (Novak and Robinson 1975; Savage 2002). Males arrive following heavy rains in early to mid-April, before females, and some males remain at the breeding pools after the breeding season ended in about late May (Savage 2002). Males may also leave the pond and then return (Savage 2002). Females generally remained at the breeding pool for less than an hour (Savage 2002). Multiple males (2-8) attempt amplexus simultaneously, forming mating balls (Savage 2002). Amplexus is inguinal (Novak and Robinson 1975), and males were found to frequently amplex with other species (Atelopus senex and Rana vibicaria), often drowning the other species since several males amplexed simultaneously (Savage 2002).
Blair (1972) noted that this toad is unusual in having hypertrophied testes (similar to Bufo haematiticus), and also noted that all interspecies crosses failed (using males of these two bufonids with females of other species).
Clutches vary in size from 45-137 eggs, with eggs 2.5-3.5 mm in diameter and eggs plus envelopes measuring 7 mm in diameter. Eggs have two outer gelatinous layers; although the inner layer is crenate, no partitions were observed within the jelly layers. Hatching takes place in about 12 days. Larvae are thought to be facultatively non-feeding. Metamorphosis occurs about 27 days post-hatching (Novak and Robinson 1975; Savage 2002).
Diet includes a wide variety of arthropod invertebrates, including spiders, larval stages of lepidopterans, flies, and beetles, and adult beetles, Dermoptera, ants, and mites (Savage 2002).
Trends and Threats
This species was long thought to be extinct, as it was not seen for over 25 years. Although it was once common (Nowak and Robinson 1975), especially during the breeding season, it was not recorded between 1986 and 2010 despite extensive searches. Because it vanished from apparently undisturbed habitat (near where the golden toad, Bufo periglenes, also vanished), chytridiomycosis was thought to be the major cause of population decline for Bufo holdridgei, perhaps in synergy with the effects of climate change. It was rediscovered in 2010 in a secondary oak forest of Alto El Roble, in the Cordillera Volcánica Central, an area where the chytrid fungal pathogen Bd is now enzootic (Abarca et al. 2010). Juveniles were found, indicating relatively recent reproductive activity, but no large aggregations were seen; this species should be considered Critically Endangered (Abarca et al. 2010).
The entire known range of Bufo holdridgei falls within a protected area: Parque Nacional Braulio Carrillo (Stuart et al. 2008). However, breeding ponds in Alto El Roble are near the main road and may be under threat from increasing tourism (Abarca et al. 2010).
Possible reasons for amphibian decline
Habitat modification from deforestation, or logging related activities
Climate change, increased UVB or increased sensitivity to it, etc.
Species authority: Taylor (1952).
Savage (2002) noted that a high proportion of B. holdridgei samples lacked part or all of a limb, but did not speculate as to whether this might be due to predation or congenital deformity.
The karyotype is 2N=22, with all chromosomes being metacentrics or submetacentrics. Six pairs of chromosomes are larger than the remaining five, and a secondary constriction is present on chromosome 1. NF=44 (Bogart 1972).
A Spanish-language species account can be found at the website of Instituto Nacional de Biodiversidad (INBio).
Abarca, J., Chaves, G., Garcia-Rodriguez, A., and Vargas, R. (2010). ''Reconsidering extinction: Rediscovery of Incilius holdridgei (Anura: Bufonidae) in Costa Rica after 25 years.'' Herpetological Review, 41, 15-152.
Blair, W. F. (1972). ''Bufo of North and Central America.'' Evolution in the Genus Bufo. University of Texas Press, Austin.
Bogart, J. P. (1972). ''Karyotypes.'' Evolution in the Genus Bufo. W. F. Blair, eds., University of Texas Press, Austin.
Novak, R. M. and Robinson, D. C. (1975). ''Observations on the reproduction and ecology of the tropical montane toad, Bufo holdrigei Taylor in Costa Rica.'' Revista de Biología Tropical, 23, 213-237.
Savage, J. M. (2002). The Amphibians and Reptiles of Costa Rica. University of Chicago Press, Chicago and London.
Stuart, S., Hoffmann, M., Chanson, J., Cox, N., Berridge, R., Ramani, P., and Young, B. (eds) (2008). Threatened Amphibians of the World. Lynx Edicions, IUCN, and Conservation International, Barcelona, Spain; Gland, Switzerland; and Arlington, Virginia, USA.
Taylor, E.H. (1952). "A review of the frogs and toads of Costa Rica." University of Kansas Science Bulletin, 35, 577-942.
Written by Kellie Whittaker and Aisha Butt (abutt AT berkeley.edu), University of California, Berkeley
First submitted 2009-11-02
Edited by Kellie Whittaker (2011-10-04)
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