AMPHIBIAWEB
Atelopus exiguus
family: Bufonidae

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Conservation Status (definitions)
IUCN (Red List) Status Critically Endangered (CR)
See IUCN account.
CITES No CITES Listing
Other International Status None
National Status None
Regional Status None

   

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Description

Diagnosis: This species is a relatively small member of the genus Atelopus, which can be distinguished by the following combination of characters: small adult body size (adult male SVL ranging from 21.1-27.1 mm and adult female SVL ranging from 28.7-35.4 mm); short limbs (tibial length/SVL = 0.305-0.347); a phalangeal formula for the hand of 2-2-3-3; a foot webbing formula of I0-(1/2-1)II(1/2-1)-(1-3)III(1/2-2)-(1-3)IV(1-3)-(1/2-2)V; an acuminate snout that projects beyond the lower jaw; lack of tympanic membrane, annulus, and stapes; relatively few warts on the dorsal surface; the presence of flat yellow spiculae (becoming cream in preservative) on dorsum, flanks, forelimbs, and dorsal surfaces of thighs; inconspicuousness of vertebral neural processes; bright yellowish-green to blackish-green dorsum and flanks; yellow to orange venter in life (cream-colored in preservative); white palmar and thenar tubercles; no spiculae or coni on the gular or pectoral regions (Coloma et al. 2000).

Description: Adult males measure 21.1-27.1 mm SVL and adult females measure from 28.7-35.4 SVL. The body is robust. The head is as broad as it is long, with a snout that is pointed (acuminate) when viewed from above and projecting beyond the lower jaw when viewed in profile. The dorsal surface of the snout is weakly depressed. Nares are lateral and visible from above. The canthus rostralis is distinct, running in a straight line from the naris to the tip of the snout but concave from eye to naris. The loreal region is concave. Tympanic membrane, annulus, and stapes are lacking. Choanae are small and rounded and are widely separated. The tongue is free for half its length posteriorly, and is 2x as long as wide. Ostia pharyngea lacking. The forearm is relatively short. Fingers lack lateral fringes and have relative lengths of III>IV>II>I. The phalangeal formula for the hand is 2-2-3-3. The palm is smooth with only a few weakly developed tubercles. The outer metacarpal tubercle is distinct, while the inner metacarpal tubercle is weak. Hindlimbs (tibia) are relatively short, with tibial length/SVL = 0.305-0.347. Toes lack lateral fringes and the plantar surfaces of the foot are relatively smooth with only a few weakly developed tubercles. Subarticular tubercles are found only on the proximal joints of toes. Both inner and outer metatarsal tubercles are well developed, with the outer metatarsal tubercle being round and more prominent. Relative length of toes is IV>V>III>II>I. Foot webbing formula is I0-(1/2-1)II(1/2-1)-(1-3)III(1/2-2)-(1-3)IV(1-3)-(1/2-2)V. The dorsum bears spiculae, concentrated mostly laterally and ventrolaterally with few on the proximal part of the head and mid-dorsum, and found also on the temporal region, forelimbs, and hindlimbs. Otherwise the remaining portions of the extremities and the distal snout are relatively smooth. The belly is smooth. Adult males have keratinized nuptial pads on the dorsal and inner surfaces of the thumb and proximal phalange of Finger II, short robust forearms (vs. long slender forearms in females), considerably fewer spiculae than adult females (though subadult females also have fewer spiculae), and vocal slits. Toe I is lacking in several specimens: one juvenile and three adult males (Coloma et al. 2000).

Coloration in life: Dark to bright green dorsum (also described as olive green in Moore 2007) and flanks, all having yellow spiculae (pustular warts), and a yellow venter (Coloma 2002) or yellow anterior venter and pale orange posterior venter (Coloma et al. 2000). The posterior surfaces of the thighs are yellow-green and the groin is pale orange (Coloma et al. 2000). The palms are white and the soles are black (Coloma et al. 2000). Coloma and Ron (2001) provide a color photograph of a gravid female of Mazán, Azuay Province, Ecuador, and Moore (2007) provides a color photograph of an amplectant pair.

Similar species: Few other Atelopus species have a uniform green dorsum; those that do (A. angelito, A. bomolochos, A. eusebianus, A. muisca, A. peruensiss) all have larger adult body sizes. A. exiguus can be further distinguished from A. bomolochos by flank coloration (green in A. exiguus, never orange or yellow as in A. bomolochos) and iris coloration (almost entirely black in A. exiguus, never a green ring around the pupil as in A. bomolochos). A. exiguus can be further distinguished from A. angelito, A. eusebianus, and A. muisca by lack of black markings on the gular region, chest, belly, and undersides of thighs (vs. black ventral markings present in all three of the latter species). A. exiguus can be further distinguished from A. peruensis by flank coloration (dark to bright green in A. exiguus, generally black in A. peruensis but sometimes dull green), lack of yellow digit tips (vs. present in A. peruensis), having vocal slits (absent in A. peruensis), and absent or poorly-developed posterolateral processes on the hyoid (vs. well-developed in A. peruensis).

Larvae: Tadpoles are gastromyzophorous. The total length of a representative larval specimen at Stage 31 is 16.9 mm, with tail length being 60.5% of total length. The body is an elongated ovoid in shape, depressed dorsally, and widest at the posterior part. It is constricted slightly at the levels of the eyes and spiracle. The snout is bluntly rounded when viewed from above and sloping in lateral view. Eyes are dorsal and directed dorsolaterally. Nares are small. The spiracle is sinistral and elongated, originating at the midpoint of the body. The vent tube is short and medial. Tail musculature is robust at the anterior, narrowing abruptly at a point just posterior to the mid-length of the tail, and terminating anterior to the rounded tail tip. The dorsal fin does not extend onto the body and reaches its highest point posterior to the midlength of the tail. The mouth is ventral with a complete oral disc, slender serrated jaw sheaths, one row of marginal papillae at the anterior, two rows of papillae at the corners of the mouth, and no papillae at the posterior. LTRF is 2/3, with complete rows angulate at the anterior. The suctorial disc extends from the posterior labium for three-quarters of the body length, forming a complete disc with a raised edge. In life, the body is black with bluish-white marks on the rostrum , across the midbody, and on the distal part of the body. The tail musculature is black until midlength, with a white area following and then black pigmentation at the distal end. Fins are translucent but reticulated with black (Coloma et al. 2000).

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Ecuador

View distribution map using BerkeleyMapper.
Endemic to southern Ecuador. It is known from eight localities in the inter-Andean region in the Province of Azuay, in the Cordillera Occidental of the Andes, at elevations ranging from 3,150-3,850 m asl. The type locality is Laguna Llaviuco, Azuay Province, Ecuador. This species inhabits páramo and subpáramo, and has also been found in grassland adjacent to Lake Lluviaco. The annual mean precipitation in the zone where this species occurs is 1000-2000 mm, and annual mean temperature is 7-12° C (Coloma et al. 2000).

Life History, Abundance, Activity, and Special Behaviors
Individuals have been found walking on trails during the day (Read 1986, treating as A. ignescens, cited in Coloma et al. 2000), sheltering under stones (Read 1986, Moore 2007), actively moving about during the day in cushion vegetation in paramo habitat (Coloma et al. 2000), and in pasture area during the day after a rain (Coloma et al. 2000).

Despite the lack of tympana, tympanic annuli, and stapes, this species calls, and a recording exists in the National Sound Archive (Coloma et al. 2000). The call is pulsed and consists of 19-21 notes, lasting 0.48-0.52 sec, with an interval of 11.6 sec, at a dominant frequency of 2150-2700 Hz that increases gradually during the call (Coloma et al. 2000). The call is quiet at first and rises in intensity , peaking near the end of the call, then decreases, with note rate remaining constant (Coloma et al. 2000).

Calling occurs primarily in the morning, especially on warm days following heavy rains. Males call from crevices or holes besides small seepages and streams. Amplectant pairs were encountered frequently from July-September of 1986; five amplectant pairs were brought into captivity in mid-September and remained amplexed one month later in captivity. Clutches are attached to the bottom of stones in slowly flowing tributaries. Tadpoles have been found in small streams descending from paramo as well as in Río Mazán, at about 3400 m, and have been collected from Río Quinuas at 3150 m and 3540 m asl. New metamorphs and juveniles were found in piles of loose stones and under vegetation near Río Mazán, in September 1986 (Read 1986, quoted in Coloma et al. 2000).

Trends and Threats
This species was very common in the Río Mazán Valley when surveyed in 1986 (Read 1986, cited in Coloma et al. 2000). Now it is rarely seen and is considered Critically Endangered due to significant population decline (Stuart et al. 2008). It is one of only two high-elevation paramo/puna-dwelling Atelopus species not to have gone completely extinct (the other being A. mucubajiensis, in Venezuela) (La Marca et al. 2005).

The genus Atelopus has been the hardest hit by the fungal pathogen Batrachochytrium dendrobatidis, or Bd, which causes the disease chytridiomycosis; many species of Atelopus appear to have suffered major population declines or gone extinct, particularly high-elevation stream-breeding species (La Marca et al. 2005). Like other Atelopus species, A. exiguus is likely to have been affected by chytridiomycosis (Ron and Merino-Viteri 2000; La Marca et al. 2005). Other threats to this species include habitat degradation and loss (La Marca et al. 2005 estimate that 45% of the habitat has been converted to agriculture and pasture), due to the introduction of predatory non-native fish (trout) as well as non-native vegetation (pine trees), the construction of dams, increasing agriculture, and livestock grazing (Stuart et al. 2008). Its range overlaps with two protected areas, Parque Nacional Cajas and Bosque Protector Mazán (Coloma et al. 2000). Toral and Frenkel (2006) reported a count of 29 individuals (1 female, 18 males, 10 juveniles) found in Mazán, Azuay Province (cited in Coloma et al. 2007). Captive breeding is being attempted at the Pontificia Universidad Católica of Ecuador (Moore 2007).

Possible reasons for amphibian decline

General habitat alteration and loss
Intensified agriculture or grazing
Dams changing river flow and/or covering habitat
Disease
Climate change, increased UVB or increased sensitivity to it, etc.

Comments
This species was first described by Boettger (1892). It has sometimes been treated as a subspecies or synonym of A. ignescens, and was defined as a species complex with A. bomolochos by Gray (1983), but was redescribed as a separate species by Coloma et al. (2000). Guayasamin et al. (2010) examined phylogenetic relationships and confirmed that A. exiguus has affinity with the A. bomolochos clade rather than the A. ignescens clade.

Some specimens (4 of 23) showed digital reduction, with complete loss of Toe I, the first published report of intraspecific variation in digital reduction (Coloma et al. 2000).

The specific epithet exiguus means "small" in Latin (Coloma et al. 2000).

References
 

Boettger, O. (1892): Katalog der Batrachier-Sammlung im Museum der Senckenbergischen Naturforschenden Gesellschaft in Frankfurt am Main.  

Coloma, L. A., Lotters, S. A., and Salas, A. W. (2000). ''Taxonomy of the Atelopus ignescens complex (Anura: Bufonidae): Designation of a neotype of Atelopus ignescens and recognition of Atelopus exiguus.'' Herpetologica, 56(3), 303-324.  

Coloma, L. A., Lötters, S., Duellman, W.E., and Miranda-Leiva, A. (2007). ''A taxonomic revision of Atelopus pachydermus, and description of two new (extinct?) species of Atelopus from Ecuador (Anura: Bufonidae).'' Zootaxa, 1557, 1-32.  

Coloma, L. A., and Ron, S. R. (2001). Ecuador Megadiverso: Anfibios, Reptiles, Aves, Mamiferos / Megadiverse Ecuador: Amphibians, Reptiles, Birds, And Mammals. Serie de divulgación del Centro de Biodiversidad y Ambiente. Quito, Ecuador.  

Gray, P. (1983). Morphometrics of the Atelopus ignescens Complex (Anura: Bufonidae). M. S. Thesis. University of Kansas, Lawrence, Kansas.  

Guayasamin, J. M., Bonaccorso, E., Duellman, W. E., and Coloma, L. A. (2010). ''Genetic differentiation in the nearly extinct harlequin frogs (Bufonidae: Atelopus), with emphasis on the Andean Atelopus ignescens and A. bomolochos species complexes.'' Zootaxa , 2574, 55-68.  

La Marca, E., Lötters, S., Puschendorf, R., Ibáñez, R., Rueda-Almonacid, J. V., Schulte, R., Marty, C., Castro, F., Manzanilla-Puppo, J., García-Pérez, J. E., Bolaños, F., Chaves, G., Pounds, J. A., Toral, E., and Young, B. E. (2005). ''Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus).'' Biotropica, 37(2), 190-201.  

Moore, R. (2007). ''In search of Atelopus exiguus.'' Froglog, 83, 1-2.  

Read, M. (1986). ''Reptiles and amphibians.'' Río Mazán Project, 1986 Report. F. Robinson, eds., Department of Plant Sciences, Oxford University, Oxford, U. K..  

Ron, S.R., and Merino-Viteri, A. (2000). ''Amphibian declines in Ecuador: overview and first report of chytridiomycosis from South America.'' Froglog, 42, 2-3.  

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.  

Toral, E., and and Frenkel, C. (2006). ''Population state of Atelopus exiguus in the South Ecuadorian Andes (Abstracts).'' Joint Meeting of Ichthyologists & Herpetologists, 2006. M. A. Donnelly and K. E. Cooper, eds., New Orleans, LA, 111-112.



Written by Kellie Whittaker (kwhittaker AT berkeley.edu), UC Berkeley
First submitted 2008-12-08
Edited by Kellie Whittaker (2012-01-09)



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Citation: AmphibiaWeb: Information on amphibian biology and conservation. [web application]. 2014. Berkeley, California: AmphibiaWeb. Available: http://amphibiaweb.org/. (Accessed: Oct 24, 2014).

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