Description
The snout-vent length for females of this frog species ranges from 39.5–49.9 mm, while males are smaller at 28.2–34.6 mm. It is relatively slender. Males have a broader, longer head, and thicker forearms. The snout is flat, subtriangular, extends beyond the lower jaw, and is obtusely pointed in dorsal view. The canthus is straight and angular. The interorbital space is flat. Eye diameter is equal to the distance between the eye and the nostril. The pupil is a mix between slit-shaped and round. No tympanic membrane, tympanic ring, or ostia pharyngea are present. The thumb is half the length of the hand and has two phalanges. Finger III is long. The tips of fingers II, III, and IV are broadened. There is basal webbing between fingers II and III, but the webbing is either absent or extremely minimal between fingers III and IV. This species has long hind limbs and feet. Toes have swollen tips and are 50-75% webbed. There are outer and inner metacarpal and metatarsal tubercles. The palm may have a few faint, round, supernumerary tubercles, and there are distinct subarticular tubercles at most phalangeal joints of all toes, and fingers II, III, and IV. In males, finger I has a nuptial excrescence. There are small, rounded, glandular warts on the dorsolateral and lateral head surfaces behind the eye. The warts continue in a row down the dorsal surface to the groin and onto the dorsal surfaces of the arms and legs, and partly onto the hand and tarsus (Lötters et al. 2004). This species was redescribed after it was noted that the original type material actually represented a related species from Central America, Atelopus varius (Lötters et al. 2004).

The dorsal surface is yellowish-green to olive green. The ventral surface fades into yellowish-cream on the belly and throat. There is a dark brown or black lateral stripe that passes all the way from the snout to the groin. Black stippling and marbling is present on all dorsal surfaces. Also present is a more or less defined cross-pattern behind the head (sometimes described as an "X" at the nape of the neck) and sometimes a chevron mark in the sacral region. The ventral surfaces of the limbs and flanks are widely marked with dark brown or black (Lötters et al. 2004).

Tadpoles of the genus Atelopus have large abdominal suckers that enables them to cling to rocks in rushing stream waters (Lötters 2007). Atelopus cruciger tadpoles have longer tails (61% of the body length) than other Atelopus species (Mebs 1980).

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Venezuela

	View distribution map in BerkeleyMapper.
	View Bd and Bsal data (57 records).

This species is restricted to several localities in the northern and southern versants of the Cordillera de la Costa of Venezuela (Estadoes Aragua, Carabobo, Miranda, Vargas, Yaracuy and the Distrito Federal). It has also been found in the Cerro Azul, Estado Cojedes (Rivas Fuenmayor 1998) which suggests that the species might be present throughout the entire mountainous area of the central coastal range (Lötters et al. 2004; Stuart et al. 2008). It occurs at elevations of 30 to 2,200 m, in montane and lowland humid forest (La Marca et al. 2005). It breeds along swift-flowing streams. One tiny population was found by a cascading mountain stream in cloud forest at 600m asl, within the Parque Nacional Henri Pittier (Manzanilla and La Marca 2004). Two other small populations were found in 2004-2005 at lower elevations (220m and 322m asl) on the northern slopes of the Parque Nacional Henri Pittier, along with another reported observation from Río El Duro, Edo, Aragua in 2006 (Rodríguez-Contreras et al. 2008).

Life History, Abundance, Activity, and Special Behaviors
Atelopus cruciger is diurnal. During breeding season (the dry season), this species lives near freshwater streams, typically found on rocks within the stream, or streamside vegetation climbing up to 1.5 m above the ground (Stuart et al. 2008). Adults feed on ants and other insects (Lötters 2006).

Although Atelopus cruciger lacks a tympanum and middle ear structures, this species exhibits three types of distinct calls: pulsed ("buzzes"), pure-toned ("whistles"), rising in frequency, and short ("chirps" or "twitters"), descending in frequency. A short, quiet, partially pulsed call, descending in frequency, is the characteristic vocalization for male frogs in the vicinity of other "non-interacting" individuals, males placed in a collecting bag with other males, and males in amplexus. An amplexing male will increase his call rate when another male approaches or touches him. In addition to the three distinct call types, one male was observed to give a series of variable calls before a series of pulsed calls (Cocroft et al. 1990).

Breeding occurs at fast-moving, cascading streams, but during the dry season (around April) so the eggs and tadpoles do not wash away (Lötters 1996). Males tend to spend much more time alongside cascading streams whereas females usually only reside next to the streams during breeding periods. Females spend more time in the hillsides and in the forests (McDiarmid 1973). Crump (1986) theorized that there are resident and transient individuals in the A. cruciger communities on the basis of her work in A. varius and a study done by Sexton (1958).

In these stream breeding areas, the males prefer damp, rocky surfaces, as opposed to the water which the breeding couples occupy (Sexton 1958). Often, males find females away from the streams and amplexus begins there, so by the time a female nears the stream, she is likely to be carrying a male (Sexton 1958). Other males wait at the stream for females, but the vast majority of females already have partners by the time they encounter these waiting males (Sexton 1958). Amplexus may last up to 19 days (Sexton 1958). The female lays around 150-270 eggs on a substrate in a cascading, fairly fast-moving stream, in several clutches. The eggs are tan in color. and each egg has a diameter of about 1 mm. Eggs can be seen through the venters of gravid females (Lynch 1986). Embryos hatch into free-living tadpoles. Tadpoles have large abdominal suckers, enabling them to cling to underwater rocks in rapidly-moving streams (Lötters 2007).

Atelopus cruciger secretes toxins via its skin that dissuade predators, as do other atelopids (see account for Atelopus zeteki, the most toxic member of the genus. The toxins of Atelopus cruciger are 3-17 fold less potent than those of A. zeteki, though they cause the same sequence of symptoms when injected into mice: Fuhrman et al. 1969). These compounds were originally named atelopidtoxins (now called zetekitoxins) and affect the heart (Fuhrman et al. 1969). Although tetrodotoxin, a potent neurotoxin, has been found in the skin of the closely related species Atelopus varius from Costa Rica (Kim et al. 1975), skin extracts made from Atelopus cruciger museum specimens did not contain tetrodotoxin (Mebs et al. 1995). It has apparently not been established whether the Atelopus cruciger toxin is in fact the steroidal alkaloid zetekitoxin. This possibility was raised by Daly et al. (1993), and atelopidtoxin has been renamed to zetekitoxin (Kim et al. 1975; Brown et al. 1977), but zetekitoxin itself is thought to be unique to A. zeteki (Yotsu-Yamashita et al. 2004 and references therein). Zetekitoxin blocks voltage-dependent sodium-channels, with zetekitoxin C being a less potent form and zetekitoxin AB being a more potent form (Brown et al. 1977; Yotsu-Yamashita et al. 2004).

This species is now exceedingly rare, following significant decline in its population. One small population was reported from 600 m asl (Manzanilla and La Marca 2004) and two other small populations were discovered during survey work in 2004-2005 at 220 m and 322 m asl, all on the northern slopes of the Parque Nacional Henri Pittier (Rodríguez-Contreras et al. 2008). Mostly males were found, but a few juveniles were also encountered at one location, indicating that at least one of the populations was breeding. Another population was found in Río El Duro, Edo, Aragua, in February 2006 (Valera and Frontado unpublished, cited in Rodríguez-Contreras et al. 2008).

Trends and Threats
Atelopus cruciger has undergone a rapid decline, with most of the population having disappeared, despite many of the known localities falling within national parks (Parque Nacional Henri Pittier, Parque Nacional Rancho Grande and Parque Nacional San Esteban; Stuart et al. 2008). Museum records indicate that A. cruciger was formerly abundant, with 627 records from 33 localities, widely distributed over most of the Cordillera de La Costa (Rodríguez-Contreras et al. 2008). This species was thought to be extinct after only two specimens were collected in 1986 and no individuals were discovered in the years immediately post-1986. For nearly 20 years, no sightings were reported. However, after 8 years of intensive surveys, a small population was found in 2004 near a cascading mountain stream in the Parque Nacional Henri Pittier cloud forest, south of Cata at an elevation of 600m asl (Manzanilla and La Marca 2004), and a small number of others have since been reported (Rodríguez-Contreras et al. 2008). Atelopus cruciger is listed as Critically Endangered (Stuart et al. 2008).

Of the last two specimens collected in 1986, one of the two was retrospectively examined by histology and reported to have been infected with chytrid fungus (Bd) (Bonaccorso et al. 2003). Chytridiomycosis, with an epidemic possibly triggered by a severe drought in 1988, is also thought to be the primary factor in the rapid decline of several other Venezuelan Andean members of this genus (A. carbonerensis, A. mucubajiensis, and A. sorianoi; Lampo et al. 2006). The existing Atelopus cruciger populations in the Parque Nacional Henri Pittier are infected with Bd, and one adult male was found morbid and heavily infected (Rodríguez-Contreras et al. 2008).

Another possible threat is industrial pollution, particularly in the Valencia-Maracay area where many industries are emitting gases (Stuart et al. 2008).

Relation to Humans
Before its disappearance, A. cruciger was occasionally collected for the pet trade (Stuart et al. 2008).

Possible reasons for amphibian decline

Prolonged drought
Floods
Intentional mortality (over-harvesting, pet trade or collecting)
Climate change, increased UVB or increased sensitivity to it, etc.

Comments

This species was first described by Lichtenstein and von Martens (1865).

The genus Atelopus, with 113 described and putative species, appears to be the most threatened clade of amphibians (La Marca et al. 2005). At least 30 species appear to be extinct, having been missing from all known localities for at least 8 years (La Marca et al. 2005). Only 52 of the surviving species have sufficient data with which to evaluate population trends; of these, 81% (42 of 52) have population sizes that have been reduced by at least half (La Marca et al. 2005). Only 10 of the 52 species appear to have stable populations (La Marca et al. 2005). Higher-elevation species (those living at least 1000 m asl) have been hit the worst, with 75% (21 of 28) having disappeared entirely (La Marca et al. 2005). In Venezuela there are ten endemic Atelopus species (La Marca and Reinthaler 1991); nine are classified as Critically Endangered and one is thought extinct (Rodríguez and Rojas-Suárez 1995; Rodríguez-Contreras et al. 2008; Stuart et al. 2008). Chytridiomycosis is thought to be a primary factor in the decline and disappearance of species in this genus (La Marca et al. 2005). Most Atelopus species are restricted to very limited areas (no more than two localities) and occur along mid- to high-elevation streams (1500-3000 m asl, though the maximum vertical range is from sea level to permanent snow; Lötters 2007), a habitat preference frequently associated with the co-occurrence of chytridiomycosis (La Marca et al. 2005). Habitat loss has occurred within the ranges of many Atelopus species, but does not appear to be a major factor in the decline of most Atelopus species; 22 species declined despite occurring in protected areas (La Marca et al. 2005). Many Atelopus species are local endemics, putting them at particular risk of extinction, with at least 26 species known only from a single population inhabiting a narrow altitudinal range (La Marca et al. 2005). Due to their restricted ranges, they are thought to have limited ability to adapt to warming climatic conditions (Lötters 2007).

Defenders of Wildlife and SSN recommended in 2009 to the United States that Atelopus cruciger should be included in Appendix II in CITES (Convention on International Trade in Endangered Species), during COP15 (the UN Climate Change Conference 2009). Since a small population of this species is only found in Northern and Southern versants of the Corillera de la Costa of Venezuela, submitting this species into Appendix II would enact recommendations for controlling commercial trade. However, the Dept. of U. S. Fish and Wildlife noted that unless Venezuela requested assistance or "significant additional information is received" pertaining to the species trade or population status, Atelopus cruciger would not be submitted into Appendix II.

References

Brown, G. B., Kim, Y. H., Küntzel, H., Mosher, H. S., Fuhrman, G. J. and Fuhrman, F. A. (1977). ''Chemistry and pharmacology of skin toxins from the frog Atelopus zeteki (atelopidtoxin: zetekitoxin).'' Toxicon, 15, 115-128.

Bonaccorso, E., Guayasamin J. M., Méndez, D., and Speare, R. (2003). ''Chytridiomycosis in a Venezuelan amphibian (Bufonidae: Atelopus cruciger). .'' Herpetological Review, 34, 331-334.

Cocroft, R. B., McDiarmid, R. W., Jaslow, A. P., and Ruiz-Carranza, P. M. (1990). ''Vocalization of eight species of Atelopus (Anura: Bufonidae) with comments on the communication in the genus.'' Copeia, 1990, 631-643.

Crump, M. L. (1986). ''Homing and site fidelity in a neotropical frog, Atelopus varius (Bufonidae).'' Copeia, 1986, 438-444.

Daly, J. W. (2004). ''Marine toxins and nonmarine toxins: convergence or symbiotic organisms?'' Journal of Natural Products, 67, 1211-1215.

Daly, J. W., Garraffo, H. M., and Spande, T. F. (1993). ''Amphibian Alkaloids.'' The Alkaloids: Chemistry and Pharmacology. Volume 43. G. A. Cordell, eds., Academic Press.

Fuhrman, F. A., Fuhrman, G. J., and Mosher, H. S. (1969). ''Toxin from skin of frogs of the genus Atelopus: differentiation from dendrobatid toxins.'' Science, 165(3900), 1376-1377.

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.

La Marca, E., and Reinthaler, H. P. (1991). ''Population changes in Atelopus species of the Cordillera de Merida, Venezuela.'' Herpetological Review, 22, 125-128.

Lampo, M., Rodríguez-Contreras, A., La Marca, E., and Daszak, P. (2006). ''A chytridiomycosis epidemic and a severe dry season precede the disappearance of Atelopus species from the Venezuelan Andes.'' Herpetological Journal, 16, 395-402.

Lichtenstein, M. H. C., and Von Martens, E. C. (1856). Nomenclator Reptilium et Amphibiorum Musei Zoologici Berolinensis. Königlich Akademie der Wissenschaften zu Berlin, Berlin.

Lynch, J. D. (1986). ''Notes on the reproductive biology of Atelopus subornatus.'' Journal of Herpetology, 20, 126-129.

Lötters, S. (2007). ''The fate of the Harlequin Toads — help through a synchronous multi-disciplinary approach and the IUCN ‘Amphibian Conservation Action Plan’.'' Zoosystematics and Evolution, 83( Supplement 1), 69-73.

Lötters, S., La Marca, E., and Vences, M. (2004). ''Redescriptions of two toad species of the genus Atelopus from coastal Venezuela.'' Copeia, 2004, 222-234.

Manzanilla, J., and La Marca, E. (2004). ''Population status of the Rancho Grande Harlequin Frog (Atelopus cruciger Lichtenstein and Martens 1856), a proposed critically endangered species from the Venezuelan Coastal Range.'' Memoria de la Fundacion La Salle de Ciencias Naturales, Caracas, 62, 5-29.

McDiarmid, R. W., and Altig, R. (1999). Tadpoles: the Biology of Anuran Larvae. The University of Chicago Press, Chicago and London.

Mebs, D. (1980). ''Zur Fortpflanzung von Atelopus cruciger (Amphibia: Salientia: Bufonidae).'' Salamandra, 16(2), 65-81.

Mebs, D., Yotsu-Yamashita, M., Yasumoto, T., Lötters, S., and Schluter, A. (1995). ''Tetrodotoxin in South American Atelopus species (Bufonidae).'' Toxicon, 33(3), 299.

Rivas Fuenmayor, G. (1998). ''Geographic distribution. Anura. Atelopus cruciger.'' Herpetological Review, 29, 172.

Rodríguez, J.P. and Rojas-Suárez, F. (1995). Libro Rojo De La Fauna Venezolana. PROVITA, Caracas.

Rodríguez-Contreras, A., Celsa Señaris, J., Lampo, M., and Rivero, R. (2008). ''Rediscovery of Atelopus cruciger (Anura: Bufonidae): current status in the Cordillera de La Costa, Venezuela.'' Oryx, 42, 301-304.

Sexton, O. (1958). ''Observations of the life history of a Venezuelan frog, Atelopus cruciger.'' Acta Biological Venezuelica, 2, 235-242.

Stuart, S., Hoffmann, M., Chanson, J., Cox, N., Berridge, R., Ramani, P., Young, B. (eds) (2008). Threatened Amphibians of the World. Lynx Edicions, IUCN, and Conservation International, Barcelona, Spain; Gland, Switzerland; and Arlington, Virginia, USA.

Yotsu-Yamashita, M., Kim, Y.H., Dudley, Jr., S.C., Choudhary, G., Pfahnl, A., Oshima, Y., and Daly, J.W. (2004). ''The structure of zetekitoxin AB, a saxitoxin analog from the Panamanian golden frog Atelopus zeteki: a potent sodium-channel blocker.'' Proceedings of the National Academy of Sciences of the United States of America, 101(13), 4346-4351.

Species Account Citation: AmphibiaWeb 2014 Atelopus cruciger: Rancho Grande Harlequin Frog <https://amphibiaweb.org/species/43> University of California, Berkeley, CA, USA. Accessed Nov 24, 2024.

Citation: AmphibiaWeb. 2024. <https://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 24 Nov 2024.

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