EcoHealth 5, 27–33, 2008

DOI: 10.1007/s10393-008-0159-z

2008 International Association for Ecology and Health

Original Contribution

Batrachochytriumdendrobatidis and Chytridiomycosis in

Anuran Amphibians of Colombia

Angélica Ruiz1 and José Vicente Rueda-Almonacid2

1
Universidad de los Andes, Carrera 78 p No. 35 19 sur, Bogotá, Colombia
2
Threatened Species Program, Conservación Internacional—Colombia, Bogotá, Colombia

Abstract: In order to investigate the possible presence of the chytrid fungus Batrachochytrium dendrobatidis
(Chytridiomycota: Chytridiales) in frogs (Amphibia: Anura) of Colombia, we made a retrospective examination
of formalin-fixed specimens preserved in natural history collections. Using the staining technique of hema-
toxylin and eosin to identify B. dendrobatidis in histological slices, we found evidence of the fungus in 3 of the 53
frog species examined from a total of 672 specimens collected in 17 departments within Colombia between 1968
and 2006. The infected specimens were found dead or dying in recent years in high elevation sites, suggesting
that chytridiomycosis (the disease caused by the fungus) may represent a significant threat to Colombian
amphibians. We conclude that a more extensive search for B. dendrobatidis in museum specimens and wild-
caught frogs should be undertaken as soon as possible, using both histological and molecular genetic techniques,
in order to further characterize the geographic and taxonomic extent of infections of B. dendrobatidis.

Keywords: Batrachochytrium dendrobatidis, Colombia, amphibians, chytridiomycosis, population decline

INTRODUCTION crease of ultraviolet radiation, introduced species, envi-

The global decline of amphibians is an alarming phenom-
enon. An estimated 43.2% of the 5743 described species in
the world have experienced some reduction in population
size, while only an estimated 0.5% of species have increased
in number and 27.2% have remained stable (Stuart et al.,
2004). The conservation status of 29% of amphibian species
is unknown due to a lack of basic information (Stuart et al.,
2004). Among the many potential causes of amphibian
declines that may be acting alone or synergistically are
habitat destruction, over-exploitation, climate change, in-
Published online: February 17, 2008
Correspondence to: Angélica Ruiz, e-mail: angelica.ruiz@gmx.net
ronmental pollution, and infectious diseases (Berger et al.,
1998; Alford and Richards, 1999; Daszak et al., 1999; Young
et al., 2001; Hamer et al., 2004; La Marca et al., 2005).
Recent research has implicated a skin mycosis caused
by the chytrid fungus Batrachochytrium dendrobatidis as the
proximate cause of amphibian declines at high elevation
sites in temperate and tropical regions of Australia, New
Zealand, Europe, and America, including many sites that
lack any obvious signs of anthropogenic disturbance to the
environment (Berger et al., 1998; Bosch et al., 2001; Fellers
et al., 2001; Davidson et al., 2003; Bell et al., 2004; Lips
et al., 2004). B. dendrobatidis infects the keratinized cells of
the amphibian epidermis, causing hyperplasia and hyper-
keratosis of the stratum corneum and stratum granulosum
(Berger et al., 1998). Infection by B. dendrobatidis is fre-
28 Angélica Ruiz and José Vicente Rueda-Almonacid

quently but not always lethal to amphibians (Davidson

Table 1. Number of Individuals Studied by Year Collected
et al., 2003; Mazzoni et al., 2003; Hanselmann et al., 2004;
Weldon et al., 2004). The mechanism by which B. dend- Year of collection No. positive No. examined
robatidis causes death in amphibians is not clear, but it is 1968 12
believed that infection of the skin by B. dendrobatidis affects 1969 8
cutaneous respiration and osmoregulation, and that the 1970 48
fungus may produce and release a substance toxic to its 1971 1
host (Berger et al., 1998). 1972 7
As of 2002, B. dendrobatidis has been implicated in 1973 2
mortality events across 93 amphibian species belonging to 1974 4
14 families and two orders (Anura and Caudata), and has 1975 4
been found in various countries of Africa, America, Europe 1976 16
and Oceania (Speare and Berger, 2004). Not all species of 1977 1
1978 14
amphibians appear to be equally susceptible. Numerous
1979 2
mass mortality events have been recorded in wild and
1980 21
captive populations. In each event, the conspicuous chan-
1981 43
ges in the epidermis associated with the B. dendrobatidis- 1982 13
caused disease, chytridiomycosis, are observed (Berger et 1983 26
al., 1998; Nichols et al., 1998; Bosch et al., 2001; Lips et al., 1984 14
2003; Muths et al., 2003). Certain species, however, appear 1985 39
to be resistant to chytridiomycosis, even when infected with 1986 16
B. dendrobatidis. Examples of resistant species include two 1987 9
frogs that have been introduced by humans to different 1988 25
continents: the African three-clawed frog (Xenopus laevis) 1989 25
and the North American bullfrog (Rana catesbeiana), which 1990 24
could serve as potential vectors of fungal pathogens 1991 23
1992 38
(Davidson et al., 2003; Mazzoni et al., 2003; Daszak et al.,
1993 39
2004; Hanselmann et al., 2004; Weldon et al., 2004).
1994 84
Colombia has the second most diverse amphibian
1996 2
fauna in the world, containing around 785 described spe- 1997 1
cies (Stuart et al., 2006). In recent years, herpetologists and 1998 36
conservationists have confirmed the precipitous decline of 2001 10
more than 50 of these species, pointing out that amphibi- 2002 5
ans comprise that group of animals that is most vulnerable 2004 5 25
to extinction in Colombia (Rueda-Almonacid et al., 2004). 2005 2 2
For most of these 50 species, the causes of decline are not 2006 2
clear, leaving chytridiomycosis as a distinct possible cause Undated 31
in need of investigation. The present study seeks to explore Total 7 672
the presence and distribution of B. dendrobatidis in
Colombian amphibians through histological analyses of
each of the 672 specimens examined, we took a sample of
skin samples taken from museum specimens belonging to
skin tissue of approximately 5 mm2 from the ventral sur-
Colombia’s major natural history collections.
face near the inguinal region. Each skin sample was
embedded in paraffin, sliced in serial sections 6 lm in
MATERIALS AND METHODS width, and stained with hematoxylin and eosin following
the method described by Berger et al. (1999). For each skin
We undertook a retrospective study of amphibian speci- sample, 5–10 skin sections were observed using a com-
mens fixed in 10% formalin and stored in 70% ethanol. For pound light microscope with 40 · and 100 · objective
 Chytridiomycosis in Colombia 29

lenses. Slides containing histological slices will be deposited

Table 2. List of Species Examined for B. dendrobatidisa
at the museum from which each sample was taken.
Specimens were obtained from the collections of the Location Species No. of
Instituto de Ciencias Naturales, Universidad Nacional de (department) individuals
Colombia (ICN-MHN), the Museo de Historia Natural of examined
the Pontificia Universidad Javeriana (MUJ), and the Insti- Amazonas Edalorhina perezi 1
tuto Alexander von Humboldt (IAvH). The 672 specimens Rhinella margaritifera 3
examined for presence/absence of B. dendrobatidis were Eleutherodactylus sp. 1
collected between 1968 and 2006 (Table 1), and belong to Antioquia Atelopus carauta 1
the anuran genera Atelopus, Rhinella, Oophaga, Edalorhina, Atelopus nicefori 5
Eleutherodactylus, Gastrotheca, Dendrosophus, Hyloscirtus, Atelopus sanjosei 1
Leptodactylus, and Allobates. The collecting localities are Atelopus sernai 5
distributed across 17 departments within Colombia (Ta- Atelopus spp. 16
Boyacá Atelopus ebenoides 115
ble 2). The number of specimens examined per species was
marinkellei
subject to their availability in museum collections.
Atelopus sp. 1
The samples studied included most of the species of the
Caldas Atelopus sp. nov 46
genus Atelopus available in the four museums that gave Gastrotheca dendronastes 7
access to their facilities—species which were thought to Hyloscirtus group bogotensis 5
have, or for which there were serious indications of having, Cauca Atelopus ebenoides ebenoides 17
suffered severe or local decline. Also included in the sample Atelopus elegans 54
was a set of species derived from the National Natural Park Atelopus eusebianus 27
Selva de Florencia, which constitutes the area in Colombia Atelopus famelicus 20
with the richest amphibian biodiversity. Atelopus simulatus 1
Caecilia nigricans 1
Atelopus spp. 9
RESULTS Cesar Atelopus carrikeri 1
Chocó Atelopus flavescens 3
Atelopus glyphus 1
The prevalence of B. dendrobatidis in the genus Atelopus was
Atelopus spurrelli 3
1%. Five specimens were found to be positive for the chytrid
Oophaga histrionica 1
fungus among 588 specimens examined. Atelopus mitter-
Cundinamarca Atelopus lozanoi 39
meieri was the only specie of Atelopus found to be infected. Atelopus muisca 49
According to field notes accompanying these specimens, Atelopus pedimarmoratus 2
none were reported to show signs of chytridiomycosis. In- Atelopus subornatus 23
fected specimens of A. mittermeieri were collected in June of Eleutherodactylus elegans* 1
2004 at the headwaters of the Rı́o Cercado in the Santuario Eleutherodactylus grupo e 9
de Fauna y Flora Guanent á (610¢ N, 72 56¢ W, 2250–2750 legans
m), department of Santander, and are now housed at the Eleutherodactylus ingeri 3
herpetological collection of the Museo de Historia Natural, Hyloscirtus bogotensis* 1
Pontificia Universidad Javeriana (catalog numbers MUJ Atelopus spp. 2
Eleutherodactylus cf. bogotensis 6
3388, 3389, 3392, 4360, 4362). Histological analyses of 41 A.
Guajira Atelopus carrikeri 1
mittermeieri captured in 1981 and 1983 revealed no evi-
Magdalena Atelopus carrikeri 3
dence of Bd infection, which suggests that chytridiomycosis
Atelopus laetissimus 19
appeared in this region after this date. Atelopus nahumae 13
Two other species were found to be infected with B. Atelopus walkeri 13
dendrobatidis: Hyloscirtus bogotensis (a froglet) and Eleut- Eleutherodactylus santaemartae 1
herodactylus elegans (an adult) found in April and August Meta Atelopus minutulus 6
2005, respectively, during surveys sponsored by Conserva- Hyloscirtus group bogotensis 2
tion International—Colombia to determine the status of
30 Angélica Ruiz and José Vicente Rueda-Almonacid
Table 2. Continued
Location Species No. of
(department) individuals
examined
Nariño Atelopus aff. ignescens
Atelopus lynchi
Eleutherodactylus labiosus
Putumayo Allobates femoralis
Dendrosophus minutus
Juvenile eleutherodactyline
Eleutherodactylus spp.
Eleutherodactylus sulcatus
Not determinate
Leptodactylus lineatus
Rhinella margaritifera
Eleutherodactylus lanthanites
Eleutherodactylus conspicillatus
Eleutherodactylus ockendeni
Eleutherodactylus w-nigrum
Eleutherodactylus croceoinguinis
Eleutherodactylus dolops
Eleutherodactylus lacrimosus
Eleutherodactylus martiae
Quindio Atelopus quimbaya
Risaralda Atelopus grupo carauta
Atelopus spp.
Eleutherodactylus simoterus
Santander Atelopus eusebianus
Atelopus mittermeieri*
Dendrosophus subocularis
Eleutherodactylus bicolor
Tolima Atelopus simulatus
Atelopus spp.
Total 672
a
Asterisk indicates positive-infected species.
Colostethus edwardsi, Atelopus lozanoi, A. muisca, and A.
subornatus in Cundinamarca. The infected individual of H.
bogotensis was found nearly dead and sloughing skin from
the tail, venter, and part of the dorsum. It was collected at
La Cueva de los Moyas, municipio de la Calera (4 39¢ N,
74 01¢ W, 3127 m) (catalog number MUJ 4471). The in-
fected individual of E. elegans was found dead on mossy
vegetation without evident signs of chytridiomycosis, and
was collected in the Parque Ecológico de Matarredonda
located in Vereda Verjón Alto, 15 km along the road be-
tween Bogotá and Choachı́, department of Cundinamarca
(4 33¢ N, 74 0¢ W, 3260 m) (catalog number MUJ 5101).
16
9
2
1
1
2
4
1
1
1
10
1
5
1
1
2
2 Figure 1. Skin section of Atelopus mittermeieri (MUJ3389) showing
2 strong stratum corneum hyperkeratosis and B. dendrobatidis sporangia.
1
In the three infected species, we observed an excessive
9
inflammation or hyperkeratosis of the stratum corneum,
1
3
appearing to be four to six times thicker than that of a
1 healthy animal, reaching a thickness of up to 60 lm
1 (Fig. 1). Embedded within the keratinized tissues, we ob-
46 served roughly spherical zoosporangia with refractile walls,
1 either with or without clearly visible septa. These zoospo-
2 rangia have a diameter of 9–23 lm (N = 43, standard
5 deviation = 3.3 lm). These observations match well those
2 described by Berger et al. (1998) and Longcore et al. (1999)
for the zoosporangia of B. dendrobatidis.
DISCUSSION
To the best of our knowledge, the results of this study
constitute the first documented evidence of the presence of
B. dendrobatidis in Colombia. Twelve species of Atelopus
have now been found infected with the chytrid fungus (La
Marca et al., 2005). Of these, A. carbonerensis and A. so-
rianoi from Venezuela, A. chiriquiensis from Panamá and
Costa Rica, and an undescribed species from Ecuador are
now presumed to be extinct (La Marca et al., 2005). Pop-
ulations of A. bomolochos from Ecuador, A. cruciger and A.
mucubajiensis from Venezuela, A. pulcher from Perú, and A.
varius and A. zeteki from Panamá, are considered to have

been reduced by at least 50%, and the conservation status of
A. spumarius spumarius and two undescribed species re-
mains unknown (La Marca et al., 2005). Chytridiomycosis
is considered to be the most likely cause for the decline of
Atelopus, as many other potential factors have been ruled
out, such as habitat destruction and the introduction of
exotic species (Lötters et al., 2004). However, there is still no
conclusive evidence indicating that chytridiomycosis is the
principal cause of declines in many Atelopus species (La
Marca et al., 2005). Recent research strongly supports the
hypothesis that an increase in global temperatures has
contributed to the disappearance of many populations and
species of amphibians by promoting optimal growth of Bd
(Pounds et al., 2006). Atelopus mittermeieri was recently
rediscovered north of the locality where we detected B.
dendrobatidis, and the status of this population is currently
under study (Acosta-Galvis et al., 2006).
While our study demonstrates that Bd is present in
Colombia, results suggest that the fungus is currently at a
very low prevalence. Is this the case, or are we failing to
detect infection in some samples? While histology is an
inexpensive and low-cost method for detecting B. dendro-
batidis infection, one difficulty in using this method to
measure the prevalence of B. dendrobatidis infection within
frog populations is the possibility of false negatives, failing
to detect infection when it is, in fact, present in a given frog
(Annis et al., 2004; Boyle et al., 2004; Kriger et al., 2006;
Puschendorf et al., 2006;). The histological method used
here has been shown to be very efficient at detecting B.
dendrobatidis in frog skin when the extent of infection
within the individual is high (Boyle et al., 2004). However,
when a frog is found in a low or early phase of infection,
histological techniques are known to lack adequate sensi-
tivity in detecting the fungus (Boyle et al., 2004). This could
explain the low frequency of infection in our sample of
Atelopus (1%). This low frequency is similar to that ob-
served in the retrospective A. cruciger study made by Bon-
accorso et al. (2003), in which the infection frequency was
1.7% (1 positive from the 59 specimens examined), Lampo
et al. (2006) who found 7.4% in the three Atelopus species (7
positive from 95 specimens), and also to that reported in
Xenopus by Weldon et al. (2004), who found 2.7% infected
individuals (19 positives from 697 specimens).
Frog species that have been found to be infected and
whose populations have declined share many of the fol-
lowing characteristics: they are distributed on mountains,
are less fecund, reproduce in streams, and have narrow
geographic ranges (Williams and Hero, 1998; Lips et al.,
Chytridiomycosis in Colombia 31
2003). These characteristics also describe the majority of
Atelopus species: 61% of described Atelopus species are
found above 1500 meters, chiefly in the northern Andes of
South America, while 31% can be found in lowlands, and
only 7% are widely distributed (Lötters, 1996; La Marca
et al., 2005). Most species of Atelopus are found near
streams during at least part of the year, which is a factor
that increases their likelihood of acquiring chytridiomy-
cosis (Kriger and Hero, 2007).
The geographic distribution of the two other species
infected with B. dendrobatidis (Hyloscirtus bogotensis and
Eleutherodactylus elegans) is limited from moderate to high
elevation sites in the departments of Cundinamarca, Boy-
acá, and Santander in the Eastern Cordillera of the
Colombian Andes. Little information is available on the
current conservation status of either of these two anurans.
There are records of Hyloscirtus bogotensis and Eleut-
herodactylus elegans from the Cundiboyacense plateau
(Ruiz-Carranza et al., 1996). In Chingaza National Natural
Park, close to the area where the infected species were
found, drastic population declines of very abundant species
were observed, including Colostethus subpunctatus and
Bolitoglossa adspersa, and there have been no sightings of
two of the more common frogs of the Park, Atelopus muisca
and Atelopus lozanoi, for over a decade (Rueda-Almonacid
et al., 2004).
The results of our study suggest that chytridiomycosis
may be a primary factor in the disappearance of many of
Colombia’s amphibian population, and may represent a
significant threat to the future of Colombian amphibian
biodiversity.
ACKNOWLEDGMENTS
We thank the following curators for the loan of material
and their kind permission to take skin samples: John D.
Lynch of the Instituto de Ciencias Naturales de la
Universidad Nacional de Colombia; Andrés Acosta of the
Pontificia Universidad Javeriana; and Juan Manuel Renjifo,
formerly of the Instituto Alexander von Humboldt. We also
thank Rafael Rubio, Diana Galindo, Angélica Pérez, and
Andrés Diavanera for the loan of their Eleutherodactylus
elegans and Hyloscirtus bogotensis individuals. For their
patient advice and instructions examining the histological
material for the presence of B. dendrobatidis, we thank
Diana Méndez and Lee Berger of the School of Public
Health and Tropical Medicine at James Cook University,
32 Angélica Ruiz and José Vicente Rueda-Almonacid
Australia, and Andrés Merino of the Pontificia Universidad
Católica of Ecuador. Thanks to Andrew Crawford for the
translation and critical revision of this document, and
Ariadne Angulo and Álvaro Andrés Velásquez for the
careful revision of the final manuscript. Finally, thanks to
Enrique La Marca and an anonymous evaluator, who
enriched this document enormously with their commen-
taries. This work was financed by a grant from the
Programa de Especies Amenazadas de Conservación Inter-
nacional Colombia and funds provided by the Darwin
Initiative.
REFERENCES
Acosta-Galvis A, Rueda-Almonacid JV, Velásquez-Álvarez A,
Sánchez-Pacheco S, Peña-Prieto J (2006) Descubrimiento de
una nueva especie de Atelopus (Bufonidae) para Colombia: ¿una
luz de esperanza o el ocaso de los sapos arlequines?. Revista de la
Academia Colombiana de Ciencias Exactas, Fı́sicas y Naturales
30:279–190
Alford RA, Richards SJ (1999) Global amphibian declines: a
problem in applied ecology. Annual Review of Ecology and
Systematics 30:133–165
Annis SL, Dastoor FP, Ziel H, Daszak P, Longcore JE (2004) A
DNA-based assay identifies Batrachochytrium dendrobatidis in
amphibians. Journal of Wildlife Diseases 40:420–428
Bell B, Carver S, Mitchel N, Pledger S (2004) The recent decline of
a New Zealand endemic: how and why did populations of Ar-
chey’s frog Leiopelma archeyi crash over 1996–2001?. Biological
Conservation 120:189–199
Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin
CL, et al. (1998) Chytridiomycosis causes amphibian mortality
associated with population declines in the rain forest of Aus-
tralia and Central America. Proceedings of the National Academy
of Sciences of the United States of America 95:9031–9036
Berger L, Speare R, Kent A (1999) Diagnosis of chytridiomycosis
in amphibians by histologic examination. Available:
http://www.jcu.edu.au/school/phtm/PHTM/frogs/histo/
chhisto.htm [accessed May 15, 2006]
Bonaccorso E, Guayasamin JM, Méndez D, Speare R (2003)
Chytridiomycosis as a possible cause of population declines in
Atelopus cruciger (Anura: Bufonidae). Herpetological Review
34:331–334
Bosch J, Martı́nez-Solano I, Garcı́a-Parı́s M (2001) Evidence of a
chytrid fungus infection involved in the decline of the common
midwife toad (Alytes obstetricans) in protected areas of central
Spain. Biological Conservation 97:331–337
Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004)
Rapid quantitative detection of chytridiomycosis (Batracho-
chytrium dendrobatidis) in amphibian samples using real-time
Taqman PCR assay. Disease of Aquatic Organisms 60:141–148
Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE,
Speare R (1999) Emerging infectious diseases and amphibian
population declines. Emerging Infectious Diseases 5:735–748
Daszak P, Strieby A, Cunningham AA, Longcore JE, Brown CC,
Porter D (2004) Experimental evidence that the bullfrog (Rana
catesbeiana) is a potential carrier of chytridiomycosis, an
emerging fungal disease of amphibians. Herpetological Journal
14:201–207
Davidson E, Parris M, Collins J, Longcore JE, Pessier AP, Brunner
J (2003) Pathogenicity and transmission of chytridiomycosis in
tiger salamanders (Ambystoma tigrinum). Copeia 3:601–607
Fellers GM, Green E, Longcore JE (2001) Oral chytridiomycosis in
the mountain yellow-legged frog (Rana muscosa). Copeia 4:945–
953
Hamer AJ, Makings JA, Lane SJ, Mahony MJ (2004) Amphibian
decline and fertilizer used on agricultural land in south-eastern
Australia. Agriculture Ecosystems and Environment 102:299–305
Hanselmann R, Rodrı́guez A, Lampo M, Fajardo-Ramos L, Agu-
irre A, Kilpatrick M, et al. (2004) Presence of an emerging
pathogen of amphibians in introduced bullfrogs Rana cates-
beiana in Venezuela. Biological Conservation 120:115–119
Kriger M, Hero JM (2007) The chytrid fungus Batrachochytrium
dendrobatidis is non-randomly distributed across amphibian
breeding habitats. Diversity and Distributions; DOI:
10.1111/j.1472-4642.2007:00394.x [Online September 26, 2007]
Kriger KM, Hines HB, Hyatt AD, Boyle DG, Hero JM (2006)
Techniques for detecting chytridiomycosis in wild frogs: com-
paring histology with real-time Taqman PCR. Diseases of
Aquatic Organisms 71:141–148
La Marca E, Lips K, Lötters S, Puschendorf R, Ibáñez R, Rueda-
Almonacid JV, et al. (2005) Catastrophic population decline
and extinctions in neotropical harlequin frogs (Bufonidae: A-
telopus). Biotropica 37:190–201
Lampo M, Rodrı́guez-Contreras A, La Marca E, 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
Lips KR, Green DE, Papendick R (2003) Chytridiomycosis in wild
frogs from southern Costa Rica. Journal of Herpetology 37:215–
218
Lips KR, Mendelson JR III, Muñoz-Alonso A, Canseco-Márquez,
Mulcahy DG (2004) Amphibian population declines in mon-
tane southern Mexico: resurveys of historical localities. Biolog-
ical Conservation 119:555–564
Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium
dendrobatidis gen. et sp. nov., a chytrid pathogenic to
amphibians. Mycologia 91:219–227
Lötters S (1996) The Neotropical Toad Genus Atelopus. Checklist,
Biology, Distribution, Köln, Germany: Vences and Glaw Verlags
Lötters S, La Marca E, Stuart S, Gagliardo R, Veith M (2004) A
new dimension of current biodiversity loss?. Herpetotropicos
1:29–31
Mazzoni R, Cunningham AA, Daszak P, Apolo A, Perdomo E,
Speranza G (2003) Emerging pathogen of wild amphibians in
frogs (Rana catesbeiana) farmed for international trade.
Emerging Infectious Diseases 9:995–998
Muths E, Corn PS, Pessier A, Green DE (2003) Evidence for
disease-related amphibian decline in Colorado. Biological Con-
servation 110:357–365
Nichols DK, Pessier AP, Logcore J (1998) Cutaneous chytridi-
omycosis in amphibians: an emerging disease? Proceedings of
the American Association of Zoo Veterinarians/American
Association of Wildlife Veterinarians, Joint Conference 1998,
Media, PA: American Association of Zoo Veterinarians, pp 269–
271
Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden
ML, Foster PN, et al. (2006) Widespread amphibian extinctions

from epidemic disease driven by global warming. Nature
439:161–167
Puschendorf R, Bolaños F, Chaves G (2006) The amphibian
chytrid fungus along an altitudinal transect before the first re-
ported declines in Costa Rica. Biological Conservation 132:136–
142
Rueda-Almonacid JV, Lynch JD, Amézquita A (2004) Libro Rojo
de Anfibios de Colombia. Serie Libros Rojos de Especies Ame-
nazadas de Colombia, Bogotá, Colombia: Conservación Inter-
nacional Colombia, Instituto de Ciencias
Naturales—Universidad Nacional de Colombia, Ministerio del
Medio Ambiente
Ruiz-Carranza PM, Ardila-Robayo MC, Lynch JD (1996) Lista
actualizada de la fauna amphibia de Colombia. Revista de la
Academia Colombiana de Ciencias Exactas, Fı́sicas y Naturales
20:365–415
Speare R, Berger L (2004) Global distribution of chytridiomycosis
in amphibians. Available: http://www.jcu.edu.au/school/phtm/
PHTM/frogs/chyglob.htm [accessed, May 15, 2006]
Chytridiomycosis in Colombia 33
Stuart S, Chanson J, Cox N, Young B (2006) El estado global de
los anfibios. In: Técnicas de Inventario y Monitoreo para los
Anfibios de la Región Tropical Andina. Conservación Inter-
nacional Serie Manuales de Campo, No 2, Angulo A, Rueda-
Almonacid JV, Rodrı́guez-Mahecha JV, La Marca E (editors),
Bogotá, Colombia: Conservación Internacional, pp 19–41
Stuart S, Chanson J, Cox N, Young B, Rodrı́gues A, Fischman D,
et al. (2004) Status and trends of amphibian declines and
extinctions worldwide. Science 306:1783–1786
Weldon C, du Preez LH, Hyatt AD, Muller R, Speare R (2004)
Origin of the amphibian chytrid fungus. Emerging Infectious
Diseases 10:2100–2105
Williams SE, Hero J-M (1998) Rainforest frogs of the Australian
wet tropics: guild classification and the ecological similarity of
declining species. Proceedings of the Royal Society of London.
Series B. Biological Sciences 265:597–602
Young B, Lips K, Reaser J, Ibáñez R, Salas A, Cedeño R, et al.
(2001) Population declines and priorities for amphibian con-
servation in Latin America. Conservation Biology 15:1213–1223