Batrachochytrium Dendrobatidis in Peru
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xvi AMPHIBIAN DISEASES MUTHS, E., B. S. PEDERSEN, AND F S. PEDERSEN. 2009. How relevant is op- LITERATURE CITED portunistic Bd sampling: Are we ready for the big picture? Herpe- tol. Rev. 40(2):183–184. BOYLE, D. G., D. B. BOYLE, V. OLSEN, J. A. T. MORGAN, AND A. D. HYATT. 2004. OUELLET, M., I. MIKAELIAN, B. D. PAULI, J. RODRIGUE, AND D. M. GREEN. Rapid quantitative detection of chytridiomycosis (Batrachochytri- 2005. Historical evidence of widespread chytrid infection in North um dendrobatidis) in amphibian samples using real-time Taqman American amphibian populations. Conserv. Biol. 19:1431–1440. PCR assay. Dis. Aquat. Org. 60:141–148. RODRIGUEZ, E. M., T. GAMBLE, M. V. HIRT, AND S. COTNER. 2009. Presence BREM, F., J. R. MENDELSON III, AND K. R. LIPS. 2007. Field-Sampling Pro- of Batrachochytrium dendrobatidis at the headwaters of the Mis- tocol for Batrachochytrium dendrobatidis from Living Amphib- sissippi River, Itasca State Park, Minnesota, USA. Herpetol. Rev. ians, Using Alcohol Preserved Swabs. Version 1.0 (18 July 2007). 40(1):48–50. Electronic document accessible at <http://www.amphibianark. SADINSKI, W., M. ROTH, S. TRELEVEN, J. THEYERL, AND P. DUMMER. DETECTION org/resources/other-documents/#Chytrid>. Conservation Inter- OF THE CHYTRID FUNGUS BATRACHOCHYTRIUM DENDROBATIDIS, ON RECENTLY national, Arlington, Virginia. METAMORPHOSED AMPHIBIANS IN THE NORTH-CENTRAL UNITED STATES. HERPE- HYATT, A. D., D. G. BOYLE, V. OLSEN, D. B. BOYLE, L. BERGER, D. OBENDORF, TOL. REV. 41(2):170–175. A. DALTON, K. KRIGER, M. HERO, H. HINES, R. PHILLOT, R. CAMPBELL, G. STEINER, S. I., AND R. M. LEHTINEN. 2008. Occurrence of the amphibian MARANTELLI, F. GLEASON, AND A. COLLING. 2007. Diagnostic assays and pathogen Batrachochytrium dendrobatidis in Blanchard’s Cricket sampling protocols for the detection of Batrachochytrium dendro- Frog (Acris crepitans blanchardi) in the U.S. Midwest. Herpetol. batidis. Dis. Aquat. Org. 73:175–192. Rev. 39(2):193–196. KINNEY, V. C., J. L. HEEMEYER, A. P. PESSIER, AND M. J. LANNOO. 2011. Sea- WOODHAMS, D. C., A. D. HYATT, D. G. BOYLE, AND L. A. ROLLINS-SMITH. 2008. sonal pattern of Batrachochytrium dendrobatidis infection and The Northern Leopard Frog Rana pipiens is a widespread reser- mortality in Lithobates areolatus: Affirmation of Vredenburg’s voir species harboring Batrachochytrium dendrobatidis in North “10,000 Zoospore Rule.” PLoS ONE 6(3):e16708. doi:10.1371/jour- America. Herpetol. Rev. 39(1): 66–68. nal.pone.0016708. ZELLMER, A. J., C. L. RICHARDS, AND L. M. MARTENS. 2008. Low prevalence LODA, J. L., AND D. L. OTIS. 2009. Low prevalence of amphibian chytrid of Batrachochytrium dendrobatidis across Rana sylvatica popu- fungus (Batrachochytrium dendrobatidis) in Northern Leopard lations in southeastern Michigan, USA. Herpetol. Rev. 39(2):196– Frog (Rana pipiens) populations of north-central Iowa. Herpetol. 199. Rev. 40(4):428–431. ZIPPEL, K. C., AND C. TABAKA. 2008. Amphibian chytridiomycosis in LONGCORE, J. R., J. E. LONGCORE, A. P. PESSIER, AND W. H. HALTEMAN. 2007. captive Acris crepitans blanchardi (Blanchard’s Cricket Frog) col- Chytridiomycosis widespread in anurans of northeastern United lected from Ohio, Missouri, and Michigan, USA. Herpetol. Rev. States. J. Wildlife Manage. 71:435–444. 39(2):192–193. Herpetological Review, 2012, 43(2), 150–159. © 2012 by Society for the Study of Amphibians and Reptiles Batrachochytrium dendrobatidis in Peru The amphibian chytrid fungus, Batrachochytrium dendroba- where they were once abundant, and one of the last individu- tidis (Bd), has been well-studied in Australia, North and Central als seen was found dead and later tested Bd-positive (Lötters et America, and Europe, but relatively little information is available al. 2005). Another study in northern Peru failed to detect Bd in concerning the status of this pathogen in South America. This is 23 individuals tested using histopathological analysis (Enciso et especially disturbing given that South America contains the high- al. 2008). In southern Peru, the first record of Bd came from 3 est diversity of amphibian species in the world (Vié et al. 2009). of 4 Telmatobius marmoratus collected in 2002 in the Cordillera In Peru, sampling for Bd has been especially sparse, with only Vilcanota (Seimon et al. 2005). A later study in this region report- six studies in localized regions conducted to date (Table 1). The ed a range expansion in Bd to the highest altitude yet recorded first record of Bd in Peru came from several dead Atelopus pa- (5348 m), which Seimon et al. (2007) posit might be due to the tazensis collected in 1999 (Venegas et al. 2008). Although recent recent deglaciation and subsequent host population expansion surveys have shown that this species continues to persist, it is in the region. Additionally, it appears Bd might be contributing currently listed as critically endangered by the IUCN due to the to declines in one of the two host species in this study (Seimon combined effects of Bd and water pollution (IUCN 2011). Reli- et al. 2007). Most recently, Catenazzi et al. (2011) discovered able data are not available on the status of other Atelopus spe- dramatic declines in montane amphibian species richness and cies in Peru, though many appear to be declining (Venegas et al. abundance in southern Peru between surveys from 1999 and 2008; von May et al. 2008), a trend seen throughout the range of 2008–2009. They attributed these declines to chytridiomycosis this genus (La Marca et al. 2005). Population surveys for A. pul- rather than habitat loss because Bd is widespread in the region cher in northern Peru have not detected any adults in localities and declines occurred within the well-protected zone of Manu National Park (Catenazzi et al. 2011). TIFFANY A. KOSCH Recently, it has been shown that the global trade of amphib- Department of Biology, East Carolina University, East 5th Street, ians is a major contributor to the worldwide dispersal of Bd (Far- Greenville, North Carolina 27858, USA; rer et al. 2011; Fisher and Garner 2007). In Peru, trade of am- e-mail: [email protected] phibians is fairly common; especially in large cities such as Lima VICTOR MORALES and Cusco where Andean frogs (predominantly Telmatobius and Facultad de Ciencias Biológicas, Universidad Ricardo Palma, Lima, Peru Batrachophrynus species) are frequently sold in restaurants and KYLE SUMMERS markets as a protein source or for their perceived medicinal prop- Department of Biology, East Carolina University, East 5th Street, Greenville, North Carolina 27858, USA erties (Angulo et al. 2008). Investigations have shown that many of these frogs are Bd-positive (Catenazzi et al. 2010), indicating Herpetological Review 43(2), 2012 AMPHIBIAN DISEASES xvii TABLE 1. Summary of amphibian study sites in Peru sampled for Batrachochytrium dendrobatidis (Bd). Surveys were performed during the dry seasons (June–August) 2007 and (May–July) 2008. Locality Latitude Longitude Altitude (m) N Bd Positive Prevalence 2007 Ahuashiyacu -6.4578 -76.30843 722 15 2 0.13 Allpahuayo Mishana -3.75067 -73.28228 102 1 0 0.00 Bocatoma -6.4585 -76.34968 426 43 0 0.00 Chacos Valley and Llamaquizú -10.61583 -75.35056 1800-2100 4 1 0.25 Chazuta -6.5692 -76.12622 235-355 42 0 0.00 Huallaga River -6.58899 -75.91939 171-232 36 0 0.00 Iquitos Km 23 -3.9586 -73.375 149 37 0 0.00 Iquitos Km 71 -3.75067 -73.33228 122 15 0 0.00 Lamas -6.38493 -76.51527 645 1 0 0.00 Nanay River -3.68572 -73.2835 96 17 1 0.06 Pampa Hermosa -10.9925 -75.43278 1200-1550 10 0 0.00 Pond near Tunnel -6.43118 -76.30882 846 16 0 0.00 Pongo de Cainarachi -6.29388 -76.23598 190-220 58 0 0.00 San Jose -6.4194 -76.2901 470-589 58 0 0.00 Santa Rosa -5.4406 -78.55473 1234-1270 11 1 0.09 Sapasoa -6.89635 -76.82817 315-416 32 0 0.00 Sauce -6.72453 -76.25318 622 5 0 0.00 Seco River -8.59656 -76.08714 771 20 0 0.00 Tahuayo -4.17703 -73.15365 115 26 0 0.00 2008 Aguaytia -9.05734 -75.66543 429 6 0 0.00 Chacos Valley and Llamaquizú -10.61583 -75.35056 1800-2100 2 0 0.00 CICRA Station -12.56861 -70.09917 250-270 83 1 0.01 Cueva de las Lechuzas -9.32867 -76.02715 656 19 1 0.05 Huampal -10.18825 -75.57519 968 6 0 0.00 Ivochote -12.46317 -72.96740 471-481 32 0 0.00 Lake Milagros -9.14174 -75.99635 671-691 17 0 0.00 Lake Yarinachocha -8.32561 -74.59022 188 29 0 0.00 Manu Learning Center -12.78926 -71.39175 463 51 2 0.04 Oxapampa -10.54556 -75.35835 2355 12 0 0.00 Pilcopata -12.90997 -71.42281 480-525 49 0 0.00 Pozuzo -10.04908 -75.54059 692 10 0 0.00 Puente Maranura -12.96498 -72.66568 1068 22 0 0.00 Puerto Bermudez -10.27102 -74.93673 243-309 37 0 0.00 Puerto Inca -9.36759 -75.00175 202-229 23 0 0.00 San Pedro Market, Cusco* -13.52384 -71.97128 3363 2 1 0.50 Satipo -11.27665 -74.64673 719 23 0 0.00 Shima Venzo -11.11832 -74.22433 394-474 37 0 0.00 Tambopata Research Center -13.13333 -69.60000 350 61 0 0.00 Wayqecha -13.17956 -71.60561 2623-3240 15 1 0.07 *Specimen purchased from market that they are likely contributing to spread of the disease through- a time-constrained survey for 4 h. The primary goal of each sur- out Peru as they are moved from capture sites to markets.