Herpetologica, 76(2), 2020, 201–215 Ó 2020 by The Herpetologists’ League, Inc. Chytrid Pathogen (Batrachochytrium dendrobatidis) in African Amphibians: A Continental Analysis of Occurrences and Modeling of Its Potential Distribution 1,19 2 3,4 5,6 7 8 BREDA M. ZIMKUS ,VOJTECH BALA´ˇZ ,ANAT M. BELASEN ,RAYNA C. BELL ,ALAN CHANNING ,JOSEPH DOUMBIA ,ERIC B. 9 10 11 12,13 14 15 FOKAM ,LEGRAND N. GONWOUO ,ELI GREENBAUM ,VA´ CLAV GVOZDˇ IK´ ,MAREIKE HIRSCHFELD ,KATE JACKSON ,TIMOTHY 4 16 4 17 14 Y. JAMES ,CHIFUNDERA KUSAMBA ,JOANNA G. LARSON ,LISE-BETHY MAVOUNGOU ,MARK-OLIVER RO¨ DEL ,ANGE-GHISLAIN 17 14,18 ZASSI-BOULOU , AND JOHANNES PENNER 1 Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA 2 University of Veterinary and Pharmaceutical Sciences Brno, Faculty of Veterinary Hygiene and Ecology, Department of Biology and Wildlife Diseases, 612 42 Brno, Czech Republic 3 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA 4 Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA 5 Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA 6 Herpetology Department, California Academy of Sciences, San Francisco, CA 94118, USA 7 Unit for Environmental Sciences and Management, North-West University, Potchefstroom, 2520, South Africa 8 ONG EnviSud Guinee,´ Commune Ratoma 030BP:558 4720 Conakry, Guinee´ 9 Department of Zoology and Animal Physiology, University of Buea, 00237, Cameroon 10 Laboratory of Zoology, Faculty of Sciences, University of Yaounde´ I, P.O. Box 812, Yaounde,´ Cameroon 11 Department of Biological Sciences, University of Texas at El Paso, 500 W. University Ave., El Paso, TX 79968, USA 12 Institute of Vertebrate Biology of the Czech Academy of Sciences, 603 65 Brno, Czech Republic 13 Department of Zoology, National Museum, 193 00 Prague, Czech Republic 14 Museum fur ¨ Naturkunde Berlin, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstr. 43, 10115 Berlin, Germany 15 Department of Biology, Whitman College, 345 Boyer Avenue, Walla Walla, WA 99362, USA 16 Centre de Recherche en Sciences Naturelles, Departement´ de Biologie, Lwiro, The Democratic Republic of the Congo 17 Institut National de Recherche en Sciences Exactes et Naturelles (IRSEN), Cite´ Scientifique (Ex-ORSTOM), 2400, Republique´ du Congo 18 Chair of Wildlife Ecology and Wildlife Management, University of Freiburg, Tennenbacher Straße 4, 79106 Freiburg, Germany ABSTRACT: The fungal pathogen Batrachochytrium dendrobatidis (Bd) is implicated in global declines of amphibian populations and has been documented in African specimens originally collected as far back as the 1930s. Numerous recent surveys focusing on regional pathogen prevalence have greatly increased the number of known occurrences of Bd in African species, but few studies have focused on continental distribution patterns. We analyzed all known positive occurrences of Bd in African amphibians to date, including newly reported data from Cameroon, the Democratic Republic of the Congo, Gabon, Namibia, and the Republic of the Congo. Records from both Namibia and the Republic of the Congo reported herein represent first positive occurrences for these countries. With this most comprehensive sampling of the African continent to date we identified patterns of Bd-positive occurrences associated with (1) location (i.e., biogeographic region, country), (2) taxonomy, (3) life history, and (4) threat of extinction. We used fine-grained (30 arc seconds) environmental niche models (ENMs) to predict the continental distribution of Bd and identify hotspots for the pathogen, including areas not previously modeled to have high suitability for the fungus, and areas of high amphibian biodiversity from which Bd has not yet been documented. Our ENMs predicted that the environmentally suitable range of Bd encompasses vast areas of high amphibian biodiversity, including the Congo Basin and the Albertine Rift. Although our ENMs indicated that West Africa is environmentally suitable for Bd, the fungus has not been reported west of the Dahomey Gap. Likewise, the ENMs also identified regions across the Congo Basin and coastal Angola that are environmentally suitable for the pathogen but from which Bd has not yet been reported, underscoring a need for Bd surveys in these regions. Although amphibian declines in Africa have not been directly attributed to chytridiomycosis, Bd has been detected in over one fifth of the most-threatened African amphibians. Given the presence of the hypervirulent Bd global panzootic lineage (BdGPL) in Africa, we believe that the threat of Bd as a novel pathogen may be underestimated and that focused research is urgently needed to identify which species are susceptible to Bd-driven declines. Key words: Chytridiomycosis; Fungus; Habitat; Life history; Maxent; Taxonomy AMPHIBIANS are currently the most threatened vertebrate der Sluijs et al. 2016; Stegen et al. 2017) and causing steep group, with approximately one third of all species considered declines in populations of Fire Salamanders (Salamandra in danger of extinction with numbers continuing to rise salamandra) in the Netherlands, Belgium, and Germany. (Stuart et al. 2004; Wake and Vrendenberg 2008; IUCN Recently, Bsal was revealed to induce mass mortality in 2019). A number of causes have been linked to global Marbled Newts (Triturus marmoratus) in north-eastern declines of amphibian populations including chytridiomyco- Spain (Martel et al. 2020). Batrachochytrium dendrobatidis sis, an infectious disease caused by the chytrid fungus has been detected in 41% of amphibian species across 63% Batrachochytrium dendrobatidis (Bd), which infects the of the countries in which sampling has been reported, and keratin-containing epidermis in adults and the mouthparts in chytridiomycosis has contributed to the decline of an tadpoles (Berger et al. 1998, 2005; Johnson 2006). A second estimated 501 amphibian species worldwide, representing a species of chytrid, B. salamandrivorans (Bsal), has more catastrophic loss to biodiversity and the greatest loss recently been identified and affects salamanders, inflicting attributable to a pathogen to date (Scheele et al. 2019). skin ulcerations and necrosis (Martel et al. 2013; Spitzen-van The greatest losses attributed to Bd have been found in Central and South America, especially in large-bodied, 19 CORRESPONDENCE: email, [email protected] range-restricted anurans in wet climates, whereas the status 201 202 Herpetologica 76(2), 2020 of African amphibian chytridiomycosis-associated declines is 2019). However, the recent identification of the hyperviru- largely unknown (Hirschfeld et al. 2016; Scheele et al. 2019). lent Bd global panzootic lineage (BdGPL) in African Soto-Azat et al. (2010) documented the oldest known amphibians suggests that the threat of Bd as a novel African case of chytrid infection at the time, having detected pathogen may be underestimated (O’Hanlon et al. 2018; Bd from a museum specimen of Xenopus fraseri collected Byrne et al. 2019; Doherty-Bone et al. 2019). Herein, we from Cameroon in 1933. They suggested that southern analyze all known positive occurrences in African amphib- Africa may be the source of Bd, attributing the global spread ians to date, which include previously unpublished occur- of the fungus to the use of Xenopus laevis in human rences of Bd in several countries, to identify patterns pregnancy assays, beginning in the 1930s, and subsequent associated with distribution, taxonomic group, life history, development as a model organism for biomedical research and conservation status. We employ environmental niche (Gurdon and Hopwood 2000; Weldon et al. 2004, 2007). modeling (ENM) to test the hypothesis that areas across the Xenopus laevis is a subclinical carrier of Bd infection, and Central Africa subregion that were not previously modeled data suggest this species has exhibited a steady prevalence of as suitable habitat for Bd, specifically within the Congo infections for over 8 decades (Weldon et al. 2004; Skerratt et Basin, will be predicted as environmentally suitable for the al. 2007; Vrendenberg et al. 2013). O’Hanlon et al. (2018) fungus, given new occurrence data in this region. later refuted the ‘‘Out of Africa’’ hypothesis, concluding that the pathogen likely emerged from East Asia at the beginning MATERIALS AND METHODS of the 20th Century. The study identified known lineages of Positive Occurrence Analyses the fungus via the analysis of the genomes of hundreds of Bd samples collected from wild and captive amphibians in A systematic review of all known positive occurrences of Australia, North and South America, Africa, Asia, and Bd in continental Africa was conducted, including both Europe. They concluded that samples from Korea are published records and new accounts. Methods used to report descended from the ancestral population that gave rise to the new positive occurrences from Namibia (2007), Cameroon pandemic strain. (2009, 2016), the Democratic Republic of the Congo (2009, Although Africa was once the hypothesized source of Bd, 2010, 2013), Gabon (2013), and the Republic of the Congo the taxonomic and geographic prevalence of the pathogen (2008, 2010) are included in the Supplemental Materials and across the continent is still poorly documented. Predictions Methods (available online). Data from these new occurrenc- regarding the distribution of Bd in Africa were first based on es and