Doenças Emergentes de Anfíbios

Taran Grant | Departamento de Zoologia | taran.grant@gmail.com

I. Background sobre o declínio dos anfíbios1. História

a. Preocupação incialb. Por que os anfíbios são especiais (realmente são especiais?)c. Céticos e zelotes

2. Consenso atuala. GAAb. Taxa de “extinção” atual versus históricoc. Regiões afetadasd. Grupos afetadose. Causas

II. Doenças emergentes1. Doenças de anfíbios2. Bd

a. O que é?b. Sintomas de quitridiomicosec. Dispersão/distribuiçãod. Por que afeta algumas espécies mais do que outras?e. Interações com outros fatoresf. Conservação?

Preocupação Inicial

Incilius (ex Bufo) periglenes Monteverde, Costa Rica

Comum até 1988 – extinto

Rheobatrachus silusSudeste de Austrália

Comum até 1981 – extinto

Rana cascadae

Rana aurora

Rana muscosa

Várias espécies do oeste da América do Norte

Anaxyrus (ex Bufo) boreus

BioScience 1990Science 1991

Science 1990

Cons. Biol. 1990

Por que os anfíbios são bioindicadores especiais?(e.g., Blaustein & Wake, 1995)

1. Em contato íntimo com vários componentes do meiovida bifásicaanuros: herbívoros aquáticos/carnívoros terrestrespele fina, úmidaovos sem casco

2. Baixa vagilidade

BioScience 2000 Beebee et al. 2005

Realmente são especiais?

Céticos & Zelotes

1. Falta de evidência para diferenciar entre flutuações populacionais “normais” e declínios

2. Falta de evidência sobre causas

“...início de uma extinção local” (K. Lips)“...causado por algum protozoário” (D. Green)

Falta de chuva???

Consenso AtualGlobal Amphibian Assessment 2004

>500 cientistas de 60 paises

http://www.globalamphibians.org/

32% dos anfíbios são ameaçados435 spp “rapidly declining” (=pior que 1980)

Taxa de “Extinção”

Stuart et al. 2004

Regiões Afetadas

América do Sul:Bufonidae (Atelopus)Dendrobatidae (Colostethus, Hyloxalus)Hylodidae (Crossodactylus)Terrarana (Pristimantis)

Grupos Afetados

Corey & Waite 2008

Causas(Collins et al., 2003)

Classe I: Causas “compreendidas”Introdução de espécies exóticasSobre exploração Modificação de hábitat

Classe II: Causas não compreendidasMudanças mundiais: redução da capa de ozônio, mudanças climáticasPoluição do meio ambiente: poluentes orgânicos persistentes, metais pesadosDoenças emergentes

Doenças Emergentes

Vários patógenos associados com anfíbiosI. Virus: Ranavirus (Inviridae)2. Bacteria: Aeromonas hydrophila3. Trematoda: infestações causam malformações dos membros4. Fungos: Saprolegnia ferax ataca ovos

Batrachochytrium dendrobatidis (Bd)

Descoberto em 1997, descrito em 1999

Chytriodiomycota: usualmente aquáticos, com zoósporos flagelados, livres, parasitas de algas, plantas, invertebrados, fungos

Bd é a única espécie do grupo que infecta e se desenvolve dentro das células queratinizadas epidérmicas da pele de anfíbios vivos (larvas e adultos)

Causa quitridiomicose

Quitridiomicose = causa próxima de declínios na América Central e Austrália, implicado nos declínios da América do Norte, América do Sul, Europa

Pós-metamórficos: hiperplasia (aumento no número de células), hiperqueratose (engrossamento do estrato córneo), interfere na respiração?

Larvas: malformações do disco oral

Batrachochytrium dendrobatidis (Bd)

Fellers et al. 2001

esporángio intracelular

tubos de descarga (saída de zoósporos)

estrato córneo engrossado

Burger et al. 1998

lations on our new analyses correlating time since probableinfection and distance of spread.

We tested the robustness of the relationship between ATand LYO data reported in [17] (see Figure 3 in [17]), using aMonte Carlo analysis to examine the effect of systematicerror on LYO date that might be expected from samplingerror for Tier 1 species. First, we added bidirectional erroraround LYO data sampled from a normal distribution, with amean of zero and an increasing standard deviation of up to 6y (a conservative amount given the observed differences). Thistype of error would imply that either a DOD (not necessarilyan extinction event) occurred sometime around the LYOdate, or that because searches for individuals used in LYO

dates were not systematic, the true LYO date could have beenmissed. Next, we added error forward in time only, indicatingthat the real date of extinction occurred sometime after thelast observed individual was noticed by observers in the field.This error could especially be likely given that individualsfrom populations at low density might be difficult to detectand because, as above, searches for individuals were notsystematic. This directional error was modeled in three ways.First, we added error to LYO sampled from a uniformdistribution, with error ranging from 0 to 6 y (i.e., LYO was aslikely to occur some time after the reported date as it waslikely to occur at some time close to the reported date).Second, we added error sampled from a Poisson distribution,

Figure 2. Map of Central American Spreading Wave (Wave 1) with DOD Sites Indicated and Rate of Spread

DOD sites are indicated by open circles. Black bars indicate the hypothesized leading edge of the wave of Bd in the year indicated.doi:10.1371/journal.pbio.0060072.g002

We present elevational range for each listing and geographic coordinates. Geographic coordinates provided for a species represent the geographic centroid of the known range of thespecies, based on data from the GAA. Elevational data and geographic coordinates associated with site-specific declines represent location of the site. LYO and conservation statusrankings are from [14]: Stable¼population persisted through 1999 and no population has declined by.50%; Decline¼at least one population declined by.50%. We designated specificpopulations of A. varius, although all populations were considered together by [14,17]. We have considered separately the taxonomic and conservation status of the populations of frogson Isla Gorgona, Colombia, (variously referred to A. elegans or A. gracilis) from the mainland populations in Ecuador (A. elegans). Location information for A. spumarius subspecies maycontain error, given taxonomic uncertainties and differences between notes in [14] and GAA maps, although these errors would not affect maps of Bd spread because DOD and LYO datesare later than the final year of total spread (2000). A. balios declined due to habitat loss, not Bd, and was not included in analyses. Stable species were also not included in invasion waves.aSpecies has disappeared, with no records since 1998 despite repeated searches.bEvents are indicated on Figure 1 (Central America).cEvents are indicated on Figure 2 (South America).dAtelopus tricolor was listed as Stable in Peru [17], although expert commentaries in the original database [14] indicate a DOD in 1999–2000 (see Methods).doi:10.1371/journal.pbio.0060072.t001

PLoS Biology | www.plosbiology.org March 2008 | Volume 6 | Issue 3 | e720445

Climate, Disease, and Amphibian Declines

Lips et al., 2008

DispersãoSpatio-temporal Spread Hypothesis

Espécie invasora: Lithobates catesbeianus, rã-touro

Fisher et al. 2009

Distribuição Global

Bd distribuição atual e potencial

Bd distribuição potencial com riqueza de espécies

Bd “risco”, incluindo idoneidade climática para Bd e característics de história natural dos anfíbios

Rödder et al. 2009

Martel et al. 2014, Science

Por que afeta algumas espécies mais do que outras?

Sistema imune inato (defesa química)Peptídeos antimicrobianos (e.g., Pask et al., 2012)

Sistema imune adaptativo/adquiridoComplexo principal de histocompatibilidade (Savage & Zamudio, 2011, 2016)

Microbioma dérmicoBactérias anti-Bd (e.g., Harris et al. 2009, Bresciano et al. 2015, Bataille et al. 2015, )

Interações com Outros Fatores

Chytrid-Thermal-Optimum Hypothesis (Pounds et al. 2006)

T ºC min maior e T ºC max menor favorecem o Bd

mudança correlacionada com declínio de Atelopus

PNAS 2010

Nature 2011

mudança de clima + quitridiomicose

mudança de clima + mudança no uso da terra

mudança no uso da terra + quitridiomicose

Hof et al. 2011

Bd + …desmatamentotipo de habitat

mudança climáticaestresse ambientalimuno-competência

uso da terracobertura vegetal

pesticidasqualidade de agua

2016

2016

7 JULY 2006 VOL 313 SCIENCE www.sciencemag.org48

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Amphibian declines and extinctions areglobal and rapid: 32.5% of 5743 de-scribed species are threatened, with at

least 9, and perhaps 122, becoming extinct since1980 (1). Species have disappeared across theentire taxonomic group and in nearly all regionsof the planet. These figures are probably under-estimates as entire clades of species are threat-ened. For example, of the 113 species of harle-quin toads (genus Atelopus), 30 are possiblyextinct, and only 10 have stable populations (2).Nearly a quarter of known amphibian specieswere deemed “data-deficient” with respect toconservation status in the recent global assess-ment (1). Losing biodiversity at this taxonomicscale impacts ecosystem goods and services[e.g. (3, 4)]. As amphibian species disappear, wealso lose their untapped potential for advances inbiomedicine and biotechnology in general (5).

Losses result from familiar threats (land-usechange, commercial overexploitation, and exoticspecies) and from the emerging infectious dis-ease chytridiomycosis, caused by the fungusBatrachochytrium dendrobatidis (Bd). Pre-dictions are that within 4 to 6 months of Bd

arrival at a site where it has not previously beenpresent, ~50% of amphibian species and ~80%of individuals may disappear (6). Global climatechange may be encouraging local conditionsideal for Bd’s persistence and/or spread (7), com-mercial trade of wildlife may also contribute (8),and pollution may increase susceptibility ofspecies to pathogens (9, 10). Traditional pro-grams and current laws and policies alone areinsufficient to address global threats that crossboundaries of reserves and nations.

Global leaders in research, conservation, andpolicy agreed on an Amphibian ConservationAction Plan (ACAP) and Declaration in 2005(see Supporting Online Material). A new, inter-national body was recommended to coordinateand facilitate conservation programs for amphib-

ians and to garner and administer funds. Thus,we call for formation of The Amphibian SurvivalAlliance (ASA)—led by an international secre-tariat of the Amphibian Specialist Group of theSpecies Survival Commission of IUCN (WorldConservation Union). An initial 5-year budgetrequires at least U.S.$400 million.

Conservation activities should remain inaffected countries where possible, with coordi-nation and support through ASA, to engageand employ local scientists. A special initiativewould be regional centers for disease researchand captive breeding. Centers would existwithin government agencies, zoos, or universi-ties and would be staffed by local scientists,wildlife managers, and conservationists. ASAwould create and support readily availabledatabases from the global network of centers,as well as research and training in countrieswith few amphibian experts. Such dedicatedresearch capacity in affected regions is re-quired for this global crisis, as well as to keepamphibian research and conservation at theforefront of policy-making.

Chytridiomycosis deserves especial attentionbecause of its massive impacts on amphibiandiversity (11, 12). Natural-agent control of Bd orselecting for resistance in amphibians may bepossible (13, 14). In the meantime, we mustimplement coordinated in situ actions (e.g.,surveys, monitoring, and habitat protection) andex situ husbandry programs (e.g., survival-assurance and research colonies) at unprece-dented scales. Amphibian salvage operations arepossible at an ecosystem level (15). Ex situ pro-grams may be the only option to avoid extinctionfor many species [e.g., Kihansi Spray Toadand Panamanian Golden Frog (16, 17)], whileresearch progresses on disease control, treat-ment, and evolution of resistance (18).

The ASA model builds on programs suchas the Turtle Survival Alliance (19), GlobalEnvironment Facility (GEF) Coral Program(20), and an Australian threat abatement plan(21). Success will depend on a paradigm shiftin the scale of the coordinated response, with

stakeholders from the academic, conservation,zoo, ethics, policy, global change, privatesector, and international biodiversity conven-tion communities uniting for one goal. Supportfrom individuals, governments, foundations,and the wider conservation community isessential.

References and Notes1. S. N. Stuart et al., Science 306, 1783 (2004).2. E. La Marca et al., Biotropica 37, 190 (2005).3. J. A. Pounds et al.,Nature 398, 611 (1999).4. M. R. Whiles et al., Front. Ecol. 4, 27 (2006).5. S. E. VanCompernolle et al., J. Virol. 79, 11598 (2005).6. K. R. Lips et al., Proc. Natl. Acad. Sci. U.S.A. 103, 3165

(2006).7. J. A. Pounds et al., Nature 439, 161 (2006).8. C. Weldon et al., Emerg. Infect. Dis. 10, 2100 (2004).9. J. Kiesecker, Proc. Natl. Acad. Sci. U.S.A. 99, 9900

(2002).10. T. B. Hayes et al., Environ. Health Perspect. 114

(suppl. 1), 40 (2006).11. L. Berger et al., Proc. Natl. Acad. Sci. U.S.A. 95, 9031

(1998).12. P. Daszak et al., Science 287, 443 (2000).13. R. N. Harris et al., Ecohealth 3, 53 (2006).14. R.W. R. Retallick et al., PLoS 2, 1 (2004).15. J. R. Mendelson III, G. B. Rabb, WAZA Proceedings, World

Association of Zoos and Aquariums, 60th Annual Meeting,New York, 2 to 6 October 2005, in press.

16. K. Krajick, Science 311, 1230 (2006).17. K. C. Zippel, Herpetol. Rev. 33, 11 (2002).18. H. McCallum, Conserv. Biol. 19, 1421 (2005).19. Turtle Survival Alliance (www.turtlesurvival.org).20. Coral Reef Targeted Research and Capacity Building for

Management (CRTR) (www.gefcoral.org)21. Threat abatement plans, infection of amphibians with

chytrid fungus resulting in chytridiomycosis(www.deh.gov.au/biodiversity/threatened/publications/tap/chytrid/)

Supporting Online Material

www.sciencemag.org/cgi/content/full/313/5783/48/DC1

10.1126/science.1128396

POLICYFORUM

Stopping further global losses of amphibian

populations and species requires an

unprecedented conservation response.

Confronting AmphibianDeclines and Extinctions

BIODIVERSITY

The Panamanian Golden Frog, Atelopus zeteki,is nearly extinct in the wild as a combined resultof habitat change, illegal collecting, and fungaldisease; the species is currently secure in severalex situ programs.

Joseph R. Mendelson III,* Karen R. Lips, Ronald W. Gagliardo, George B. Rabb, James P. Collins,James E. Diffendorfer, Peter Daszak, Roberto Ibáñez D., Kevin C. Zippel, Dwight P. Lawson, KevinM. Wright, Simon N. Stuart, Claude Gascon, Hélio R. da Silva, Patricia A. Burrowes, Rafael L.Joglar, Enrique La Marca, Stefan Lötters, Louis H. du Preez, Ché Weldon, Alex Hyatt, JoséVicente Rodriguez-Mahecha, Susan Hunt, Helen Robertson, Brad Lock, Christopher J.Raxworthy, Darrel R. Frost, Robert C. Lacy, Ross A. Alford, Jonathan A. Campbell, GabrielaParra-Olea, Federico Bolaños, José Joaquin Calvo Domingo, Tim Halliday, James B. Murphy,Marvalee H. Wake, Luis A. Coloma, Sergius L. Kuzmin, Mark Stanley Price, Kim M. Howell,Michael Lau, Rohan Pethiyagoda, Michelle Boone, Michael J. Lannoo, Andrew R. Blaustein,Andy Dobson, Richard A. Griffiths, Martha L. Crump, David B. Wake, Edmund D. Brodie Jr.

*To whom correspondence should be addressed. E-mail:jmendelson@zooatlanta.org. All author affiliations can befound in the Supporting Online Material.

Published by AAAS

Conservação?

I. Background sobre o declínio dos anfíbios1. História

a. Preocupação incialb. Por que os anfíbios são especiais (realmente são especiais?)c. Céticos e zelotes

2. Consenso atuala. GAAb. Taxa de “extinção” atual versus históricoc. Regiões afetadasd. Grupos afetadose. Causas

II. Doenças emergentes1. Doenças de anfíbios2. Bd

a. O que é?b. Sintomas de quitridiomicosec. Dispersão/distribuiçãod. Por que afeta algumas espécies mais do que outras?e. Interações com outros fatoresf. Conservação?

Anomaloglossus atopoglossus