Abstract
Understanding the ecosystem-level persistence of pathogens is essential for predicting and measuring host–pathogen dynamics. However, this process is often masked, in part due to a reliance on host-based pathogen detection methods. The amphibian pathogens Batrachochytrium dendrobatidis (Bd) and B. salamandrivorans (Bsal) are pathogens of global conservation concern. Despite having free-living life stages, little is known about the distribution and persistence of these pathogens outside of their amphibian hosts. We combine historic amphibian monitoring data with contemporary host- and environment-based pathogen detection data to obtain estimates of Bd occurrence independent of amphibian host distributions. We also evaluate differences in filter- and swab-based detection probability and assess inferential differences arising from using different decision criteria used to classify samples as positive or negative. Water filtration-based detection probabilities were lower than those from swabs but were > 10%, and swab-based detection probabilities varied seasonally, declining in the early fall. The decision criterion used to classify samples as positive or negative was important; using a more liberal criterion yielded higher estimates of Bd occurrence than when a conservative criterion was used. Different covariates were important when using the liberal or conservative criterion in modeling Bd detection. We found evidence of long-term Bd persistence for several years after an amphibian host species of conservation concern, the boreal toad (Anaxyrus boreas boreas), was last detected. Our work provides evidence of long-term Bd persistence in the ecosystem, and underscores the importance of environmental samples for understanding and mitigating disease-related threats to amphibian biodiversity.
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References
Almberg ES, Cross PC, Johnson CJ, Heisey DM, Richards BJ (2011) Modeling routes of chronic wasting disease transmission: environmental prion persistence promotes deer population decline and extinction. PLoS One 6:e19896. https://doi.org/10.1371/journal.pone.0019896
Arnold TW (2010) Uninformative parameters and model selection using Akaike’s Information Criterion. J Wildl Manag 74:1175–1178. https://doi.org/10.2193/2009-367
Berger L, Hyatt AD, Speare R, Longcore JE (2005) Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Organ 68:51–63. https://doi.org/10.3354/dao068051
Bletz MC, Rebollar EA, Harris RN (2015) Differential efficiency among DNA extraction methods influences detection of the amphibian pathogen Batrachochytrium dendrobatidis. Dis Aquat Organ 113:1–8. https://doi.org/10.3354/dao02822
Blooi M, Pasmans F, Longcore JE, der Sluijs AS, Vercammen F, Martel A (2013) Duplex real-time PCR for rapid simultaneous detection of Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans in amphibian samples. J Clin Microbiol 51:4173–4177. https://doi.org/10.1128/JCM.02313-13
Boreal Toad Recovery Team, Loeffler (ed) (2001) Conservation plan and agreement for the management and recovery of the southern Rocky Mountain population of the boreal toad Bufo boreas boreas. Boreal Toad Recovery Team
Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Organ 60:141–148. https://doi.org/10.3354/dao060141
Breban R, Drake JM, Stallknecht DE, Rohani P (2009) The role of environmental transmission in recurrent avian influenza epidemics. PLoS Comput Biol 5:e1000346. https://doi.org/10.1371/journal.pcbi.1000346
Briggs CJ, Knapp RA, Vredenburg VT (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc Natl Acad Sci 107:9695–9700. https://doi.org/10.1073/pnas.0912886107
Broza M, Halpern M (2001) Pathogen reservoirs: Chironomid egg masses and Vibrio cholerae. Nature 412:40. https://doi.org/10.1038/35083691
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Carey C (1993) Hypothesis concerning the causes of the disappearance of boreal toads from the mountains of Colorado. Conserv Biol 7:355–362
Carey C, Bruzgul JE, Livo LJ, Walling ML, Kuehl KA, Dixon BF, Pessier AP, Alford RA, Rogers KB (2006) Experimental exposures of boreal toads (Bufo boreas) to a pathenogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3:5–21. https://doi.org/10.1007/PL00021734
Carver S, Marm Kilpatrick A, Kuenzi A, Douglass R, Ostfeld RS, Weinstein P (2010) Environmental monitoring to enhance comprehension and control of infectious diseases. J Environ Monit 12:2048–2055. https://doi.org/10.1039/C0EM00046A
Chestnut T, Anderson C, Popa R, Blaustein AR, Voytek M, Olson DH, Kirshtein J (2014) Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America. PLoS One 9:e106790. https://doi.org/10.1371/journal.pone.0106790
Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443–449. https://doi.org/10.1126/science.287.5452.443
Dejean T, Valentini A, Duparc A, Pellier-Cuit S, Pompanon F, Taberlet P, Miaud C (2011) Persistence of environmental DNA in freshwater ecosystems. PLoS One 6:e23398. https://doi.org/10.1371/journal.pone.0023398
Di Rosa I, Simoncelli F, Fagotti A, Pascolini R (2007) Ecology: the proximate cause of frog declines? Nature 447:E4–E5. https://doi.org/10.1038/nature04246
Dillon MJ, Bowkett AE, Bungard MJ, Beckman KM, O’Brien MF, Bates K, Fisher MC, Stevens JR, Thornton CR (2017) Tracking the amphibian pathogens Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans using a highly specific monoclonal antibody and lateral-flow technology. Microb Biotechnol 10:381–394. https://doi.org/10.1111/1751-7915.12464
Dobson A (2004) Population dynamics of pathogens with multiple host species. Am Nat 164:S64–S78. https://doi.org/10.1086/424681
Doherty PF, Nichols JD, Tautin J, Voelzer JF, Smith GW, Benning DS, Bentley VR, Bidwell JK, Bollinger KS, Brazda AR, Buelna EK, Goldsberry JR, King RJ, Roetker FH, Solberg JW, Thorpe PP, Wortham JS (2002) Sources of variation in breeding-ground fidelity of mallards (Anas platyrhynchos). Behav Ecol 13:543–550. https://doi.org/10.1093/beheco/13.4.543
Dugger KM, Forsman ED, Franklin AB, Davis RJ, White GC, Schwarz CJ, Burnham KP, Nichols JD, Hines JE, Yackulic CB, Doherty PF, Bailey L, Clark DA, Ackers SH, Andrews LS, Augustine B, Biswell BL, Blakesley J, Carlson PC, Clement MJ, Diller LV, Glenn EM, Green A, Gremel SA, Herter DR, Higley JM, Hobson J, Horn RB, Huyvaert KP, McCafferty C, McDonald T, McDonnell K, Olson GS, Reid JA, Rockweit J, Ruiz V, Saenz J, Sovern SG (2016) The effects of habitat, climate, and Barred Owls on long-term demography of Northern Spotted Owls. Condor 118:57–116. https://doi.org/10.1650/CONDOR-15-24.1
Ficetola GF, Miaud C, Pompanon F, Taberlet P (2008) Species detection using environmental DNA from water samples. Biol Lett 4:423–425. https://doi.org/10.1098/rsbl.2008.0118
Ficetola GF, Pansu J, Bonin A, Coissac E, Giguet-Covex C, De Barba M, Gielly L, Lopes CM, Boyer F, Pompanon F, Rayé G, Taberlet P (2015) Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data. Mol Ecol Resour 15:543–556. https://doi.org/10.1111/1755-0998.12338
Fisher MC (2017) Ecology: in peril from a perfect pathogen. Nature 544:300–301. https://doi.org/10.1038/544300a
Fisher MC, Garner TW, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol 63:291–310. https://doi.org/10.1146/annurev.micro.091208.073435
Garmyn A, Van Rooij P, Pasmans F, Hellebuyck T, Van Den Broeck W, Haesebrouck F, Martel A (2012) Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS One 7:e35038. https://doi.org/10.1371/journal.pone.0035038
Garner TW, Schmidt BR, Martel A, Pasmans F, Muths E, Cunningham AA, Weldon C, Fisher MC, Bosch J (2016) Mitigating amphibian chytridiomycoses in nature. Philos Trans R Soc Lond B Biol Sci 371:20160207. https://doi.org/10.1098/rstb.2016.0207
Gerber BD, Converse SJ, Muths E, Bailey LL, Mosher BA (2018) Identifying species conservation strategies to reduce disease-associated declines. Conserv Lett 11:1–10. https://doi.org/10.1111/conl.12393
Godfray HCJ, Briggs CJ, Barlow ND, O’Callaghan M, Glare TR, Jackson TA (1999) A model of insect—pathogen dynamics in which a pathogenic bacterium can also reproduce saprophytically. Proc R Soc Lond B Biol Sci 266:233–240. https://doi.org/10.1098/rspb.1999.0627
Goldberg CS, Turner CR, Deiner K, Klymus KE, Thomsen PF, Murphy MA, Spear SF, McKee A, Oyler-McCance SJ, Cornman RS et al (2016) Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods Ecol Evol 7:1299–1307. https://doi.org/10.1111/2041-210X.12595
Gomez-Diaz E, Doherty PF, Duneau D, McCoy KD (2010) Cryptic vector divergence masks vector-specific patterns of infection: an example from the marine cycle of Lyme borreliosis. Evol Appl 3:391–401. https://doi.org/10.1111/j.1752-4571.2010.00127.x
Grant EHC, Muths E, Katz RA, Canessa S, Adams MJ, Ballard JR, Berger L, Briggs CJ, Coleman JT, Gray MJ, Harris MC, Harris RN, Hossack B, Huyvaert KP, Kolby J, Lips KR, Lovich RE, McCallum HI, Mendelson JR, Nanjappa P, Olson DH, Powers JG, Richgels KL, Russell RE, Schmidt BR, Spitzen-van der Sluijs A, Watry MK, Woodhams DC, White CL (2017) Using decision analysis to support proactive management of emerging infectious wildlife diseases. Front Ecol Environ 15:214–221. https://doi.org/10.1002/fee.1481
Hammerson GA (1999) Amphibians and reptiles in Colorado, 2nd edn. University Press of Colorado, Colorado Division of Wildlife, Niwot
Hammerson GA, Langlois D (1981) Colorado reptile and amphibian distribution latilong study. Colorado Division of Wildlife, Denver
Hossack BR, Corn PS (2007) Responses of pond-breeding amphibians to wildfire: short-term patterns in occupancy and colonization. Ecol Appl 17:1403–1410. https://doi.org/10.1890/06-2037.1
Hoyt JR, Langwig KE, Sun K, Lu G, Parise KL, Jiang T, Frick WF, Foster JT, Feng J, Kilpatrick AM (2016) Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions. Proc R Soc Lond B Biol Sci 283:20152861. https://doi.org/10.1098/rspb.2015.2861
Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, Obendorf D, Dalton A, Kriger K, Hero M, Hines H (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis Aquat Organ 73:175–192. https://doi.org/10.3354/dao073175
Hyman OJ, Collins JP (2012) Evaluation of a filtration-based method for detecting Batrachochytrium dendrobatidis in natural bodies of water. Dis Aquat Organ 97:185–195. https://doi.org/10.3354/dao02423
Johnson ML, Speare R (2003) Survival of Batracochytrium dendrobatidis in water: quarantine and disease control implications. Emerg Infect Dis 9:922–925. https://doi.org/10.3201/eid0908.030145
Johnson ML, Speare R et al (2005) Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Dis Aquat Organ 65:181–186. https://doi.org/10.3354/dao065181
Kerby JL, Schieffer A, Brown JR, Whitfield S (2012) Utilization of fast qPCR techniques to detect the amphibian chytrid fungus: a cheaper and more efficient alternative method. Methods Ecol Evol 1:5. https://doi.org/10.1111/j.2041-210x.2012.00263.x
Kirshtein JD, Anderson CW, Wood JS, Longcore JE, Voytek MA (2007) Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. Dis Aquat Organ 77:11–15. https://doi.org/10.3354/dao01831
Kriger KM, Hero J-M (2007) Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. J Zool 271:352–359. https://doi.org/10.1111/j.1469-7998.2006.00220.x
Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118. https://doi.org/10.2307/2937171
Liew N, Moya MJM, Wierzbicki CJ, Hollinshead M, Dillon MJ, Thornton CR, Ellison A, Cable J, Fisher MC, Mostowy S (2017) Chytrid fungus infection in zebrafish demonstrates that the pathogen can parasitize non-amphibian vertebrate hosts. Nat Commun 8:15048. https://doi.org/10.1038/ncomms15048
Livo LJ (2004) Methods for obtaining Batrachochytrium dendrobatidis (Bd) samples for PCR testing. Colo Div Wildl Boreal Toad Res Rep 2003:64–68
Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227. https://doi.org/10.2307/3761366
Lorch JM, Muller LK, Russell RE, O’Connor M, Lindner DL, Blehert DS (2013) Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United States. Appl Environ Microbiol 79:1293–1301. https://doi.org/10.1128/AEM.02939-12
MacKenzie DI, Nichols JD, Lachman GB, Droege S, Andrew Royle J, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248–2255
Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W, Ducatelle R, Fisher MC, Woeltjes A, Bosman W, Chiers K, Bossuyt F, Pasmans F (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc Natl Acad Sci 110:15325–15329. https://doi.org/10.1073/pnas.1307356110
McClintock BT, Nichols JD, Bailey LL, MacKenzie DI, Kendall WL, Franklin AB (2010) Seeking a second opinion: uncertainty in disease ecology. Ecol Lett 13:659–674. https://doi.org/10.1111/j.1461-0248.2010.01472.x
McKee AM, Spear SF, Pierson TW (2015) The effect of dilution and the use of a post-extraction nucleic acid purification column on the accuracy, precision, and inhibition of environmental DNA samples. Biol Conserv 183:70–76. https://doi.org/10.1016/j.biocon.2014.11.031
McMahon TA, Brannelly LA, Chatfield MW, Johnson PT, Joseph MB, McKenzie VJ, Richards-Zawacki CL, Venesky MD, Rohr JR (2013) Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proc Natl Acad Sci 110:210–215. https://doi.org/10.1073/pnas.1200592110
Miller DAW, Talley BL, Lips KR, Campbell Grant EH (2012) Estimating patterns and drivers of infection prevalence and intensity when detection is imperfect and sampling error occurs. Methods Ecol Evol 3:850–859. https://doi.org/10.1111/j.2041-210X.2012.00216.x
Minakawa N, Sonye G, Mogi M, Githeko A, Yan G (2002) The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. J Med Entomol 39:833–841. https://doi.org/10.1603/0022-2585-39.6.833
Mitchell KM, Churcher TS, Garner TWJ, Fisher MC (2008) Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proc R Soc Lond B Biol Sci 275:329–334. https://doi.org/10.1098/rspb.2007.1356
Mosher BA, Huyvaert KP, Chestnut T, Kerby JL, Madison JD, Bailey LL (2017) Design- and model-based strategies for detecting and quantifying an amphibian pathogen in environmental samples. Ecol Evol 7:10952–10962. https://doi.org/10.1002/ece3.3616
Mosher BA, Bailey LL, Hubbard BA, Huyvaert KP (2018a) Inferential biases linked to unobservable states in complex occupancy models. Ecography 41:32–39. https://doi.org/10.1111/ecog.02849
Mosher BA, Bailey LL, Muths E, Huyvaert KP (2018b) Host-pathogen metapopulation dynamics suggest high elevation refugia for boreal toads. Ecol Appl. https://doi.org/10.1002/eap.1699
Moyer GR, Díaz-Ferguson E, Hill JE, Shea C (2014) Assessing environmental DNA detection in controlled lentic systems. PLoS One 9:e103767. https://doi.org/10.1371/journal.pone.0103767
Muths E, Stephen Corn P, Pessier AP, Earl Green D (2003) Evidence for disease-related amphibian decline in Colorado. Biol Conserv 110:357–365. https://doi.org/10.1016/S0006-3207(02)00239-2
Muths E, Pilliod DS, Livo LJ (2008) Distribution and environmental limitations of an amphibian pathogen in the Rocky Mountains, USA. Biol Conserv 141:1484–1492. https://doi.org/10.1016/j.biocon.2008.03.011
Muths E, Bailey LL, Watry MK (2014) Animal reintroductions: an innovative assessment of survival. Biol Conserv 172:200–208. https://doi.org/10.1016/j.biocon.2014.02.034
Navidi W, Arnheim N, Waterman MS (1992) A multiple-tubes approach for accurate genotyping of very small DNA samples by using PCR: statistical considerations. Am J Hum Genet 50:347
Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Garner TWJ, Weaver G, Fisher MC, The Bd Mapping Group (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS One 8:e56802. https://doi.org/10.1371/journal.pone.0056802
Petersen CE, Lovich RE, Phillips CA, Dreslik MJ, Lannoo MJ (2016) Prevalence and seasonality of the amphibian chytrid fungus Batrachochytrium dendrobatidis along widely separated longitudes across the United States. EcoHealth 13:368–382. https://doi.org/10.1007/s10393-016-1101-4
Pilliod DS, Muths E, Scherer RD, Bartelt PE, Corn PS, Hossack BR, Lambert BA, McCaffery R, Gaughan C (2010) Effects of amphibian chyrid fungus on individual survival probability in wild boreal toads. Conserv Biol 24:1259–1267. https://doi.org/10.1111/j.1523-1739.2010.01506.x
Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15. https://doi.org/10.1080/15572536.2005.11832990
Reeder NM, Pessier AP, Vredenburg VT (2012) A reservoir species for the emerging amphibian pathogen Batrachochytrium dendrobatidis thrives in a landscape decimated by disease. PLoS One 7:e33567. https://doi.org/10.1371/journal.pone.0033567
Richgels KL, Russell RE, Adams MJ, White CL, Grant EHC (2016) Spatial variation in risk and consequence of Batrachochytrium salamandrivorans introduction in the USA. R Soc Open Sci 3:150616. https://doi.org/10.1098/rsos.150616
Rogers DJ, Randolph SE (2000) The global spread of malaria in a future, warmer world. Science 289:1763–1766. https://doi.org/10.1126/science.289.5485.1763
Royle JA, Nichols JD (2003) Estimating abundance from repeated presence-absence data or point counts. Ecology 84:777–790
Scheele BC, Hunter DA, Brannelly LA, Skerratt LF, Driscoll DA (2017) Reservoir-host amplification of disease impact in an endangered amphibian. Conserv Biol 31:592–600. https://doi.org/10.1111/cobi.12830
Schmidt BR, Kéry M, Ursenbacher S, Hyman OJ, Collins JP (2013) Site occupancy models in the analysis of environmental DNA presence/absence surveys: a case study of an emerging amphibian pathogen. Methods Ecol Evol 4:646–653. https://doi.org/10.1111/2041-210X.12052
Shapard EJ, Moss AS, Francisco MJS (2012) Batrachochytrium dendrobatidis can infect and cause mortality in the nematode Caenorhabditis elegans. Mycopathologia 173:121–126. https://doi.org/10.1007/s11046-011-9470-2
Sharp A, Pastor J (2011) Stable limit cycles and the paradox of enrichment in a model of chronic wasting disease. Ecol Appl 21:1024–1030. https://doi.org/10.1890/10-1449.1
Shin J, Bataille A, Kosch TA, Waldman B (2014) Swabbing often fails to detect amphibian chytridiomycosis under conditions of low infection load. PLoS One 9:e111091. https://doi.org/10.1371/journal.pone.0111091
Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, Hines HB, Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–134. https://doi.org/10.1007/s10393-007-0093-5
Spitzen-van der Sluijs A, Spikmans F, Bosman W, de Zeeuw M, van der Meij T, Goverse E, Kik M, Pasmans F, Martel A (2013) Rapid enigmatic decline drives the fire salamander (Salamandra salamandra) to the edge of extinction in the Netherlands. Amphib-Reptil 34:233–239. https://doi.org/10.1163/15685381-00002891
Stegen G, Pasmans F, Schmidt BR, Rouffaer LO, Van Praet S, Schaub M, Canessa S, Laudelout A, Kinet T, Adriaensen C, Haesebrouck F, Bert W, Bossuyt F, Martel A (2017) Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nature 544:353–356. https://doi.org/10.1038/nature22059
Thomsen PF, Kielgast J, Iversen LL, Wiuf C, Rasmussen M, Gilbert MTP, Orlando L, Willerslev E (2012) Monitoring endangered freshwater biodiversity using environmental DNA. Mol Ecol 21:2565–2573. https://doi.org/10.1111/j.1365-294X.2011.05418.x
Venesky MD, Liu X, Sauer EL, Rohr JR (2014) Linking manipulative experiments to field data to test the dilution effect. J Anim Ecol 83:557–565. https://doi.org/10.1111/1365-2656.12159
Walker SF, Baldi Salas M, Jenkins D, Garner TWJ, Cunningham AA, Hyatt AD, Bosch J, Fisher MC (2007) Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. Dis Aquat Organ 77:105. https://doi.org/10.3354/dao01850
White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:S120–S139
Woodhams DC, Ardipradja K, Alford RA, Marantelli G, Reinert LK, Rollins-Smith LA (2007) Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim Conserv 10:409–417. https://doi.org/10.1111/j.1469-1795.2007.00130.x
Woodworth BL, Atkinson CT, LaPointe DA, Hart PJ, Spiegel CS, Tweed EJ, Henneman C, LeBrun J, Denette T, DeMots R, Kozar KL, Triglia D, Lease D, Gregor A, Smith T, Duffy D (2005) Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proc Natl Acad Sci USA 102:1531–1536. https://doi.org/10.1073/pnas.0409454102
Yackulic CB, Nichols JD, Reid J, Der R (2015) To predict the niche, model colonization and extinction. Ecology 96:16–23. https://doi.org/10.1890/14-1361.1
Acknowledgements
We thank the members of The Boreal Toad Recovery Team for their support of this project and for their assistance with environmental and swab sample collection. We thank K. Davenport, The Bailey Lab, The Huyvaert Lab, The Grant Lab, W. C. Funk (Colorado State University), E. Muths (USGS), L. Belden, and one anonymous reviewer for providing valuable comments on earlier drafts of this manuscript. This is contribution number 650 of the USGS Amphibian Research and Monitoring Initiative (ARMI).
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BAM, KPH, and LLB conceived of the study, BAM conducted the statistical analyses, and BAM, KPH, and LLB wrote the manuscript.
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Communicated by Lisa Belden.
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Mosher, B.A., Huyvaert, K.P. & Bailey, L.L. Beyond the swab: ecosystem sampling to understand the persistence of an amphibian pathogen. Oecologia 188, 319–330 (2018). https://doi.org/10.1007/s00442-018-4167-6
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DOI: https://doi.org/10.1007/s00442-018-4167-6