EcoHealth

, Volume 13, Issue 2, pp 368–382 | Cite as

Prevalence and Seasonality of the Amphibian Chytrid Fungus Batrachochytrium dendrobatidis Along Widely Separated Longitudes Across the United States

  • Christopher E. Petersen
  • Robert E. Lovich
  • Christopher A. Phillips
  • Michael J. Dreslik
  • Michael J. Lannoo
Original Contribution
First Online:
Received:
Revised:
Accepted:

Abstract

The chytrid fungus Batrachochytrium dendrobatidis (Bd) has been implicated in amphibian declines on almost all continents. We report on prevalence and intensity of Bd in the United States amphibian populations across three longitudinally separated north-to-south transects conducted at 15 Department of Defense installations during two sampling periods (late-spring/early summer and mid to late summer). Such a standardized approach minimizes the effects of sampling and analytical bias, as well as human disturbance (by sampling restricted military bases), and therefore permits a cleaner interpretation of environmental variables known to affect chytrid dynamics such as season, temperature, rainfall, latitude, and longitude. Our prevalence of positive samples was 20.4% (137/670), and our mean intensity was 3.21 zoospore equivalents (SE = 1.03; range 0.001–103.59). Of the 28 amphibian species sampled, 15 tested positive. Three sites had no evidence of Bd infection; across the remaining 12 Bd-positive sites, neither infection prevalence nor intensity varied systematically. We found a more complicated pattern of Bd prevalence than anticipated. Early season samples showed no trend associated with increasing temperature and precipitation and decreasing (more southerly) latitudes; while in late season samples, the proportion of infected individuals decreased with increasing temperature and precipitation and decreasing latitudes. A similar pattern held for the east–west gradient, with the highest prevalence associated with more easterly/recently warmer sites in the early season then shifting to more westerly/recently cooler sites in the later season. Bd intensity across bases and sampling periods was comparatively low. Some of the trends in our data have been seen in previous studies, and our results offer further continental-level Bd sampling over which more concentrated local sampling efforts can be overlaid.

Keywords

amphibians chytrid fungus department of defense Batrachochytrium dendrobatidis 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

Support for this project (10-426) came from the Department of Defense Legacy Resource Management Program https://www.dodlegacy.org.legacy/index.aspx. The authors thank Chris Bucciantini, David Davis, Jackie Hancock, Ethan Kessler, John Maile, Jeff Phillips, and Dan Wylie for collecting specimens. For providing access to their installations and support in the field, we thank David Beckmann, Fort McCoy; Jay Brezinka, Camp Ripley; Chris Bucciantini, Naval Air Station Meridian; Angy Chambers, Cape Canaveral Air Force Station; Liz Clark, Fort Hunter Liggett; David Davis, Shaw Air Force Base; Chad Garber, Marine Corps Base, Camp Lejeune; Jackie Hancock, Fort Hunter Liggett; Jim Heide, Naval Support Activity Mid-South; Andrew Irvine, Marine Corps Mountain Warfare Training Center; Jim Lynch, Fort Lewis; Jeff Mach, Camp Rilea Armed Forces Training Facility; John Maile, Camp Ripley; John Miller, Jim Creek Naval Radio Station; Kari Moore, Naval Computer and Telecommunications Station, Cutler; Cindy Nolan, Scott Air Force Base; John Richardson, Fort Lewis; Bill Rogers, Marine Corps Base, Camp Lejeune; Kristen Sharp, Fort Dix; Roger Smith, Fort Dix; Linda Wagoner, Jim Creek Naval Radio Station; Rob Williamson, Naval Support Activity Mid-South.

References

  1. Adams MJ, Galvan S, Reinitz D, Cole RA, Payre S, Hahr M, Govindarajulu P (2007) Incidence of the fungus Batrachochytrium dendrobatidis in amphibian populations along the Northwest Coast of North America. Herpetological Review 38:430–431.Google Scholar
  2. Bates D, Maechler M, Bolker BM, Walker S (2015) lme4: Linear mixed-effects models using Eigen and S4_. R package version 1.1-8. http://CRAN.R-project.org/package=lme4.
  3. Becker CG, Zamudio KR (2011) Tropical amphibian populations experience higher disease risk in natural habitats. Proceedings of the National Academy of Science 108(24):9893–9898.CrossRefGoogle Scholar
  4. Becker CG, Rodriguez D, Toledo LF, Longo AV, Lambertini C, Corrêa DT, Leite DS, Haddad CF, Zamudio KR (2014) Partitioning the net effect of host diversity on an emerging amphibian pathogen. Proceedings of the Royal Society B: Biological Sciences 281(1795):20141796.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (1998) Chytridiomycosis causes amphibian mortality associated with population decline in the Rain Forests of Australia and Central America. Proceedings of the National Academy of Science 95:9031–9036.CrossRefGoogle Scholar
  6. Berger L, Speare R, Hines HB, Marantelli G, Hyatt AD, McDonald KR, Skerratt LF, Olsen V, Clarke JM, Gillespie G, Mahony M, Sheppard N, Williams C, Tyler MJ (2004) Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal 82:434–439.CrossRefPubMedGoogle Scholar
  7. Bletz MC, Harris RN (2013) Occurrence of Batrachochytrium dendrobatidis in Notophthalmus viridescens in Northwestern Virginia, USA. Herpetological Review 44:257–259.Google Scholar
  8. Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian sample using real-time Taqman PCR assay. Disease of Aquatic Organisms 60:141–148.CrossRefGoogle Scholar
  9. Briggs CJ, Knapp RA, Vredenburg VT (2010) Enzootic and epizootic dynamics of the chytrid fungus pathogen of amphibians. Proceedings of the National Academy of Sciences 107:9695–9700.CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002) Model selection and multimodal inference: A practical information theoretic approach. 2nd ed. Springer, New York, New York.Google Scholar
  11. Chestnut T, Johnson JE, Wagner RS (2008) Results of amphibian chytrid (Batrachochytrium dendrobatidis) sampling in Denali National Park, Alaska, USA. Herpetological Review 39:202–204.Google Scholar
  12. Davidson SR, Chambers DL (2011) Occurrence of Batrachochytrium dendrodatidis in amphibians of Wise County, Virginia, USA. Herpetological Review 42:214–216.Google Scholar
  13. DiRosa I, Simoncelli F, Fagotti A, Pascolini R (2007) The proximate cause of amphibian declines? Nature 447: E4–E5.CrossRefGoogle Scholar
  14. Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Ann Rev Microbiol 63: 291–310.CrossRefPubMedGoogle Scholar
  15. Fox J (2003) Effect displays in R for generalized linear models. Journal of Statistical Software. 8:1–27.CrossRefGoogle Scholar
  16. Gaertner JP, Brown DJ, Mendoza JA, Forstner MRJ, Bonner T, Hahn D (2012) Geographic variation in Batrachochytrium dendrobatidis occurrence among populations of Acris crepitans blanchardi in Texas, USA. Herpetological Review 43:274–278.Google Scholar
  17. Gaertner JP, Forstner MRJ, O’Donnell L, Hahn D (2009) Detection of Batrachochytrium dendrobatidis in endemic salamander species from Central Texas. EcoHealth 6:20–26.CrossRefPubMedGoogle Scholar
  18. Groner ML, Relyea RA (2010) Batrachochytrium dendrobatidis is present in northwest Pennsylvania, USA, with high prevalence in Notophthalmus viridescens. Herpetological Review 41:462–465.Google Scholar
  19. Hasken J, Newby JL, Grelle AM, Boling J, Estes J, Garey LK, Wilmes T, McKee R, Gomez D, Jackson T, Gibson N, Davinroy E, Montgomery DE, Kelrick MJ (2009) Evaluation of chytrid infection level in a newly discovered population of Anaxyrus boreas in the Rio Grande National Forest, Colorado, USA. Herpetological Review 40(4):426–428.Google Scholar
  20. Huang R, Wilson LA (2013) Batrachochytrium dendrobatidis in amphibians of the Piedmont and Blue Ridge provinces in northern Georgia, USA. Herpetological Review 44:95–98.Google Scholar
  21. Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, Obendorf D, Dalton A, Krieger K, Hero M, Hines H, Phillott R, Campbell R, Marantelli G, Gleason F, Colling A (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 73:175–192.CrossRefPubMedGoogle Scholar
  22. IUCN Red List 2014. http://www.iucnredlist.org/initiatives/amphibians/analysis. Accessed 24 March 2014
  23. Johnson ML, Speare R (2005) Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Diseases of Aquatic Organisms 65:181–186.CrossRefPubMedGoogle Scholar
  24. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993.CrossRefPubMedGoogle Scholar
  25. Kinney VC, Heemeyer JL, Pessier AP, Lannoo MJ (2011) Seasonal pattern of Batrachochytrium dendrobatidis infection and mortality in Lithobates areolatus: Affirmation of Vredenburg’s “10,000 zoospore rule.” PLoS ONE 6(3): e16708. doi: 10.1371/journal.pone.0016708.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kriger KM, Pereoglou F, Hero J-M. 2007. Latitudinal variation in the prevalence and intensity of chytrid (Batrachochytrium dendrobatidis) infection in eastern Australia. Conservation Biology 21:1280–1290.CrossRefPubMedGoogle Scholar
  27. Krynak TJ, Robison TL, Scott JJ (2012) Detection of Batrachochytrium dendrobatidis in amphibian populations of northeast Ohio. Herpetological Review 43:87–89.Google Scholar
  28. Lannoo, MJ (ed.). 2005. Amphibian declines: The conservation status of United States species. University of California Press, Berkeley.Google Scholar
  29. Lannoo MJ, Petersen C, Lovich RE, Nanjappa P, Phillips C, Mitchell, J, McAllister, I (2011) Do frogs get their kicks on Route 66? Continental U.S. transect reveals spatial and temporal patterns of Batrachochytrium dendrobatidis infection. PLoS ONE 6(7):e22211. doi: 10.1371/journal.pone.0022211.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessier AP, Collins JP (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Ecology 103:3165–3170.Google Scholar
  31. Liu X, Rohr JR, Li Y (2013) Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proceedings of the Royal Society B: Biological Sciences 280(1753):20122506.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Longcore J, Pessier A, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227.CrossRefGoogle Scholar
  33. Longo AV, Burrowes PA, Joglar RL (2010) Seasonality of Batrachochytrium dendrobatidis infection in direct-developing frogs suggests a mechanism for persistence. Diseases of Aquatic Organisms 92:253–260.CrossRefPubMedGoogle Scholar
  34. Mazerolle MJ (2015) AICcmodavg: Model selection and multimodal inference based on (Q)AIC(c). R package version 2.0-3. http://CRAN.R-project.org/package=AICcmodavg
  35. Murray KA, Skerratt LF, Speare R, McCallum H (2009) Impact and dynamics of disease in species threatened by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Conservation Biology 32:1242–1252.CrossRefGoogle Scholar
  36. Murray KA, Retallick RWR, Puschendorf R, Skerratt LF, Rosauer D, Mccallum HI, Berger L, Speare R, Vanderwal J (2011) Assessing spatial patterns of disease risk to biodiversity: implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis. Journal of Applied Ecology 48(1):163–173.CrossRefGoogle Scholar
  37. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Garner TWJ, Weaver G, The Bd Mapping Group, Fisher MC (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PloS One 8(2):e56802.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ouellet M, Mikaelian I, Pauli BD, Rodrigues J, Green DM 2005. Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology 19:1431–1440.CrossRefGoogle Scholar
  39. Pessier AP, Mendelson III JR (2010) A manual for control of infectious diseases in amphibian survival assurance colonies and reintroduction programs. Proceedings from a Workshop 16–18 February 2009, San Diego Zoo, San Diego, California, USAGoogle Scholar
  40. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15.CrossRefPubMedGoogle Scholar
  41. Rachowicz LJ, Knapp RA, Morgan JAT, Stice MJ, Vredenburg VT, Parker JM, Briggs CJ (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671–1683.CrossRefPubMedGoogle Scholar
  42. Raffel TR, Michel PJ, Sites EW, Rohr JR (2010) What drives chytrid infections in newt populations? Associations with substrate, temperature, and shade. EcoHealth 7(4):526–536.CrossRefPubMedGoogle Scholar
  43. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  44. Retallick RWR, McCallum H, Speare R (2004) Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biology 2:1965–1971.CrossRefGoogle Scholar
  45. Rodriguez EM, Gamble T, Hirt MV, Cotner S (2009) Presence of Batrachochytrium dendrobatidis at the headwaters of the Mississippi River, Itasca State Park, Minnesota, USA. Herpetological Review 40:48–50.PubMedPubMedCentralGoogle Scholar
  46. Rohr JR, Raffel TR (2010) Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Science USA 107(18):8269–8274.CrossRefGoogle Scholar
  47. Rohr JR, Halstead NT, Raffel TR (2011) Modeling the future distribution of the amphibian chytrid fungus: the influence of climate and human-associated factors. Journal of Applied Ecology 48(1):174–176.CrossRefGoogle Scholar
  48. Savage AE, Zamudio KR, Sredl MJ (2011) Disease dynamics vary spatially and temporally in a North American amphibian. Biological Conservation 144(6):1910–1915. doi: 10.1016/j.biocon.2011.03.018.CrossRefGoogle Scholar
  49. Seanz D, Kavanagh BT, Kwiatkowski MA (2010) Batrachochytrium dendrobatidis detected in amphibians from national forests in eastern Texas, USA. Herpetological Review 41:47–49.Google Scholar
  50. 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.CrossRefGoogle Scholar
  51. Stein BA, Scott C, Benton N (2008) Federal Lands and Endangered Species: The Role of Military and Other Federal Lands in Sustaining Biodiversity. BioScience 58:339–347.CrossRefGoogle Scholar
  52. Stevenson LA, Alford RA, Bell SC, Roznik EA, Berger L, et al. (2013) Variation in Thermal Performance of a Widespread Pathogen, the Amphibian Chytrid Fungus Batrachochytrium dendrobatidis. PLoS ONE 8(9):e73830. doi: 10.1371/journal.pone.0073830.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibians and extinctions worldwide. Science 306:1783–1786.CrossRefPubMedGoogle Scholar
  54. Tatarian P, Tatarian G (2010) Chytrid infection of Rana draytonii in the Sierra Nevada, California, USA. Herpetological Review 41:325–327.Google Scholar
  55. Terrell VCK, Engbrecht NJ, Pessier AP, Lannoo MJ (2014) Drought reduces chytrid fungus (Batrachochytrium dendrobatidis) infection intensity and mortality but not prevalence in adult Crawfish Frogs (Lithobates areolatus). Journal of Wildlife Diseases 50:56–62.CrossRefPubMedGoogle Scholar
  56. Tupper TA, Streicher JW, Greenspan SE, Timm BC, Cook RP (2011) Detection of Batrachochytrium dendrobatidis in anurans of Cape Cod National Seashore, Barnstable County, Massachusetts, USA. Herpetological Review 42:62–65.Google Scholar
  57. Venesky MD, Liu X, Sauer EL, Rohr JR (2013) Linking manipulative experiments to field data to test the dilution effect. Journal of Animal Ecology, 83(3):557–565.CrossRefPubMedGoogle Scholar
  58. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Science. 107(21):9689-94. doi: 10.1073/pnas.0914111107.CrossRefGoogle Scholar
  59. Woodhams DC, Alford RA, Marantelli G (2003) Emerging disease of amphibians cured by elevated body temperature. Diseases of Aquatic Organisms 55:65–67.CrossRefPubMedGoogle Scholar
  60. Woodhams DC, Alford RA, Maraentelli G (2005) Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queensland. Conservation Biology 19:1449–1459.CrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health (outside the USA) 2016

Authors and Affiliations

  • Christopher E. Petersen
    • 1
  • Robert E. Lovich
    • 2
  • Christopher A. Phillips
    • 3
  • Michael J. Dreslik
    • 3
  • Michael J. Lannoo
    • 4
  1. 1.Naval Facilities Engineering Command AtlanticNorfolkUSA
  2. 2.Naval Facilities Engineering Command SouthwestSan DiegoUSA
  3. 3.Illinois Natural History Survey, Prairie Research InstituteUniversity of Illinois at Urbana-ChampaignChampaignUSA
  4. 4.Indiana University School of MedicineTerre HauteUSA

Personalised recommendations