Skip to main content

Advertisement

SpringerLink
Log in

Effects of urbanization on the occurrence of Batrachochytrium dendrobatidis: do urban environments provide refuge from the amphibian chytrid fungus?

  • Published:
Urban Ecosystems Aims and scope Submit manuscript

Abstract

Batrachochytrium dendrobatidis (Bd) is a widespread pathogenic fungus that is known to cause the disease, chytridiomycosis, which can be lethal to many amphibians. We compared occurrence rates on spring peepers (Pseudacris crucifer) in urban and forested breeding sites in eastern Texas, USA. All study sites were at approximately the same latitude and altitude, and samples were collected at the same time of year to isolate differences in Bd infection rates between habitat types. We found significant differences (p < 0.001) in the occurrence of Bd between habitats; with dramatically lower rates of occurrence at urban sites (19.5 %), compared to forested sites (62.9 %). The exact reason for the observed differences in the occurrence of Bd is not known, however, we suspect that warmer temperatures or lower population densities and lower species richness at urban sites all could play a role in our results. Our findings suggest that urban environments may provide a refuge for some amphibians from the pathogen.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied ecology. Ann Rev Ecol Syst 30:133–165

    Article  Google Scholar 

  • Becker CG, Zamudio KR (2011) Tropical amphibian populations experience higher disease risk in natural habitats. Proc Natl Acad Sci U S A 108:9893–9898

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Becker CG, Rodriguez D, Longo AV, Talaba AL, Zamudio KR (2012) Disease risk in temperate amphibian populations is higher at closed-canopy sites. PLoS ONE 7(10):e48205. doi:10.1371/journal.pone.0048205

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berger L, Speare R, Daszak PD, Green ED, 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 declines in the rain forests of Australia and Central America. Proc Natl Acad Sci U S A 95:9031–9036

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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. Aust Vet J 82:31–36

    Google Scholar 

  • Berger L, Speare R, Marantelli G, Skerratt LF (2009) A zoospore inhibition technique to evaluate the activity of antifungal compounds against Batrachochytrium dendrobatidis and successful treatment of experimentally infected green tree frogs (Litoria caerulea) by fluconazole and benzalkonium chloride. Res Vet Sci 87:106–110

    Article  CAS  PubMed  Google Scholar 

  • Brem FMR, Lips KR (2008) Batrachochytrium dendrobatidis infection patterns among Panamanian amphibian species, habitats, and elevations during epizootic and enzootic stages. Dis Aquat Organ 81:189–202

    Article  PubMed  Google Scholar 

  • Chatfield MWH, Richards-Zawacki CL (2011) Elevated temperature as a treatment for Batrachochytrium dendrobatidis infection in captive frogs. Dis Aquat Organ 94:235–238

    Article  PubMed  Google Scholar 

  • Collins JP, Storfer A (2003) Global amphibian decline: sorting the hypotheses. Divers Distrib 9:89–98

    Article  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9:141–150

    Article  Google Scholar 

  • Faulkner S (2004) Urbanization impacts on the structure and function of forested wetlands. Urban Ecosyst 7:89–106

    Article  Google Scholar 

  • Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and chytridiomycosis in space, time, and host. Annu Rev Microbiol 63:291–310

    Article  CAS  PubMed  Google Scholar 

  • Hamer AJ, McDonnell MJ (2008) Amphibian ecology and conservation in the urbanizing world: a review. Biol Conserv 141:2432–2449

    Article  Google Scholar 

  • Hoffmann M et al (2010) The impact of conservation on the status of the World’s vertebrates. Science 330:1503–1509

    Article  CAS  PubMed  Google Scholar 

  • Hossack BR, Lowe HW, Ware JL, Corn PS (2013) Disease in a dynamic landscape: host behavior and wildfire reduce amphibian chytrid infection. Biol Conserv 157:293–299

    Article  Google Scholar 

  • Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755

    Article  CAS  PubMed  Google Scholar 

  • Johnson ML, Berger L, Philips L, Speare R (2003) Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Organ 57:255–260

    Article  CAS  PubMed  Google Scholar 

  • Karraker NE, Ruthig GR (2009) Effect of road deicing salt on the susceptibility of amphibian embryos to infection to water molds. Environ Res 109:40–45

    Article  CAS  PubMed  Google Scholar 

  • Kilpatrick AM, Briggs CJ, Daszak P (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 25:109–118

    Article  PubMed  Google Scholar 

  • Kim HH (1992) Urban heat island. Int J Remote Sens 13:2319–2336

    Article  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kriger KM, Hero JM (2008) Altitudinal distribution of chytrid (Batrachochytrium dendrobatidis) infection in subtropical Australian frogs. Aust Ecol 33:1022–1032

    Article  Google Scholar 

  • Kriger KM, Pereoglou F, Hero JM (2007) Latitudinal variation in the prevalence and intensity of chytrid (Batrachochytrium dendrobatidis) infection in eastern Australia. Conserv Biol 5:1280–1290

    Article  Google Scholar 

  • Lane A, Burgin S (2008) Comparison of frog assemblages between urban and non-urban habitats in the upper Blue Mountains of Australia. Freshw Biol 53:2484–2493

    Article  Google Scholar 

  • Lannoo MJ, Petersen C, Lovich RE, Nanjappa P, Philliips C, Mitchell JC, Macallister 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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. Proc Natl Acad Sci U S A 103:3165–3170

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen et sp nov, a chytrid pathogenic to amphibians. Mycologia 91:219–227

    Article  Google Scholar 

  • McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890

    Article  Google Scholar 

  • McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176

    Article  Google Scholar 

  • Murphy PJ, St-Hilaire S, Bruer S, Corn PS, Peterson CR (2009) Distribution and pathogenicity of Batrachochytrium dendrobatidis in boreal toads from the Grand Teton area of western Wyoming. EcoHealth 6:109–120

    Article  PubMed  Google Scholar 

  • Murphy PJ, St-Hilaire S, Corn PS (2011) Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads. Dis Aquat Organ 95:31–42

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Naeem S, Thompson LJ, Lawler SP, Lawton JH, Woodfin RM (1994) Declining biodiversity can alter the performance of ecosystems. Nature 368:734–737

    Article  Google Scholar 

  • Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Garner TWJ, Weaver G, Group TBM, Fisher MC (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS ONE 8(2):e56802. doi:10.1371/journal.pone.0056802

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Parris MJ, Baud DR (2004) Interactive effects of a heavy metal and chytridiomycosis on gray treefrog larvae (Hyla chrysoscelis). Copeia 2004:344–350

    Article  Google Scholar 

  • Pauza MD, Driessen MM, Skerratt LF (2010) Distribution and risk factors for spread of amphibian chytrid fungus Batrachochytrium dendrobatidis in the Tasmanian Wilderness World Heritage Area, Australia. Dis Aquat Organ 92:193–199

    Article  PubMed  Google Scholar 

  • Pechmann JHK, Wilbur HM (1994) Putting declining amphibian populations in perspective: natural fluctuations and human impacts. Herpetologica 50:65–84

    Google Scholar 

  • Rachowics LJ, Briggs CJ (2007) Quantifying the disease transmission function: effects of density on Batrachochytrium dendrobatidis transmission in the mountain yellow-legged frog, Rana mucosa. J Anim Ecol 76:711–721

    Article  Google Scholar 

  • Raffel TR, Michel PJ, Sites EW, Rhor JR (2010) What drives chytrid infections in newt populations? Association with substrate, temperature, and shade. EcoHealth 7:526–536

    Article  PubMed  Google Scholar 

  • Rodder D, Veith M, Lotters S (2008) Environmental gradients explaining the prevalence and intensity of infection with the amphibian chytrid fungus: the host’s perspective. Anim Conserv 11:513–517

    Article  Google Scholar 

  • Saenz D, Fitzgerald LA, Baum KA, Conner RN (2006) Abiotic correlates of anuran calling phenology: the importance of rain, temperature, and season. Herpetol Monogr 20:64–82

    Article  Google Scholar 

  • Saenz D, Kavanaugh BT, Kwiatkowski MA (2010) Batrachochytrium dendrobatidis detected in amphibians from National Forests in Eastern Texas, USA. Herpetol Rev 41:47–49

    Google Scholar 

  • Sanso D, Hecnar SJ (2006) Effects of de-icing salt (NaCl) on larval wood frogs (Rana silvatica). Environ Pollut 140:247–256

    Article  Google Scholar 

  • Schlaepfer MA, Sredl MJ, Rosen PC, Ryan MJ (2007) High prevalence of Batrachochytrium dendrobatidis in wild populations of lowland leopard frogs Rana yavapaiensis in Arizona. EcoHealth 4:421–427

    Article  Google Scholar 

  • Schloegel LM, Daszak P, Cunningham AA, Speare R, Hill B (2010) Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the World Organization for Animal Health (OIE): an assessment. Dis Aquat Organ. doi:10.3354/dao02140

    PubMed  Google Scholar 

  • Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott DA, Hines HB, Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–136

    Article  Google Scholar 

  • Soule ME (1991) Conservation: tactics for a constant crisis. Science 253:744–750

    Article  CAS  PubMed  Google Scholar 

  • Stockwell MP, Clulow J, Mahony MJ (2012) Sodium chloride inhibits the growth and infective capacity of the amphibian chytrid fungus and increases host survival rates. PLoS ONE 7(5):e36942. doi:10.1371/journal.pone.0036942

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  CAS  PubMed  Google Scholar 

  • Van Sluys M, Hero J-M (2009) How does chytrid infection vary among habitats? The case of Litoria wilcoxii (Anura, Hylidae) in SE Queensland, Australia. EcoHealth 6:576–583

    Article  PubMed  Google Scholar 

  • Wake DB (1991) Declining amphibian populations. Science 253:860

    Article  CAS  PubMed  Google Scholar 

  • Whitfield SM, Kerby J, Gentry LR, Donnelly MA (2012) Temporal variation in infection prevalence by the amphibian chytrid fungus in three species of frogs at La Selva, Costa Rica. Biotropica 44:779–784

    Article  Google Scholar 

  • Woodhams DC, Alford RA (2005) Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queensland. Conserv Biol 19:1449–1459

    Article  Google Scholar 

  • Woodhams DC, Geiger CC, Reinert LK, Rollins-Smith LA, Lam B, Harris RN, Briggs CJ, Vredenburg VT, Voyles J (2012) Treatment of amphibians infected with chytrid fungus: learning from failed trials with itraconozole, antimicrobial peptides, bacteria, and heat therapy. Dis Aquat Organ 98:11–25

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Nancy Koerth, Dede Olson, and Cory Adams for constructive comments on an earlier draft of this manuscript.

Author information

Authors and Affiliations

  1. Southern Research Station, Forest Service, U. S. Department of Agriculture, 506 Hayter Street, Nacogdoches, TX, 75965-3556, USA

    Daniel Saenz

  2. Department of Science and Mathematics, Angelina College, Lufkin, TX, USA

    Taylor L. Hall

  3. Department of Biology, Stephen F. Austin State University, 1936 North Street, Nacogdoches, TX, 75962-3050, USA

    Matthew A. Kwiatkowski

Authors
  1. Daniel Saenz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Taylor L. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew A. Kwiatkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel Saenz.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saenz, D., Hall, T.L. & Kwiatkowski, M.A. Effects of urbanization on the occurrence of Batrachochytrium dendrobatidis: do urban environments provide refuge from the amphibian chytrid fungus?. Urban Ecosyst 18, 333–340 (2015). https://doi.org/10.1007/s11252-014-0398-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11252-014-0398-4

Keywords

Search

Navigation