Heterogeneous occupancy and density estimates of the pathogenic fungus Batrachochytrium dendrobatidis in waters of North America

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Chestnut, Tara ^a,b   Anderson, Chauncey ^b   Popa, Radu ^c   Blaustein, Andrew R ^a   Voytek, Mary ^d   Olson, Deanna H ^e   Kirshtein, Julie ^b  

^a OREGON STATE UNIVERSITY   (United States)

^b U S GEOLOGICAL SURVEY   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d NASA HEADQUARTERS   (United States)

^e PACIFIC NORTHWEST RESEARCH STATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SURFACE WATER;

AMPHIBIA; AQUATIC SPECIES; ARTICLE; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGUS IDENTIFICATION; GENETIC HETEROGENEITY; NONHUMAN; NORTH AMERICA; POPULATION DENSITY; PROBABILITY; SEASONAL VARIATION; SPECIES HABITAT; WATER ANALYSIS; WATER QUALITY; WATER SAMPLING; WETLAND; ZOOSPORE; ANIMAL; BIODIVERSITY; BIOLOGICAL MODEL; CHYTRIDIOMYCETES; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYSIOLOGY; UNITED STATES;

BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI;

AMPHIBIANS; ANIMALS; BIODIVERSITY; CHYTRIDIOMYCOTA; MODELS, BIOLOGICAL; NORTH AMERICA; OREGON; POPULATION DENSITY; WATER MICROBIOLOGY; WETLANDS;

EID: 84907143479     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106790     Document Type: Article

References (114)

1. Vaughn CC (2010) Biodiversity losses and ecosystem function in freshwaters: emerging conclusions and research directions. BioScience 60: 25-35.
2. Pereira HM, Leadley PW, Proença V, Alkemade R, Scharlemann JPW, et al. (2010) Scenarios for global biodiversity in the 21st century. Science 330: 1496-1501. doi: 10.1126/science.1196624
3. Jones JP, Collen BEN, Atkinson G, Baxter PW, Bubb P, et al. (2011) The why, what, and how of global biodiversity indicators beyond the 2010 target. Conserv Biol 25: 450-457.
4. Mora C, Sale PF (2011) Ongoing global biodiversity loss and the need to move beyond protected areas: a review of the technical and practical shortcomings of protected areas on land and sea. Mar Ecol Prog Ser 434: 251-266. doi: 10.3354/meps09214
5. Hooper DU, Adair EC, Cardinale BJ, Byrnes JE, Hungate BA, et al. (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486: 105-108.
6. Krauss J, Bommarco R, Guardiola M, Heikkinen RK, Helm A, et al. (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13: 597-605. doi: 10.1111/j.1461-0248.2010.01457.x
7. Hoffmann M, Hilton-Taylor C, Angulo A, Böhm M, Brooks TM, et al. (2010) The impact of conservation on the status of the world's vertebrates. Science 330: 1503-1509. doi: 10.1126/science.1194442
8. Seto KC, Güneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. P Natl Acad Sci USA 109: 16083-16088. doi: 10.1073/pnas.1211658109
9. Chapin III FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, et al. (2000) Consequences of changing biodiversity. Nature 405: 234-242. doi: 10.1038/35012241
10. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52: 273-288. doi: 10.1016/j.ecolecon.2004.10.002
11. Relyea RA (2005) The impact of insecticides and herbicides on the biodiversity and productivity of aquatic communities. Ecol Appl 15: 618-627.
12. Relyea RA (2009) A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159: 363-376.
13. Clements WH, Rohr JR (2009) Community responses to contaminants: Using basic ecological principles to predict ecotoxicological effects. Environ Toxicol Chem 28: 1789-1800. doi: 10.1897/09-140.1
14. Lawler JJ, Shafer SL, White D, Kareiva P, Maurer EP, et al. (2009) Projected climate-induced faunal change in the Western Hemisphere. Ecology 90: 588-597.
15. Dawson TP, Jackson ST, House JI, Prentice IC, Mace GM (2011) Beyond predictions: biodiversity conservation in a changing climate. Science 332: 53-58. doi: 10.1126/science.1200303
16. Mantyka-pringle CS, Martin TG, Rhodes JR (2012) Interactions between climate and habitat loss effects on biodiversity: a systematic review and metaanalysis. Glob Change Biol 18: 1239-1252. doi: 10.1111/j.1365-2486.2011.02593.x
17. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287: 443-449.
18. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, et al. (2008) Global trends in emerging infectious diseases. Nature 451: 990-993. doi: 10.1038/nature06536
19. McCallum ML (2007) Amphibian decline or extinction? Current declines dwarf background extinction rate. J Herpetol 41: 483-491.
20. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, et al. (2004) Status and trends of amphibian declines and Extinctions worldwide. Science 306: 1783-1786. doi: 10.1126/science.1103538
21. Adams MJ, Miller DAW, Muths E, Corn PS, Grant EHC, et al. (2013) Trends in amphibian occupancy in the United States. PLoS ONE 8: e64347. doi: 10.1371/journal.pone.0064347
22. Blaustein AR, Grant Hokit D, O'Hara RK, Holt RA (1994) Pathogenic fungus contributes to amphibian losses in the Pacific Northwest. Biol Conserv 67: 251-254.
23. Romansic JM, Johnson PTJ, Searle CL, Johnson JE, Tunstall TS, et al. (2011) Individual and combined effects of multiple pathogens on Pacific treefrogs. Oecologia 166: 1029-1041. doi: 10.1007/s00442-011-1932-1
24. Ault KK, Johnson JE, Pinkart HC, Wagner RS (2012) Genetic comparison of water molds from embryos of amphibians Rana cascadae, Bufo boreas and Pseudacris regilla. Dis Aquat Org 99: 127-137. doi: 10.3354/dao02456
25. Bradford DF (1991) Mass mortality and extinction in a high-elevation population of Rana muscosa. J Herpetol 25: 174-177. doi: 10.2307/1564645
26. Mao J, Green D., Fellers G, Chinchar V (1999) Molecular characterization of iridoviruses isolated from sympatric amphibians and fish. Virus Res 63: 45-52. doi: 10.1016/S0168-1702(99)00057-X
27. Chinchar VG (2002) Ranaviruses (family Iridoviridae): emerging cold-blooded killers. Arch Virol 147: 447-470. doi: 10.1007/s007050200000
28. Jancovich JK, Davidson EW, Parameswaran N, Mao J, Chinchar VG, et al. (2005) Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Mol Ecol 14: 213-224. doi: 10.1111/j.1365-294X.2004.02387.x
29. Chinchar VG, Robert J, Storfer AT (2011) Ecology of viruses infecting ectothermic vertebrates-the impact of ranavirus infections on amphibians. In: Hurst CJ, editor, Studies in viral ecology: animal host systems, volume 2. Hoboken, NJ: John Wiley & Sons. pp. 231-259.
30. Davis AK, Yabsley MJ, Keel MK, Maerz JC (2007) Discovery of a novel alveolate pathogen affecting southern leopard frogs in Georgia: description of the disease and host effects. EcoHealth 4: 310-317. doi: 10.1007/s10393-007-0115-3
31. Jones MEB, Armin AG, Rothermel BB, Pessier AP (2012) Granulomatous myositis associated with a novel alveolate pathogen in an adult southern leopard frog (Lithobates sphenocephalus). Dis Aquat Org 102: 163-167. doi: 10.3354/dao02539
32. Johnson PT, Lunde KB, Thurman EM, Ritchie EG, Wray SN, et al. (2002) Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecol Monogr 72: 151-168.
33. Blaustein AR, Johnson PTJ (2003) The complexity of deformed amphibians. Front Ecol Environ 1: 87-94.
34. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008) Evaluating the links between climate, disease spread, and amphibian declines. P Natl Acad Sci USA 105: 17436-17441.
35. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. P Natl Acad Sci USA 107: 9689-9694.
36. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, et al. (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLoS ONE 8: e56802.
37. Shearer C, Descals E, Kohlmeyer B, Kohlmeyer J, Marvanová L, et al. (2007) Fungal biodiversity in aquatic habitats. Biodiv Conserv 16: 49-67. doi: 10.1007/s10531-006-9120-z
38. Adl SM, Simpson AGB, Lane CE, Lukes J, Bass D, et al. (2012) The revised classification of Eukaryotes. J Eukaryot Microbiol 59: 429-493. doi: 10.1111/j.1550-7408.2012.00644.x
39. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, et al. (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111: 509-547. doi: 10.1016/j.mycres.2007.03.004
40. Gleason FH, Küpper FC, Amon JP, Picard K, Gachon CM, et al. (2011) Zoosporic true fungi in marine ecosystems: a review. Mar Freshwater Res 62: 383-393.
41. Ibelings B, De Bruin A, Kagami M, Van Donk E (2007) Diatom blooms, chytrid epidemics and the evolutionary. J Phycol 43: 2-2.
42. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, et al. (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818-822. doi: 10.1038/nature05110
43. Kagami M, Van Donk E, de Bruin A, Rijkeboer M, Ibelings BW (2004) Daphnia can protect diatoms from fungal parasitism. Limnol Oceanogr 49: 680-685.
44. Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen et sp nov, a chytrid pathogenic to amphibians. Mycologia 91: 219-227. doi: 10.2307/3761366
45. Martel A, Sluijs AS der, Blooi M, Bert W, Ducatelle R, et al. (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. PNAS: 201307356. doi: 10.1073/pnas.1307356110
46. Berger L, Hyatt AD, Speare R, Longcore JE (2005) Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Org 68: 51-63. doi: 10.3354/dao068051
47. Rosenblum EB, Voyles J, Poorten TJ, Stajich JE (2010) The deadly chytrid fungus: a story of an emerging pathogen. PLoS Pathog 6: e1000550. doi: 10.1371/journal.ppat.1000550
48. Kirshtein JD, Anderson CW, Wood JS, Longcore JE, Voytek MA (2007) Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. Dis Aquat Org 77: 11.
49. Walker SF, Baldi Salas M, Jenkins D, Garner TW, Cunningham AA, et al. (2007) Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. Dis Aquat Org 77: 105.
50. Hyman OJ, Collins JP (2011) Evaluation of a filtration-based method for detecting Batrachochytrium dendrobatidis in natural bodies of water. Dis Aquat Org 97: 185-195. doi: http://dx.doi.org.ezproxy.proxy.library.oregonstate.edu/10.3354/dao02423
51. Johnson ML, Speare R (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg Infect Dis 9: 922.
52. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96: 9-15. doi: 10.2307/3761981
53. Voyles J, Johnson LR, Briggs CJ, Cashins SD, Alford RA, et al. (2012) Temperature alters reproductive life history patterns in Batrachochytrium dendrobatidis, a lethal pathogen associated with the global loss of amphibians. Ecol Evol 2: 2241-2249. doi: 10.1002/ece3.334
54. Cheng TL, Rovito SM, Wake DB, Vredenburg VT (2011) From the cover: Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. P Natl Acad Sci USA 108: 9502-9507. doi: 10.1073/pnas.1105538108
55. Mitchell KM, Churcher TS, Garner TW., Fisher MC (2008) Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. P Roy Soc B-Biol Sci 275: 329-334. doi: 10.1098/rspb.2007.1356
56. Schmidt BR (2010) Estimating the impact of disease in species threatened by amphibian chytrid fungus: comment on Murray et al. Conserv Biol 24: 897-899. doi: 10.1111/j.1523-1739.2010.01507.x
57. Woodhams DC, Alford RA, Briggs CJ, Johnson M, Rollins-Smith LA (2008) Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology 89: 1627-1639.
58. Berger L, Speare R, Hines HB, Marantelli G, Hyatt AD, et al. (2004) Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Aust Vet J 82: 434-439.
59. Drew A, Allen EJ, Allen LJS (2006) Analysis of climatic and geographic factors affecting the presence of chytridiomycosis in Australia. Dis Aquat Org 68: 245.
60. Raffel TR, Michel PJ, Sites EW, Rohr JR (2010) What drives chytrid infections in newt populations? Associations with substrate, temperature, and shade. EcoHealth 7: 526-536. doi: http://dx.doi.org.ezproxy.proxy.library. oregonstate.edu/10.1007/s10393-010-0358-2
61. Rohr JR, Raffel TR (2010) Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. P Natl Acad Sci USA 107: 8269-8274.
62. Seimon TA, Seimon A, Daszak P, Halloy SR p., Schloegel LM, et al. (2007) Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Glob Change Biol 13: 288-299. doi: 10.1111/j.1365-2486.2006.01278.x
63. 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.
64. Retallick RW, McCallum H, Speare R (2004) Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol 2: e351.
65. Kriger KM, Hero J-M (2006) Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. J Zool: 060905012106004-? doi: 10.1111/j.1469-7998.2006.00220.x
66. Pearl CA, Bull EL, Green DE, Bowerman J, Adams MJ, et al. (2007) Occurrence of the amphibian pathogen Batrachochytrium dendrobatidis in the Pacific Northwest. J Herpetol 41: 145-149.
67. 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: e16708.
68. Gervasi SS, Urbina J, Hua J, Chestnut T, Relyea RA, et al. (2013) Experimental evidence for American Bullfrog (Lithobates catesbeianus) susceptibility to chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth: 1-6. doi: 10.1007/s10393-013-0832-8
69. MacKenzie DI, Nichols JD, Lachman GB, Droege S, Andrew Royle J, et al. (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83: 2248-2255.
70. Thompson KG (2007) Use of site occupancy models to estimate prevalence of Myxobolus cerebralis infection in trout. J Aquat Anim Health 19: 8-13. doi: 10.1577/H06-016.1
71. Adams MJ, Chelgren ND, Reinitz D, Cole RA, Rachowicz LJ, et al. (2010) Using occupancy models to understand the distribution of an amphibian pathogen, Batrachochytrium dendrobatidis. Ecol Appl 20: 289-302.
72. McClintock BT, Nichols JD, Bailey LL, MacKenzie DI, Kendall WL, et al. (2010) Seeking a second opinion: uncertainty in disease ecology. Ecol Lett 13: 659-674. doi: 10.1111/j.1461-0248.2010.01472.x
73. U.S. Geological Survey (2010) National field manual for the collection of waterquality data: U.S. Geological Survey Techniques of Water-Resources Investigations, book 9, chaps. A1-A9. Available: http://pubs.water.usgs.gov/twri9A US Department of the Interior, US Geological Survey.
74. Ficetola GF, Miaud C, Pompanon F, Taberlet P (2008) Species detection using environmental DNA from water samples. Biol Lett 4: 423-425.
75. Goldberg CS, Pilliod DS, Arkle RS, Waits LP (2011) Molecular detection of vertebrates in stream water: a demonstration using Rocky Mountain Tailed Frogs and Idaho Giant Salamanders. PLoS ONE 6: e22746. doi: 10.1371/journal.pone.0022746
76. Simon D, Moline J, Helms G, Friedl T, Bhattacharya D (2005) Divergent histories of rDNA group I introns in the lichen family Physciaceae. J Mol Evol 60: 434-446. doi: 10.1007/s00239-004-0152-2
77. Daly C, Halbleib M, Smith JI, Gibson WP, Doggett MK, et al. (2008) Physiographically sensitive mapping of climatological temperature and precipitation across the conterminous United States. Int J Climatol 28: 2031-2064.
78. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available: http://www.R-project.org/
79. Dobson A (2004) Population dynamics of pathogens with multiple host species. Am Nat 164: S64-S78.
80. 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. Method Ecol Evol 4: 646-653. doi: 10.1111/2041-210X.12052
81. Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5: 597-608.
82. Bancroft BA, Han BA, Searle CL, Biga LM, Olson DH, et al. (2011) Specieslevel correlates of susceptibility to the pathogenic amphibian fungus Batrachochytrium dendrobatidis in the United States. Biodivers Conserv 20: 1911-1920. doi: 10.1007/s10531-011-0066-4
83. Gervasi S, Gondhalekar C, Olson DH, Blaustein AR (2013) Host identity matters in the amphibian-Batrachochytrium dendrobatidis system: fine-scale patterns of variation in responses to a multi-host pathogen. PLoS ONE 8. doi: 10.1371/journal.pone.0054490
84. Welsh HH, Lind AJ (2002) Multiscale habitat relationships of stream amphibians in the Klamath-Siskiyou region of California and Oregon. J Wildlife Manage 66: 581. doi: 10.2307/3803126
85. Euliss NH, LaBaugh JW, Fredrickson LH, Mushet DM, Laubhan MK, et al. (2004) The wetland continuum: A conceptual framework for interpreting biological studies. Wetlands 24: 448-458. doi: 10.1672/0277-5212(2004)024[0448: TWCACF]2.0.CO;2
86. Browne CL (2009) The relationship of amphibian abundance to habitat features across spatial scales in the Boreal Plains. Ecoscience: 209-223. doi: 10.2980/16-2-3220
87. Murray KA, Retallick RWR, Puschendorf R, Skerratt LF, Rosauer D, et al. (2011) Assessing spatial patterns of disease risk to biodiversity: implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis. J Appl Ecol 48: 163-173. doi: 10.1111/j.1365-2664.2010.01890.x
88. Lannoo MJ, Petersen C, Lovich RE, Nanjappa P, Phillips C, et al. (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: e22211. doi: 10.1371/journal.pone.0022211
89. Gsell AS, Domis LNDS, Naus-Wiezer SMH, Helmsing NR, Van Donk E, et al. (2013) Spatiotemporal variation in the distribution of chytrid parasites in diatom host populations. Freshw Biol 58: 523-537. doi: 10.1111/j.1365-2427.2012.02786.x
90. Retallick RW, McCallum H, Speare R (2004) Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol 2: e351.
91. Moss AS, Reddy NS, Dortaj IM, San Francisco MJ (2008) Chemotaxis of the amphibian pathogen Batrachochytrium dendrobatidis and its response to a variety of attractants. Mycologia 100: 1-5.
92. McMahon TA, Brannelly LA, Chatfield MW, Johnson PT, Joseph MB, et al. (2013) Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. P Natl Acad Sci USA 110: 210-215.
93. Shapard EJ, Moss AS, San Francisco MJ (2012) Batrachochytrium dendrobatidis can infect and cause mortality in the nematode Caenorhabditis elegans. Mycopathologia 173: 121-126.
94. Johnson ML, Speare R (2005) Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Dis Aquat Org 65: 181-186. doi: 10.3354/dao065181
95. Garmyn A, Van Rooij P, Pasmans F, Hellebuyck T, Van Den Broeck W, et al. (2012) Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS ONE 7: e35038. doi: 10.1371/journal. pone.0035038
96. Buck JC, Truong L, Blaustein AR (2011) Predation by zooplankton on Batrachochytrium dendrobatidis: biological control of the deadly amphibian chytrid fungus? Biodiv Conserv 20: 3549-3553. doi: 10.1007/s10531-011-0147-4
97. Duffy MA (2009) Staying alive: The post-consumption fate of parasite spores and its implications for disease dynamics. Limnol Oceanogr 54: 770-773. doi: 10.4319/lo.2009.54.3.0770
98. Searle CL, Mendelson JR, Green LE, Duffy MA (2013) Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles. Ecol Evol 3: 4129-4138. doi: 10.1002/ece3.777
99. Blaustein AR, Gervasi SS, Johnson PT, Hoverman JT, Belden LK, et al. (2012) Ecophysiology meets conservation: understanding the role of disease in amphibian population declines. Philos T Roy Soc B 367: 1688-1707.
100. Hayes MP, Jennings MR (1986) Decline of ranid frog species in western North America: are Bullfrogs (Rana catesbeiana) responsible? J Herpetol 20: 490. doi: 10.2307/1564246
101. Reddy KR (1981) Diel variations of certain physico-chemical parameters of water in selected aquatic systems. Hydrobiologia 85: 201-207. doi: 10.1007/BF00017610
102. Maberly SC. (1996) Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshwater Biol 35: 579-598. doi: 10.1111/j.1365-2427.1996.tb01770.x
103. Halstead BG, Tash JC (1982) Unusual diel pHs in water as related to aquatic vegetation. Hydrobiologia 96: 217-224. doi: 10.1007/BF00010613
104. Litaor IM, Thurman EM (1988) Acid neutralizing processes in an alpine watershed front range, Colorado, U.S.A.-1: Buffering capacity of dissolved organic carbon in soil solutions. Appl Geochem 3: 645-652. doi: 10.1016/0883-2927(88)90096-0
105. Herlihy AT, Kaufmann PR, Mitch ME (1991) Stream chemistry in the eastern United States: 2. Current sources of acidity in acidic and low acid-neutralizing capacity streams. Water Resour Res 27: 629-642. doi: 10.1029/90WR02768
106. Chamier A-C (1987) Effect of pH on microbial degradation of leaf litter in seven streams of the English Lake District. Oecologia 71: 491-500. doi: 10.1007/BF00379287
107. Gleason FH, Kagami M, Lefevre E, Sime-Ngando T (2008) The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol Rev 22: 17-25. doi: 10.1016/j.fbr.2008.02.001
108. MacKenzie DI, Royle JA, Brown JA, Nichols JD (2004) Occupancy estimation and modeling for rare and elusive populations. In: Thompson WL, editor. Sampling rare or elusive species. Washington, DC: Island Press. pp. 149-172.
109. Hines JE, Nichols JD, Royle JA, MacKenzie DI, Gopalaswamy AM, et al. (2010) Tigers on trails: occupancy modeling for cluster sampling. Ecol Appl 20: 1456-1466.
110. Royle JA, Link WA (2006) Generalized site occupancy models allowing for false positive and false negative errors. Ecology 87: 835-841.
111. Miller DA, Nichols JD, McClintock BT, Grant EHC, Bailey LL, et al. (2011) Improving occupancy estimation when two types of observational error occur: non-detection and species misidentification. Ecology 92: 1422-1428. doi: 10.1890/10-1396.1
112. Miller DAW, Nichols JD, Gude JA, Rich LN, Podruzny KM, et al. (2013) Determining occurrence dynamics when false positives occur: estimating the range dynamics of wolves from public survey data. PLoS ONE 8: e65808. doi: 10.1371/journal.pone.0065808
113. Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71: 1599-1608.
114. Blaustein AR, Han B, Fasy B, Romansic J, Scheessele EA, et al. (2004) Variable breeding phenology affects the exposure of amphibian embryos to ultraviolet radiation and optical characteristics of natural waters protect amphibians from UV-B in the US Pacific Northwest: Comment. Ecology 85: 1747-1754.