Individual and combined effects of multiple pathogens on Pacific treefrogs

Oecologia

Volumn 166, Issue 4, 2011, Pages 1029-1041

  Romansic, John M ^a   Johnson, Pieter T J ^b   Searle, Catherine L ^a   Johnson, James E ^c   Tunstall, Tate S ^d   Han, Barbara A ^e   Rohr, Jason R ^f   Blaustein, Andrew R ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c CENTRAL WASHINGTON UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF GEORGIA   (United States)

^f UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Amphibian decline; Coinfection; Concomitant infections; Emerging infectious disease; Polyparasitism

Indexed keywords

BIOLOGICAL DEVELOPMENT; DISEASE PREVALENCE; EXTINCTION; FLATWORM; FROG; FUNGUS; HOST-PATHOGEN INTERACTION; INFECTIOUS DISEASE; INFECTIVITY; MORTALITY; PATHOGEN; POPULATION DECLINE; SYNERGISM;

ACHLYA; ANIMAL; ANIMAL DISEASE; ARTICLE; CHYTRIDIOMYCETES; CONGENITAL DISORDER; FROGS AND TOADS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; LARVA; METAMORPHOSIS; MICROBIOLOGY; MYCOSIS; PARASITOLOGY; PHYSIOLOGY; TREMATODE; TREMATODIASIS;

ACHLYA; ANIMALS; ANURA; CHYTRIDIOMYCOTA; CONGENITAL ABNORMALITIES; HOST-PATHOGEN INTERACTIONS; LARVA; METAMORPHOSIS, BIOLOGICAL; MYCOSES; TREMATODA; TREMATODE INFECTIONS;

ACHLYA; ACHLYA FLAGELLATA; AMPHIBIA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; HYLA; OOMYCETES; PSEUDACRIS REGILLA; RIBEIROIA; TREMATODA;

EID: 79960338873     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-011-1932-1     Document Type: Article

References (90)

1. Becker MH, Harris RN (2010) Cutaneous bacteria of the redback salamander prevent morbidity associated with a lethal disease. PLoS One 5: e10957.
2. Belden LB, Harris RN (2007) Infectious diseases in wildlife: the community ecology context. Front Ecol Environ 5: 533-539.
3. Bentwich Z, Kalinkovich A, Weisman Z, Borkow G, Beyers N, Beyers (1999) Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunol Today 20: 485-487.
4. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AH, 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 USA 95: 9031-9036.
5. Bisht GS, Bisht D, Joshi C, Khulbe RD (1996) Potential threat to reservoir fishery by fungi in Kumaun Himalaya, India. Curr Sci India 71: 720-723.
6. Blaustein AR, Johnson PTJ (2003) The complexity of deformed amphibians. Front Ecol Environ 1: 87-94.
7. Blaustein AR, Hatch A, Belden LK, Wildy EL (2001) Influence of abiotic and biotic factors on amphibians in ephemeral ponds with special reference to long-toed salamanders (Amybstoma macrodactylum). Isr J Zool 47: 333-346.
8. Blaustein AR, Romansic JM, Scheesele EA, Han BA, Pessier AP, Longcore LE (2005) Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conserv Biol 19: 1460-1468.
9. Bowerman J, Johnson PTJ (2003) Timing of trematode-related malformations in Oregon spotted frogs and Pacific treefrogs. Northwest Nat 82: 142-145.
10. 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 Org 60: 133-139.
11. Briggs CJ (1993) Competition among parasitoid species on a stage-structured host and its effect on host suppression. Am Nat 141: 372-397.
12. Crump ML (1989a) Effect of habitat drying on developmental time and size at metamorphosis in Hyla pseudopuma. Copeia 1989: 794-797.
13. Crump ML (1989b) Life history consequences of feeding versus non-feeding in a facultatively non-feeding toad larva. Oecologia 78: 486-489.
14. Cunningham AA, Langton TES, Bennet PM, Lewin JF, Drury SEN, Gough RE, Macgregor SK (1996) Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Philos Trans R Soc Lond B 351: 1539-1557.
15. Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9: 141-150.
16. Davidson EW, Parris M, Collins JP, Longcore JE, Pessier AP, Brunner J (2003) Pathogenicity and transmission of chytridiomycosis in tiger salamanders (Ambystoma tigrinum). Copeia 2003: 601-607.
17. Duffus ALJ (2009) Chytrid blinders: what other disease risks to amphibians are we missing? EcoHealth 6: 335-339.
18. Firth D (1993) Bias reduction in maximum likelihood estimates. Biometrika 80: 27-38.
19. Fisher MC, Garner TWJ, Walker SF (2009) Emergence of Batrachochytrium and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol 63: 291-310.
20. Garcia TS, Romansic JM, Blaustein AR (2006) Survival of three species of anuran metamorphs exposed to UV-B radiation and the pathogenic fungus Batrachochytrium dendrobatadis. Dis Aquat Org 72: 163-169.
21. Garner TWJ, Walker S, Bosch J, Leech S, Rowcliffe JM, Cunningham AA, Fisher MC (2009) Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118: 783-791.
22. Gomez-Mestre I, Touchon JC, Warkentin KM (2006) Amphibian embryo and parental defenses and a larval predator reduce egg mortality from water mold. Ecology 87: 2570-2581.
23. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183-190.
24. Green DE, Converse KA (2005) Diseases of amphibian eggs and embryos. In: Majumdar S, Huffman J, Brenner F, Panah A (eds) Wildlife diseases: landscape epidemiology, spatial distribution and utilization of remote sensing technology. Pennsylvania Academy of Science, Easton, pp 62-71.
25. Green DE, Converse KA, Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001. Ann NY Acad Sci 969: 323-339.
26. Greer AL, Berrill M, Wilson PJ (2005) Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada. Dis Aquat Org 67: 9-14.
27. Heinze G (2006) A comparative investigation of methods for logistic regression with separated or nearly separated data. Stat Med 25: 4216-4226.
28. Johnson TW Jr (1956) The Genus Achlya: morphology and taxonomy. University of Michigan Press, Ann Arbor.
29. Johnson PTJ, Buller I (2010) Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions. doi: 10. 1890/10-0570. 1.
30. Johnson PTJ, Hartson RB (2009) All hosts are not equal: explaining differential patterns of malformations in an amphibian community. J Anim Ecol 78: 191-201.
31. Johnson PTJ, Lunde KB (2005) Parasite infection and limb malformations: a growing problem in amphibian conservation. In: Lanoo M (ed) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, pp 124-138.
32. Johnson PTJ, Lunde KB, Ritchie EG, Launer AE (1999) The effect of trematode infection on amphibian limb development and survivorship. Science 284: 802-804.
33. Johnson PTJ, Lunde KB, Haight RW, Bowerman J, Blaustein AR (2001) Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Can J Zool 79: 370-379.
34. Johnson PTJ, Lunde KB, Thurman EM, Ritchie EG, Wray SN, Sutherland DR, Kapfer JM, Frest TJ, Bowerman J, Blaustein AR (2002a) Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecol Monogr 72: 151-168.
35. Johnson TW Jr, Seymour RL, Padgett, DE (2002b) Biology and systematics of the Saprolegniaceae. On-line publication: http://dl. uncw. edu/digilib/biology/fungi/taxonomy%20and%20systematics/padgett%20book/.
36. Johnson PTJ, Lunde KB, Zelmer DA, Werner JK (2003) Limb deformities as an emerging parasitic disease in amphibians: evidence from museum specimens and resurvey data. Conserv Biol 17: 1724-1737.
37. Johnson PTJ, Sutherland DR, Kinsella JM, Lunde KB (2004) Review of the trematode genus Ribeiroia (Psilostomidae): ecology, life history and pathogenesis with special emphasis on the amphibian malformation problem. Adv Parasit 57: 191-253.
38. Johnson PTJ, Preu ER, Sutherland DR, Romansic J, Han B, Blaustein AR (2006) Adding infection to injury: synergistic effects of predation and parasitism on salamander limb malformations. Ecology 87: 2227-2235.
39. Johnson PTJ, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, Sutherland DR, Carpenter SR (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. Proc Natl Acad Sci USA 104: 15781-15786.
40. Johnson PTJ, Hartson RB, Larson DJ, Sutherland DR (2008) Diversity and disease: community structure drives parasite transmission and host fitness. Ecol Lett 11: 1017-1026.
41. Jolles AE, Ezenwa VO, Etienne RS, Turner WC, Olff H (2008) Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89: 2239-2250.
42. Joly DO, Messier F (2005) The effect of bovine tuberculosis and brucellosis on reproduction and survival of wood bison in Wood Buffalo National Park. J Anim Ecol 74: 543-551.
43. Kerby JL, Storfer A (2009) Combined effects of atrazine and chlorpyrifos on susceptibility of the tiger salamander to Ambystoma tigrinum virus. Ecohealth 6: 91-98.
44. Khulbe RD (1992) Watermolds and their activity in Kumaun Himalaya, India. Water Sci Technol 26: 2595-2598.
45. Khulbe RD (1994) A world monograph of parasitic watermolds. Shree Almora, Almora.
46. Khulbe RD, Joshi C, Bisht GS (1995) Fungal diseases of fish in Nanak Sagar. Mycopathologia 130: 71-74.
47. Kiesecker JM (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc Natl Acad Sci USA 99: 9900-9904.
48. Kiesecker JM, Blaustein AR (1995) Synergism between UV-B radiation and a pathogen magnifies amphibian embryo mortality in nature. Proc Natl Acad Sci USA 92: 11049-11052.
49. Kiesecker JM, Skelly DK, Beard KH, Pressier E (1999) Behavioral reduction of infection risk. Proc Natl Acad Sci USA 96: 9165-9168.
50. Kilpatrick MA, Briggs CL, Daszak P (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 25: 109-118.
51. Knapp RA, Morgan JAT (2006) Tadpole mouthpart depigmentation as an accurate indicator of chytridiomycosis, an emerging disease of amphibians. Copeia 2006: 188-197.
52. Lam BA, Walke JB, Vredenburg VT, Harris RN (2010) Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biol Conserv 143: 529-531.
53. Munson L, Terio KA, Kock R, Mlengeya T, Roelke ME, Dubovi E, Summers B, Sinclair ARE, Packer C (2008) Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. PLoS One 3: e2545.
54. Newman RA (1988) Adaptive plasticity in development of Scaphiopus couchii tadpoles in desert ponds. Evolution 42: 774-783.
55. Nieto NC, Camann MA, Foley JE, Reiss JO (2007) Disease associated with integumentary and cloacal parasites in tadpoles of northern red-legged frog Rana aurora aurora. Dis Aquat Org 78: 61-71.
56. Noga EJ (1996) Fish disease diagnosis and treatment. Mosby, St. Louis.
57. Parmar MKB, Machin D (1996) Survival analysis: a practical approach. Wiley, New York.
58. Parris MJ, Baud DR (2004) Interactive effect of a heavy metal and chytridiomycosis on gray treefrog larvae (Hyla chrysoscelis). Copeia 2004: 344-350.
59. Parris MJ, Beaudoin JG (2004) Chytridiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia 140: 626-632.
60. Parris MJ, Cornelius TO (2004) Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85: 3385-3395.
61. Pearl CA, Bowerman J, Adams MJ, Chelgren ND (2009) Widespread occurrence of the chytrid fungus Batrachochytrium dendrobatidis on Oregon spotted frogs (Rana pretiosa). Ecohealth 6: 209-218.
62. Petney TN, Andrews RH (1998) Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol 28: 377-393.
63. Petranka JW, Sih A (1986) Environmental instability, competition, and density-dependent growth and survivorship of a stream-dwelling salamander. Ecology 67: 729-736.
64. Pfennig DW (2000) Effect of predator-prey phylogenetic similarity on the fitness consequences of predation: a trade-off between nutrition and disease? Am Nat 155: 335-345.
65. Post G (1987) Mycotic diseases. In: Post GW (ed) Textbook of fish health. T. E. H., Neptune City, pp 73-83.
66. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge.
67. Rachowicz LJ, Vredenburg VT (2004) Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Dis Aquat Org 61: 75-83.
68. 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.
69. Rohr JR, Elskus AA, Sheperd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, Sager T, Sih A, Palmer BD (2004) Multiple stressors and salamanders: effects of an herbicide, food limitation, and hydroperiod. Ecol Appl 14: 1028-1040.
70. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ (2008a) Evaluating the links between climate, disease spread, and amphibian declines. Proc Natl Acad Sci USA 105: 17436-17441.
71. Rohr JR, Raffel TR, Sessions SK, Hudson PJ (2008b) Understanding the net effects of pesticides on amphibian trematode infections. Ecol Appl 18: 1743-1753.
72. Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR (2008c) Agrochemicals increase trematode infections in a declining amphibian species. Nature 7217: 1235-1239.
73. Rohr JR, Swan A, Raffel TR, Hudson PJ (2009) Parasites, info-disruption, and the ecology of fear. Oecologia 159: 447-454.
74. Romansic JM, Diez KA, Higashi EM, Blaustein AR (2006) Effects of nitrate and the pathogenic water mold Saprolegnia on survival of amphibian larvae. Dis Aquat Org 68: 235-243.
75. Romansic JM, Higashi EM, Diez KA, Blaustein AR (2007) Susceptibility of newly-metamorphosed frogs to a pathogenic water mold (Saprolegnia sp.). Herpetol J 17: 161-166.
76. Romansic JM, Diez KA, Higashi EM, Johnson JE, Blaustein AR (2009) Effects of the pathogenic water mold Saprolegnia ferax on survival of amphibian larvae. Dis Aquat Org 83: 187-193.
77. Schotthoefer AM, Koehler AV, Meteyer CU, Cole RA (2003) Influence of Ribeiroia ondatrae (Trematoda: Digenea) infection on limb development and survival of northern leopard frogs (Rana pipiens): effects of host-stage and parasite exposure level. Can J Zool 81: 1144-1153.
78. Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69: 184-192.
79. Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68: 344-350.
80. Sokol A (1984) Plasticity in the fine timing of metamorphosis in tadpoles of the hylid frog, Litoria ewingi. Copeia 1984: 868-873.
81. Srivastava GC, Srivastava RC (1975) Two fungal parasites of the eggs of Channa striatus (Bl.). Curr Sci India 44: 817-818.
82. Srivastava GC, Srivastava RC (1976) Ability of Achlya flagellata Coker parasitising certain fresh water fishes. Geobios (Jodhpur) 3: 139-140.
83. Tiffney WN, Wolf FT (1939) Achlya flagellata as a fish parasite. J Elisha Mitch Sci S 53: 298-300.
84. Touchon JC, Gomez-Mestre I, Warkentin KM (2006) Hatching plasticity in two temperate anurans: responses to a pathogen and predation cues. Can J Zool 84: 556-563.
85. Warburg MR, Lewinson D, Rosenberg M (1994) Ontogenesis of amphibian epidermis. In: Heatwole H, Barthalmus G (eds) Amphibian biology. Volume 1: the integument. Surrey Beatty, Chipping Norton, pp 33-63.
86. Warkentin KM, Currie CR, Rehner SA (2001) Egg-killing fungus induces early hatching of red-eyed treefrog eggs. Ecology 82: 2860-2869.
87. Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128: 319-341.
88. Wilbur HM (1977) Density-dependent aspects of growth and metamorphosis in Bufo americanus. Ecology 58: 196-200.
89. Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182: 1305-1314.
90. Worthylake KM, Hovingh P (1989) Mass mortality of salamanders (Ambystoma tigrinum) by bacteria (Acinetobacter) in an oligotrophic seepage mountain lake. Great Basin Nat 49: 364-372.