Experimental evidence for a cost of resistance to the fungal pathogen, Batrachochytrium dendrobatidis, for the palmate newt, Lissotriton helveticus

BMC Ecology

Volumn 13, Issue , 2013, Pages

  Cheatsazan, Hamed ^a   de Almedia, Ana P Lugon Gavinho ^b   Russell, Andrew F ^a,c   Bonneaud, Camille ^a,c  

^a USR 2936   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Body condition; Chytridiomycosis; Cost of immunity; Emerging infectious disease; Resistance; Secondary sexual traits

Indexed keywords

AMPHIBIAN; BODY CONDITION; DISEASE RESISTANCE; EXPERIMENTAL STUDY; FUNGAL DISEASE; INFECTIOUS DISEASE; INOCULATION; MORBIDITY; MORTALITY; PATHOGEN; RECRUITMENT (POPULATION DYNAMICS); REPRODUCTIVE SUCCESS;

AMPHIBIA; BATRACHOCHYTRIUM DENDROBATIDIS; SALAMANDRIDAE; TRITURUS HELVETICUS;

ANIMAL; BREEDING; CHYTRIDIOMYCETES; FEMALE; IMMUNOLOGY; MALE; MICROBIOLOGY; MYCOSIS; PATHOGENICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; REPRODUCTION; SALAMANDRIDAE; VETERINARY; VIRULENCE; ANIMAL DISEASE; ARTICLE;

ANIMALS; BREEDING; CHYTRIDIOMYCOTA; FEMALE; MALE; MYCOSES; REPRODUCTION; SALAMANDRIDAE; VIRULENCE;

EID: 84880335326     PISSN: None     EISSN: 14726785     Source Type: Journal    
DOI: 10.1186/1472-6785-13-27     Document Type: Article

References (84)

1. Kilpatrick AM, Briggs CJ, Daszak P. The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 2010, 25(2):109-118. 10.1016/j.tree.2009.07.011, 19836101.
2. Bonaccorso E, Guayasamin JM, Mendez D, Speare R. Chytridiomycosis as a possible cause of population declines in Atelopus cruciger (Anura: Bufonidae). Herp Rev 2003, 34:331-334.
3. Green DE, Sherman CK. Diagnostic histological findings in Yosemite toads (Bufo canorus) from a die-off in the. J Herpetol 1970, 2001:92-103.
4. Kriger KM, Hero JM, Ashton KJ. Cost efficiency in the detection of chytridiomycosis using PCR assay. Dis Aquat Organ 2006, 71(2):149-154.
5. Voyles J, Rosenblum EB, Berger L. Interactions between Batrachochytrium dendrobatidis and its amphibian hosts: a review of pathogenesis and immunity. Microb Infect 2011, 13(2):25-32.
6. Gervasi S, Gondhalekar C, Olson D, Blaustein A. Host Identity Matters in the Amphibian-Batrachochytrium dendrobatidis System: Fine-Scale Patterns of Variation in Responses to a Multi-Host Pathogen. PLoS One 2013, 8(1):e54490. 10.1371/journal.pone.0054490, 3554766, 23382904.
7. Retallick RWR, McCallum H, Speare R. Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol 2004, 2(11):e351. 10.1371/journal.pbio.0020351, 521176, 15502873.
8. Schloegel LM, Hero JM, Berger L, Speare R, McDonald K, Daszak P. The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case of extinction by infection in a free-ranging wildlife species?. Ecohealth 2006, 3(1):35-40.
9. Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, Hines HB, Kenyon N. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 2007, 4(2):125-134.
10. Daszak P, Strieby A, Cunningham AA, Longcore JE, Brown CC, Porter D. Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herp J 2004, 14:201-208.
11. Davidson EW, Parris M, Collins JP, Longcore JE, Pessier AP, Brunner J. Pathogenicity and transmission of chytridiomycosis in tiger salamanders (Ambystoma tigrinum). Copeia 2003, 2003(3):601-607.
12. Reeder NMM, Pessier AP, Vredenburg VT. A Reservoir Species for the Emerging Amphibian Pathogen Batrachochytrium dendrobatidis Thrives in a Landscape Decimated by Disease. PLoS One 2012, 7(3):e33567. 10.1371/journal.pone.0033567, 3299797, 22428071.
13. Rollins-Smith LA. The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochim Biophys Acta Biomembranes 2009, 1788(8):1593-1599.
14. Berger L, Hyatt AD, Speare R, Longcore JE. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Organ 2005, 68(1):51-63.
15. Nichols DK, Lamirande EW, Pessier AP, Longcore JE. Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs. J Wildl Dis 2001, 37(1):1-11.
16. Pessier AP, Nichols DK, Longcore JE, Fuller MS. Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). J Vet Diagn Invest 1999, 11(2):194-199. 10.1177/104063879901100219, 10098698.
17. Lochmiller RL, Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity?. Oikos 2000, 88(1):87-98.
18. Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 1996, 11(8):317-321. 10.1016/0169-5347(96)10039-2, 21237861.
19. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G. Assessing the cost of mounting an immune response. Am Nat 2003, 161(3):367-379. 10.1086/346134, 12703483.
20. Moret Y, Schmid-Hempel P. Survival for immunity: the price of immune system activation for bumblebee workers. Science 2000, 290(5494):1166-1168. 10.1126/science.290.5494.1166, 11073456.
21. Råberg L, Nilsson J, Ilmonen P, Stjernman M, Hasselquist D. The cost of an immune response: vaccination reduces parental effort. Ecol Lett 2000, 3(5):382-386.
22. Bonneaud C, Balenger SL, Hill GE, Russell AF. Experimental evidence for distinct costs of pathogenesis and immunity against a natural pathogen in a wild bird. Mol Ecol 2012, 21(19):4787-4796. 10.1111/j.1365-294X.2012.05736.x, 22924889.
23. Hornef MW, Wick MJ, Rhen M, Normark S. Bacterial strategies for overcoming host innate and adaptive immune responses. Nat Immunol 2002, 3(11):1033-1040. 10.1038/ni1102-1033, 12407412.
24. Casadevall A, Pirofski L. The damage-response framework of microbial pathogenesis. Nat Rev Microbiol 2003, 1(1):17-24. 10.1038/nrmicro732, 15040176.
25. Davidson C, Benard MF, Shaffer HB, Parker JM, O'Leary C, Conlon JM, Rollins-Smith LA. Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environ Sci Technol 2007, 41(5):1771-1776. 10.1021/es0611947, 17396672.
26. Garner TWJ, Walker SF, Bosch J, Leech S, Marcus Rowcliffe J, Cunningham AA, Fisher MC. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 2009, 118(5):783-791.
27. Venesky MD, Parris MJ, Altig R. Pathogenecity of Batrachochytrium dendrobatidis in larval Ambystomatid Salamanders. Herp Cons Biol 2010, 5(2):174-182.
28. Venesky MD, Parris MJ, Storfer A. Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. Ecohealth 2009, 6(4):565-575. 10.1007/s10393-009-0272-7, 20135192.
29. Burrowes PA, Longo AV, Rodríguez CA. Potential fitness cost of Batrachochytrium dendrobatidis in eleutherodactylus coqui, and comments on environment-related risk of infection. Herpetotropicos 2007, 4(2):51-57.
30. Richards-Zawacki C. Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proc R Soc Lond, Ser B: Biol Sci 2010, 277(1681):519-528.
31. Secondi J, Hinot E, Djalout Z, Sourice S, Jadas-Hécart A. Realistic nitrate concentration alters the expression of sexual traits and olfactory male attractiveness in newts. Funct Ecol 2009, 23(4):800-808.
32. Nöllert A, Nöllert C. Guide des amphibiens d'Europe 2003, Paris: Delachaux et Niestlé.
33. Griffiths RA, Mylotte VJ. Observations on the development of the secondary sexual characters of male newts. Triturus vulgaris and T. helveticus. J Herpetol 1988, 22(4):476-480.
34. Baker JMR. Body condition and tail height in great crested newts, Triturus cristatus. Anim Behav 1992, 43:157-159.
35. Green AJ. Large male crests, an honest indicator of condition, are preferred by female smooth newts, Triturus vulgaris(Salamandridae) at the spermatophore transfer stage. Anim Behav 1991, 41(2):367-369.
36. Cornuau JH, Rat M, Schmeller DS, Loyau A. Multiple signals in the palmate newt: ornaments help when courting. Behav Ecol Sociobiol 2012, 66:1045-1055.
37. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Garner TWJ, Weaver G, Fisher MC, The Bd Mapping G Mapping the Global Emergence of Batrachochytrium dendrobatidis, the Amphibian Chytrid Fungus. PLoS ONE 2013, 8(2):e56802. 10.1371/journal.pone.0056802, 3584086, 23463502, The Bd Mapping G.
38. Wood LR, Griffiths RA, Schley L. Amphibian chytridiomycosis in Luxembourg. Bull Soc Nat Luxemb 2009, 110:109-114.
39. Johnson ML, Speare R. Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerging Infect Dis 2003, 9(8):922. 3020615, 12967488.
40. Longcore JE. Recognizing, isolating, and culturing Batrachochytrium dendrobatidis from amphibians. Proceedings of "Getting the Jump! on Amphibian Diseases Conference/Workshop 2000, 52-54. Queensland, Australia: James Cook University, August.
41. Boyle DG, Boyle DB, Olsen V, Morgan JA, Hyatt AD. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Organ 2004, 60(2):141-148.
42. Bielby J, Bovero S, Sotgiu G, Tessa G, Favelli M, Angelini C, Doglio S, Clare F, Gazzaniga E, Lapietra F, et al. Fatal chytridiomycosis in the tyrrhenian painted frog. Ecohealth 2009, 6(1):27-32. 10.1007/s10393-009-0232-2, 19418096.
43. Walker SF, Salas MB, Jenkins D, Garner TW, Cunningham AA, Hyatt AD, Bosch J, Fisher MC. Environmental detection of Batrachochytrium dendrobatidis in a temperate climate. Dis Aquat Organ 2007, 77(2):105-112.
44. Kriger KM, Hines HB, Hyatt AD, Boyle DG, Hero JM. Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR. Dis Aquat Organ 2006, 71(2):141-148.
45. Berger L, Longcore JE, Speare R, Hyatt AD, Skerratt LF. Amphibian Biology, Volume 8 2009, Australia: Surrey Beatty & Sons.
46. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, et al. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 2009, 326(5952):582-585. 10.1126/science.1176765, 19900897.
47. Fisher MC, Garner TW, Walker SF. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol 2009, 63:291-310. 10.1146/annurev.micro.091208.073435, 19575560.
48. Rollins-Smith LA, Conlon JM. Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev Comp Immunol 2005, 29(7):589-598. 10.1016/j.dci.2004.11.004, 15784290.
49. Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, Flaherty DC, Lam BA, Woodhams DC, Briggs CJ, Vredenburg VT, et al. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 2009, 3(7):818-824. 10.1038/ismej.2009.27, 19322245.
50. Harris RN, Lauer A, Simon MA, Banning JL, Alford RA. Addition of antifungal skin bacteria to salamanders ameliorates the effects of chytridiomycosis. Dis Aquat Organ 2009, 83(1):11-16.
51. Lam BA, Walke JB, Vredenburg VT, Harris RN. Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biol Conserv 2010, 143(2):529-531.
52. Ramsey JP, Reinert LK, Harper LK, Woodhams DC, Rollins-Smith LA. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog. Xenopus laevis. Infect Immun 2010, 78(9):3981. 10.1128/IAI.00402-10, 2937463, 20584973.
53. Rollins-Smith LA, Ramsey J, Pask J, Reinert L, Woodhams D. Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr Comp Biol 2011, 51(4):552-562. 10.1093/icb/icr095, 21816807.
54. Rollins-Smith LA, Ramsey JP, Reinert LK, Woodhams DC, Livo LJ, Carey C. Immune defenses of Xenopus laevis against Batrachochytrium dendrobatidis. Front Biosci (Schol Ed) 2009, 1:68-91.
55. Rowley J, Alford R. Hot bodies protect amphibians against chytrid infection in nature. Sci Rep 2013, 3:1515. 3604863, 23519020.
56. Venesky MD, Wilcoxen TE, Rensel MA, Rollins-Smith L, Kerby JL, Parris MJ. Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 2012, 169(1):23-31. 10.1007/s00442-011-2171-1, 22038058.
57. Woodhams DC, Bosch J, Briggs CJ, Cashins S, Davis LR, Lauer A, Muths E, Puschendorf R, Schmidt BR, Sheafor B. Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis. Frontiers in Zoology 2011, 8(1):8. 10.1186/1742-9994-8-8, 3098159, 21496358.
58. Little TJ, Killick SC. Evidence for a cost of immunity when the crustacean Daphnia magna is exposed to the bacterial pathogen Pasteuria ramosa. J Anim Ecol 2007, 76(6):1202-1207. 10.1111/j.1365-2656.2007.01290.x, 17922716.
59. Martin LB, Scheuerlein A, Wikelski M. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs?. Proc R Soc Lond Ser B: Biol Sci 2003, 270(1511):153-158.
60. Murray MJ, Murray AB. Anorexia of infection as a mechanism of host defense. Am J Clin Nutrit 1979, 32(3):593-596.
61. Kriger K, Pereoglou F, Hero J-M. Latitudinal variation in the prevalence and intensity of chytrid (Batrachochytrium dendrobatidis) infection in eastern Australia. Conservation biology: the journal of the Society for Conservation Biology 2007, 21(5):1280-1290.
62. Woodhams D, Bigler L, Marschang R. Tolerance of fungal infection in European water frogs exposed to Batrachochytrium dendrobatidis after experimental reduction of innate immune defenses. BMC Vet Res 2012, 8:197. 10.1186/1746-6148-8-197, 3485127, 23088169.
63. Kikuyama S, Yazawa T, Abe S, Yamamoto K, Iwata T, Hoshi K, Hasunuma I, Mosconi G, Polzonetti-Magni A. Newt prolactin and its involvement in reproduction. Can J Physiol Pharm 2000, 78(12):984-993.
64. Mazzi V, Vellano C. Prolactin and reproduction. Hormones and reproduction in fishes, amphibians, and reptiles 1987, 87-115. New York and London: Plenum Press, Norris DO, Jones RE, vol. 1.
65. Tassava RA, KUENZLI C. The effects of Prolactin and Thyroxine on tailk fin height, habitat chioce, and forelimbe regeneration in the adult newt (Notophthalmus viridescens). Ohio J Sci 1979, 79(2):32-37.
66. Miele R, Ponti D, Boman H, Barra D, Simmaco M. Molecular cloning of a bombinin gene from Bombina orientalis: detection of NF-kappaB and NF-IL6 binding sites in its promoter. FEBS Lett 1998, 431(1):23-28. 10.1016/S0014-5793(98)00718-2, 9684858.
67. Rollins-Smith L. Neuroendocrine-immune system interactions in amphibians: implications for understanding global amphibian declines. Immunol Res 2001, 23(2-3):273-280.
68. Kapcala L, Chautard T, Eskay R. The protective role of the hypothalamic-pituitary-adrenal axis against lethality produced by immune, infectious, and inflammatory stress. Ann N Y Acad Sci 1995, 771:419-437. 10.1111/j.1749-6632.1995.tb44699.x, 8597419.
69. Gabor C, Fisher M, Bosch J. A Non-Invasive Stress Assay Shows That Tadpole Populations Infected with Batrachochytrium dendrobatidis Have Elevated Corticosterone Levels. PLoS One 2013, 8(2):e56054. 10.1371/journal.pone.0056054, 3572145, 23418508.
70. Kloas W, Hanke W. Neurohypophysial hormones and steroidogenesis in the interrenals of Xenopus laevis. Gen Comp Endocrinol 1990, 80(2):321-330. 10.1016/0016-6480(90)90176-M, 1963609.
71. Malagón M, Ruiz-Navarro A, Torronteras R, Gracia-Navarro F. Effects of ovine CRF on amphibian pituitary ACTH and TSH cells in vivo: a quantitative ultrastructural study. Gen Comp Endocrinol 1991, 83(3):487-497. 10.1016/0016-6480(91)90157-2, 1657693.
72. Brown SC, Stocking Brown P, Yamamoto K, Matsuda K, Kikuyama S. Amphibian prolactins: Activity in the eft skin transepithelial potential bioassay. Gen Comp Endocrinol 1991, 82(1):1-7. 10.1016/0016-6480(91)90289-I, 1908395.
73. Singhas CA, Dent JN. Hormonal control of the tail fin and of the nuptial pads in the male red-spotted newt. Gen Comp Endocrinol 1975, 26(3):382-393.
74. Toyoda F, Tanaka S, Matsuda K, Kikuyama S. Hormonal control of response to and secretion of sex attractants in Japanese newts. Physiol Behav 1994, 55(3):569-576. 10.1016/0031-9384(94)90118-X, 8190778.
75. Sever DM, Staub NL. Hormones, Sex Accessory Structures, and Secondary Sexual Characteristics in Amphibians. Hormones and Reproduction in Vertebrates Volume 2: Amphibians 2010, Maryland Heights, Missouri: Elsevier Inc, In Norris DOe, vol. 2.
76. May S, Zeisset I, Beebee T, J. C Larval fitness and immunogenetic diversity in chytrid-infected and uninfected natterjack toad (Bufo calamita) populations. Conserv Genet 2011, 12:805-811. J. C.
77. Harrison JD, Gittins SP, Slater FM. The breeding migration of Smooth and Palmate newts (Triturus vulgaris and T. helveticus) at a pond in mid Wales. J Zool 1983, 199(2):249-258.
78. Verrell PA, Halliday TR, Griffiths ML. The annual reproductive cycle of the smooth newt (Triturus vulgaris) in England. J Zool 1986, 210(1):101-119.
79. Wells KD. The ecology and behavior of amphibians 2007, Chicago: University of Chicago Press.
80. Jehle R, Arntzen JW. Post-breeding migrations of newts (Triturus cristatus and T. marmoratus) with contrasting ecological requirements. J Zool 2000, 251(3):297-306.
81. Bell G. The life of the smooth newt (Triturus vulgaris) after metamorphosis. Ecol Monogr 1977, 47(3):279-299.
82. Bonneaud C, Balenger SL, Russell AF, Zhang J, Hill GE, Edwards SV. Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proc Natl Acad Sci USA 2011, 108(19):7866-7871. 10.1073/pnas.1018580108, 3093480, 21525409.
83. Eraud C, Duriez O, Chastel O, Faivre B. The energetic cost of humoral immunity in the Collared Dove, Streptopelia decaocto: is the magnitude sufficient to force energy-based trade-offs?. Funct Ecol 2005, 19(1):110-118.
84. Bosch J, Carrascal LM, Duran L, Walker S, Fisher MC. Climate change and outbreaks of amphibian chytridiomycosis in a montane area of Central Spain; is there a link?. Proc Biol Sci 2007, 274(1607):253-260. 10.1098/rspb.2006.3713, 1685858, 17148254.