Differences in susceptibility to Saprolegnia infections among embryonic stages of two anuran species

Oecologia

Volumn 165, Issue 3, 2011, Pages 819-826

  Fernández Benéitez, María José ^a   Ortiz Santaliestra, Manuel Eloy ^b   Lizana, Miguel ^a   Diéguez Uribeondo, Javier ^c  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^c CSIC   (Spain)

Author keywords

Age related sensitivity; Amphibians; Emergent diseases; Oomycetes; Water moulds

Indexed keywords

DISEASE PREVALENCE; EMBRYONIC DEVELOPMENT; FUNGAL DISEASE; FUNGUS; HOST-PATHOGEN INTERACTION; MORTALITY; TOAD;

SPAIN;

AMPHIBIA; ANURA; BUFO CALAMITA; OOMYCETES; PELOBATES CULTRIPES; SAPROLEGNIA; SAPROLEGNIA DICLINA; SAPROLEGNIA FERAX;

EID: 79951550405     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-010-1889-5     Document Type: Article

References (47)

1. Bangyeekhun E, Pylkkö P, Vennerström P, Kuronen H, Cerenius L (2003) Prevalence of a single fish-pathogenic Saprolegnia sp. clone in Finland and Sweden. Dis Aquat Org 53: 47-53.
2. Banks B, Beebee TJC (1988) Reproductive success of natterjack toads Bufo calamita in two contrasting habitats. J Anim Ecol 57: 472-492.
3. Beattie RC, Aston RJ, Milner AGP (1991) A field study of fertilization and development in the common frog Rana temporaria with particular reference to acidity and temperature. J Appl Ecol 28: 346-357.
4. Blaustein AR, Hokit DG, O'Hara RK, Holt RA (1994) Pathogenic fungus contributes to amphibian losses in the pacific northwest. Biol Conserv 67: 251-254.
5. Bosch J, Martínez-Solano I, García-París M (2001) Evidence of a chytrid fungus infection involved in the decline of common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biol Conserv 97: 331-337.
6. Bragg AN (1958) Parasitism of spadefoot tadpoles by Saprolegnia. Herpetologica 14: 34.
7. Bragg AN (1962) Saprolegnia on tadpoles again in Oklahoma. Southwest Nat 7: 79-80.
8. Cerenius L, Söderhäll K (1985) Repeated zoospore emergence as a possible adaptation to parasitism in Aphanomyces. Exp Mycol 9: 259-263.
9. Daszak P (1998) A new fungal disease associated with amphibian population declines: recent research put into perspective. Herpetol Bull 65: 38-41.
10. Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9(2): 141-150.
11. Densmore CL, Green DV (2007) Diseases of amphibians. ILAR J 48(3): 235-254.
12. Diéguez-Uribeondo J, Cerenius L, Söderhäll K (1994) Repeated zoospore emergence in Saprolegnia parasitica. Mycol Res 98: 810-815.
13. Diéguez-Uribeondo J, Fregeneda-Grandes JM, Cerenius L, Pérez-Iniesta E, Aller-Gancedo JM, Tellería MT, Söderhall K, Martín MP (2007) Re-evaluation of the enigmatic species complex Saprolegnia diclina-Saprolegnia parasitica based on morphological, physiological and molecular data. Fungal Genet Biol 44: 585-601.
14. Du Pasquier L, Schwage J, Flanjnik MF (1989) The immune system of Xenopus. Annu Rev Immunol 7: 251-275.
15. Fernández-Benéitez MJ, Ortiz-Santaliestra ME, Lizana M, Diéguez-Uribeondo J (2008) Saprolegnia diclina: another species responsible for the emergent disease "Saprolegnia infection" in amphibians. FEMS Microbiol Lett 279: 23-29.
16. Ghiasi M, Khosravi AR, Soltani M, Binaii M, Shokri H, Tootian Z, Rostamibashman M, Ebrahimzademousavi H (2010) Characterization of Saprolegnia isolates from Persian sturgeon (Acipencer persicus) eggs based on physiological and molecular data. J Mycol Med 20: 1-7.
17. Gomez-Mestre I, Touchon JC, Saccoccio VL, Warkentin KM (2008) Genetic variation in pathogen-induced early hatching of toad embryos. J Evol Biol 21: 791-800.
18. 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.
19. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16: 183-190.
20. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104(6): 1745-1750.
21. 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.
22. Karraker NE, Ruthig GR (2009) Effect of road deicing salt on the susceptibility of amphibian embryos to infection by water molds. Environ Res 109: 40-45.
23. Kaufman MR, Ikeda Y, Patton C, van Dykhuizen G, Epel D (1998) Bacterial symbionts colonize the accessory nidamental gland of the squid Loligo opalescens via horizontal transmission. Biol Bull 194(1): 36-43.
24. Ke XL, Wang JG, Gu ZM, Li M, Gong XN (2009) Morphological and molecular phylogenetic analysis of two Saprolegnia sp. (Oomycetes) isolated from silver crucian carp and zebra fish. Mycol Res 113: 637-644.
25. 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.
26. Kiesecker JM, Blaustein AR (1999) Pathogen reverses competition between larval amphibians. Ecology 80(7): 2442-2448.
27. Kiesecker JM, Blaustein AR, Miller CL (2001) Transfer of a pathogen from fish to amphibians. Conserv Biol 15: 1064-1070.
28. Lategan MJ, Torpy FR, Gibson LF (2004) Biocontrol of saprolegniosis in silver perch Bidyanus bidyanus (Mitchell) by Aeromonas media strain A199. Aquaculture 235: 77-88.
29. Martín MP, Raidl S, Tellería MT (2004) Molecular analysis confirm the relationship between Stephanospora caroticolor and Lidtneria trachyspora. Mycotaxon 90: 133-140.
30. Ortiz-Santaliestra ME, Marco A, Fernández MJ, Lizana M (2006) Influence of developmental stage on sensitivity to ammonium nitrate of aquatic stages of amphibians. Environ Toxicol Chem 25: 105-111.
31. Ovaska K, Davis TM, Novales I (1997) Hatching success and larval survival of the frogs Hyla regilla and Rana aurora under ambient and artificially enhanced solar ultraviolet radiation. Can J Zool 75: 1081-1088.
32. Poorten TJ, Kuhn RE (2009) Maternal transfer of antibodies to eggs in Xenopus laevis. Dev Comp Immunol 33: 171-175.
33. Puglis HJ, Boone MD (2007) Effects of a fertilizer, an insecticide, and a pathogenic fungus on hatching and survival of bullfrog (Rana catesbeiana) tadpoles. Environ Toxicol Chem 26(10): 2198-2201.
34. Rachowicz LJ, Hero JM, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, Collins JP, Briggs CJ (2005) The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conserv Biol 19: 1441-1448.
35. Romansic JM, Diez KA, Higashi EM, Blaustein AR (2006) Effects of nitrate and the pathogenic water mold Saprolegnia on the survival of amphibian larvae. Dis Aquat Organ 68(3): 235-243.
36. Romansic JM, Higashi EM, Diez KA, Blaustein AR (2007) Susceptibility of newly-metamorphosed frogs to a pathogenic water mould (Saprolegnia sp.). Herpetol J 17(3): 161-166.
37. 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 Organ 83(3): 187-193.
38. Ruthig G (2009) Water molds of the genera Saprolegnia and Leptolegnia are pathogenic to the North American frogs Rana catesbeiana and Pseudacriscrucifer, respectively. Dis Aquat Organ 84: 173-178.
39. Sagvik J, Uller T, Stenlund T, Olsson M (2008a) Intraspecific variation in resistance of frog eggs to fungal infection. Evol Ecol 22: 193-201.
40. Sagvik J, Uller T, Olsson M (2008b) A genetic component of resistance to fungal infection in frog embryos. Proc R Soc B 275: 1393-1396.
41. Smith MA, Berrill M, Kapron CM (2002) Photolyase activity of the embryo and the ultraviolet absorbance of embryo jelly for several Ontario amphibian species. Can J Zool 80: 1109-1116.
42. van West (2006) Saprolegnia parasitica, an oomycete pathogen with a fishy appetite: new challenges for an old problem. Mycologist 20: 99-104.
43. Walls SC, Jaeger RG (1987) Aggression and exploitation as mechanisms of competition in larval salamanders. Can J Zool 65: 2938-2944.
44. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315-322.
45. Willoughby LG (1978) Saprolegnias of salmonid fish in Windermere: a critical analysis. J Fish Dis 1: 51-67.
46. Yamasaki H, Katagiri C, Yoshizaki N (1990) Selective degradation of specific components of fertilization coat and differentiation of hatching gland cells during the two phase hatching of Bufo japonicus embryos. Dev Growth Differ 32: 65-72.
47. Zaror L, Collado L, Bohle H, Landskron E, Montaña J, Avedaño F (2004) Saprolegnia parasitica in salmon and trout from southern Chile. Arch Med Vet 36: 71-78.