Skip to main content
SpringerLink
Log in

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

  • Conservation ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Many amphibians are known to suffer embryonic die-offs as a consequence of Saprolegnia infections; however, little is known about the action mechanisms of Saprolegnia and the host–pathogen relationships. In this study, we have isolated and characterized the species of Saprolegnia responsible for infections of embryos of natterjack toad (Bufo calamita) and Western spadefoot toad (Pelobates cultripes) in mountainous areas of Central Spain. We also assessed the influence of the developmental stage within the embryonic period on the susceptibility to the Saprolegnia species identified. Only one strain of Saprolegnia was isolated from B. calamita and identified as S. diclina. For P. cultripes, both S. diclina and S. ferax were identified. Healthy embryos of both amphibian species suffered increased mortality rates when exposed to the Saprolegnia strains isolated from individuals of the same population. Embryonic developmental stage was crucial in determining the sensitivity of embryos to Saprolegnia infection. The mortalities of P. cultripes and B. calamita embryos exposed at Gosner stages 15 (rotation) and 19 (heart beating) were almost total 72 h after challenge with Saprolegnia, while those exposed at stage 12 (late gastrula) showed no significant effects at that time. This is the first study to demonstrate the role of embryonic development on the sensitivity of amphibians to Saprolegnia.

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. 1a–d

Similar content being viewed by others

References

  • 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

    Article  PubMed  Google Scholar 

  • Banks B, Beebee TJC (1988) Reproductive success of natterjack toads Bufo calamita in two contrasting habitats. J Anim Ecol 57:472–492

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bragg AN (1958) Parasitism of spadefoot tadpoles by Saprolegnia. Herpetologica 14:34

    Google Scholar 

  • Bragg AN (1962) Saprolegnia on tadpoles again in Oklahoma. Southwest Nat 7:79–80

    Article  Google Scholar 

  • Cerenius L, Söderhäll K (1985) Repeated zoospore emergence as a possible adaptation to parasitism in Aphanomyces. Exp Mycol 9:259–263

    Article  Google Scholar 

  • Daszak P (1998) A new fungal disease associated with amphibian population declines: recent research put into perspective. Herpetol Bull 65:38–41

    Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9(2):141–150

    Article  Google Scholar 

  • Densmore CL, Green DV (2007) Diseases of amphibians. ILAR J 48(3):235–254

    CAS  PubMed  Google Scholar 

  • Diéguez-Uribeondo J, Cerenius L, Söderhäll K (1994) Repeated zoospore emergence in Saprolegnia parasitica. Mycol Res 98:810–815

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Du Pasquier L, Schwage J, Flanjnik MF (1989) The immune system of Xenopus. Annu Rev Immunol 7:251–275

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104(6):1745–1750

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kiesecker JM, Blaustein AR (1999) Pathogen reverses competition between larval amphibians. Ecology 80(7):2442–2448

    Article  Google Scholar 

  • Kiesecker JM, Blaustein AR, Miller CL (2001) Transfer of a pathogen from fish to amphibians. Conserv Biol 15:1064–1070

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Martín MP, Raidl S, Tellería MT (2004) Molecular analysis confirm the relationship between Stephanospora caroticolor and Lidtneria trachyspora. Mycotaxon 90:133–140

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Poorten TJ, Kuhn RE (2009) Maternal transfer of antibodies to eggs in Xenopus laevis. Dev Comp Immunol 33:171–175

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ruthig G (2009) Water molds of the genera Saprolegnia and Leptolegnia are pathogenic to the North American frogs Rana catesbeiana and Pseudacris crucifer, respectively. Dis Aquat Organ 84:173–178

    Article  PubMed  Google Scholar 

  • Sagvik J, Uller T, Stenlund T, Olsson M (2008a) Intraspecific variation in resistance of frog eggs to fungal infection. Evol Ecol 22:193–201

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • van West (2006) Saprolegnia parasitica, an oomycete pathogen with a fishy appetite: new challenges for an old problem. Mycologist 20:99–104

    Article  Google Scholar 

  • Walls SC, Jaeger RG (1987) Aggression and exploitation as mechanisms of competition in larval salamanders. Can J Zool 65:2938–2944

    Article  Google Scholar 

  • 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

  • Willoughby LG (1978) Saprolegnias of salmonid fish in Windermere: a critical analysis. J Fish Dis 1:51–67

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

Acknowledgments

Funding was provided by the Spanish Ministry of Education and Science (refs. CGL2005-03727 and Flora Micológica Ibérica VI, CGL2006-12732-C02-01), and by the Diputación de Ávila (Inst. Gran Duque de Alba). The Castilla y León Regional Government provided permission for egg collection and the experimental procedures.

Author information

Authors and Affiliations

  1. Departamento de Biología Animal, Universidad de Salamanca, Campus Miguel de Unamuno, 37007, Salamanca, Spain

    María José Fernández-Benéitez & Miguel Lizana

  2. Instituto de Investigación en Recursos Cinegéticos UCLM-CSIC-JCCM, Rda de Toledo s/n, 13071, Ciudad Real, Spain

    Manuel Eloy Ortiz-Santaliestra

  3. Departamento de Micología, Real Jardín Botánico CSIC, Plaza Murillo 2, 28014, Madrid, Spain

    Javier Diéguez-Uribeondo

Authors
  1. María José Fernández-Benéitez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manuel Eloy Ortiz-Santaliestra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miguel Lizana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Javier Diéguez-Uribeondo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María José Fernández-Benéitez.

Additional information

Communicated by Craig Osenberg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fernández-Benéitez, M.J., Ortiz-Santaliestra, M.E., Lizana, M. et al. Differences in susceptibility to Saprolegnia infections among embryonic stages of two anuran species. Oecologia 165, 819–826 (2011). https://doi.org/10.1007/s00442-010-1889-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1889-5

Keywords

Search

Navigation