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Is Marine Dispersion of the Lethargic Crab Disease Possible? Assessing the Tolerance of Exophiala cancerae to a Broad Combination of Salinities, Temperatures, and Exposure Times

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Abstract

Since 1997, an emergent fungal disease named lethargic crab disease (LCD) has decimated stocks of the edible mangrove land crab Ucides cordatus (Linnaeus, 1763) (Brachyura: Ocypodidae) along the Brazilian coast, threatening the mangrove ecosystem and causing socioeconomic impacts. Evidence from a variety of sources suggests that the black yeast Exophiala cancerae (Herpotrichiellaceae, Chaetothyriales) has been responsible for such epizootic events. Based on the spatiotemporal patterns of the LCD outbreaks, the well-established surface ocean currents, and the range of ecological traits of Exophiala spp., a marine dispersal hypothesis may be proposed. Using in vitro experiments, we tested the survival and growth of E. cancerae CBS 120420 in a broad combination of salinities, temperatures, and exposure times. While variation in salinity did not significantly affect the growth of colony-forming units (CFUs) (P > 0.05), long exposure times visibly influenced an increase in CFUs growth (P < 0.05). However, higher temperature (30 °C) caused a reduction of about 1.2-fold in CFUs growth (P < 0.05). This result suggests that sea surface temperatures either above or below the optimum growth range of E. cancerae could play a key role in the apparent north–south limits in the geographical distribution of LCD outbreaks. In light of our results, we conclude that a fundamental step toward the understanding of LCD epidemiological dynamics should comprise a systematic screening of E. cancerae in estuarine and coastal waters.

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References

  1. Boeger WA, Pie MR, Ostrensky A, Patella L. Lethargic crab disease: multidisciplinary evidence supports a mycotic etiology. Mem Inst Oswaldo Cruz. 2005;100:161–7.

    Article  PubMed  Google Scholar 

  2. Nóbrega RR, Nishida AK. Aspectos socioeconômicos e percepção ambiental dos catadores de caranguejo-uçá, Ucides cordatus (L. 1763) (Decapoda, Brachyura) do estuário do rio Mamanguape, Nordeste do Brasil (in Portuguese). Interciencia. 2003;28:36–43.

    Google Scholar 

  3. Alves RR, Nishida AK, Hernández MI. Environmental perception of gatherers of the crab “caranguejo-uçá” (Ucides cordatus, Decapoda, Brachyura) affecting their collection attitudes. J Ethnobiol Ethnomed. 2005;. doi:10.1186/1746-4269-1-10.

    Google Scholar 

  4. Boeger WA, Pie MR, Vicente VA, Ostrensky A, Hungria D, Castilho GG. Histopathology of the mangrove land crab Ucides cordatus (Ocypodidae) affected by lethargic crab disease. Dis Aquat Organ. 2007;78:73–81.

    Article  PubMed  Google Scholar 

  5. Ferreira CP, Pie MR, Esteva L, Mancera PFA, Boeger WA, Ostrensky A. Modelling the lethargic crab disease. J Biol Dyn. 2009;3(6):620–34.

    Article  CAS  PubMed  Google Scholar 

  6. De Hoog GS, Vicente VA, Najafzadeh MJ, Harrak MJ, Badali H, Seyedmousavi S. Waterborne Exophiala species causing disease in cold-blooded animals. Persoonia. 2011;. doi:10.3767/003158511X614258.

    PubMed  PubMed Central  Google Scholar 

  7. Orélis-Ribeiro R, Boeger WA, Vicente VA, Chammas M, Ostrensky A. Fulfilling Koch’s postulates confirms the mycotic origin of lethargic crab disease. Antonie Van Leeuwenhoek. 2011;99:601–8.

    Article  PubMed  Google Scholar 

  8. Pie MR, Boeger WA, Patella L, Vicente VA, Orélis-Ribeiro R, Ostrensky A. Specific primers for the detection of the black-yeast fungus associated with the lethargic crab disease. Dis Aquat Organ. 2011;94:73–5.

    Article  CAS  PubMed  Google Scholar 

  9. Vicente VA, Orélis-Ribeiro R, Najafzadeh MJ, Sun J, Guerra RS, Miesch S, Ostrensky A, Meis JF, Klaassen CH, de Hoog GS, Boeger WA. Black yeast-like fungi associated with lethargic crab disease (LCD) in the mangrove-land crab, Ucides cordatus (Ocypodidae). Vet Microbiol. 2012;158:109–22.

    Article  CAS  PubMed  Google Scholar 

  10. Avila RP, Mancera PFA, Esteva L, Pie MR, Ferreira CP. Traveling waves in the lethargic crab disease. Appl Math Comput. 2012;218(19):9898–910.

    Google Scholar 

  11. Guerra RS, do Nascimento MMF, Miesch S, Najafzadeh MJ, Orélis-Ribeiro R, Ostrensky A, de Hoog GS, Vicente VA, Boeger WA. Black yeast biota in the mangrove, in search of the origin of the lethargic crab disease (LCD. Mycopathologia. 2013;175(5–6):421–30.

    Article  PubMed  Google Scholar 

  12. Magris RA, Barreto R. Mapping and assessment of protection of mangrove habitats in Brazil. Pan Am J Aquat Sci. 2010;5:546–56.

    Google Scholar 

  13. Melo GAS. Manual de identificação dos Brachyura (caranguejos e siris) do litoral brasileiro. São Paulo: Plêiade; 1996.

    Google Scholar 

  14. Carmichael JW. Cerebral mycetoma of trout due to a Phialophora-like fungus. Sabouraudia. 1966;5:120–3.

    Article  CAS  PubMed  Google Scholar 

  15. Mcginnis MR, Ajello LA. A new species of Exophiala isolated from channel catfish. Mycologia. 1974;66:518–20.

    Article  CAS  PubMed  Google Scholar 

  16. Pedersen OA, Langvad F. Exophiala psychrophila sp. nov., a pathogenic species of the black yeasts isolated from farmed Atlantic salmon. Mycol Res. 1989;92:153–6.

    Article  Google Scholar 

  17. Schmidt AJ. Estudo da dinâmica populacional do caranguejo-uçá, Ucides cordatus cordatus e dos efeitos de uma mortalidade em massa desta espécie em manguezais do Sul Bahia (in Portuguese). Dissertation, IOUSP, São Paulo; 2006.

  18. Iwatsu T, Miyajii M, Okmoto S. Isolation of Phialophora verrucosa and Fonsecaea pedrosoi from nature in Japan. Mycopathologia. 1981;75:149–58.

    Article  Google Scholar 

  19. Harris RR. Santos MCF. Sodium uptake and transport (Na + K+) ATPase changes following Na + depletion and low salinity acclimation in the mangrove crab Ucides cordatus (L.). Comp Biochem Physiol. 1993;105:35–42.

    Article  Google Scholar 

  20. Orélis-Ribeiro R, Chammas MA, Ostrensky A, Boeger WA. Viability of the etiologic agent of the Lethargic Crab Disease, Exophiala cancerae, during cooking of the mangrove-land crab: Does this traditional dish represent a risk to humans? Food Control. 2012;25:591–3.

    Article  Google Scholar 

  21. Ffield A. North Brazil current rings viewed by TRMM Microwave Imager SST and the influence of the Amazon Plume. Deep Sea Res Part I Oceanogr Res Pap. 2005;52(1):137–60.

    Article  Google Scholar 

  22. Miloslavich P, Klein E, Díaz JM, Hernández CE, Bigatti G, Campos L, Artigas F, Castillo J, Penchaszadeh PE, Neill PE, Carranza A, Retana MV, de Astarloa JMD, Lewis M, Yorio P, Piriz ML, Rodríguez D, Yoneshigue-Valentin Y, Gamboa L, Martín A. Marine biodiversity in the Atlantic and Pacific Coasts of South America: knowledge and gaps. PLoS ONE. 2011;. doi:10.1371/journal.pone.001463.

    Google Scholar 

  23. Bischof B, Mariano AJ, Ryan EH: “The North Brazil Current”. Ocean Surf Curr. http://oceancurrents.rsmas.miami.edu/atlantic/north-brazil.html.

  24. Bischof B, Rowe E, Mariano AJ, Ryan EH: “The Brazil Current.” Ocean Surf Curr. http://oceancurrents.rsmas.miami.edu/atlantic/brazil.html.

  25. Kjerfve B, Perillo GME, Gardner LR, Rine JM, Dias GTM, Mochel FR. Morphodynamics of muddy environments along the Atlantic coasts of North and South America. In: Healy TR, Wang Y, Healy J-A, editors. Muddy coasts of the world: processes, deposits and functions. Amsterdam: Elsevier; 2002. p. 479–532.

    Chapter  Google Scholar 

  26. Oliveira LR, Piola AR, Mata MM, Soares ID. Brazil current surface circulation and energetics observed from drifting buoys. J Geophys Res. 2009;. doi:10.1029/2008JC004900.

    Google Scholar 

  27. Campos EJD, Velhote D, Silveira ICA. Shelf break upwelling driven by Brazil current cyclonic meanders. Geophys Res Lett. 2000;. doi:10.1029/1999GL010502.

    Google Scholar 

  28. Calado L, Gangopadhyay A, Silveira ICA. A parametric model for the Brazil current meanders and eddies off Southeastern Brazil. Geophys Res Lett. 2006;. doi:10.1029/2006GL026092.

    Google Scholar 

  29. Guimaraens MA, Coutinho R. Temporal and spatial variation of Ulva spp. and water properties in the Cabo Frio upwelling region of Brazil. Aquat Bot. 2000;66:101–14.

    Article  Google Scholar 

  30. Matsuura Y. Brazilian sardine (Sardinella brasiliensis) spawning in the Southeast Brazilian bight over the period 1976–1993. Rev Bras Oceanogr. 1998;46(1):33–43.

    Article  Google Scholar 

  31. Campos PC, Moller OO Jr, Piola AR, Palma ED. Seasonal variability and coastal upwelling near Cape Santa Marta (Brazil). J Geophys Res Oceans. 2013;. doi:10.1002/2012JC008492.

    Google Scholar 

  32. Sav H, Ozakkas F, Altınbas R, Kiraz N, Tümgör A, Gümral R, Döğen A, Ilkit M, de Hoog GS. Virulence markers of opportunistic black yeast in Exophiala. Mycoses. 2016;59:343–50.

    Article  CAS  PubMed  Google Scholar 

  33. Agosta SJ, Klemens JA. Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecol Lett. 2008;. doi:10.1111/j.1461-0248.2008.01237.x.

    PubMed  Google Scholar 

  34. Agosta SJ, Janz N, Brooks DR. How specialists can be generalists: resolving the “parasite paradox” and implications for emerging infectious disease. Zoologia (Curitiba). 2010;27:151–62.

    Article  Google Scholar 

  35. Brooks DR, Agosta SJ. Children of time: the extended synthesis and major metaphors of evolution. Zoologia (Curitiba). 2012;29:497–514.

    Article  Google Scholar 

  36. Araujo SBL, Braga MP, Brooks DR, Agosta SJ, Hoberg EP, von Hartenthal FW, Boeger WA. Understanding host-switching by ecological fitting. PLoS ONE. 2015;. doi:10.1371/journal.pone.0139225.

    Google Scholar 

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Acknowledgements

We thank Robert W. Pilchowski (GIA, UFPR) for supplying the seawater used in the in vitro experiments, and Marcio R. Pie (Department of Zoology, UFPR) for advice in the experimental design and statistical analysis. This study was supported by the Companhia de Desenvolvimento Industrial e de Recursos Minerais de Sergipe (CODISE) (Sergipe, Brazil), the Secretaria de Estado da Ciência, Tecnologia e Ensino Superior do Estado do Paraná (SETI) (Paraná, Brazil), and also by a grant to WAB and a Postdoctoral Fellowship to ROR under the project entitled “Exploring a new paradigm for the evolution of host-parasites associations,” number 404344/2013-5 of the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brazil) (http://www.cnpq.br).

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Correspondence to Raphael Orélis-Ribeiro.

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Orélis-Ribeiro, R., Vicente, V.A., Ostrensky, A. et al. Is Marine Dispersion of the Lethargic Crab Disease Possible? Assessing the Tolerance of Exophiala cancerae to a Broad Combination of Salinities, Temperatures, and Exposure Times. Mycopathologia 182, 997–1004 (2017). https://doi.org/10.1007/s11046-017-0169-x

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