Abstract
Knowledge of host range and mechanisms of disease resistance is fundamental to predicting impacts and spread of marine diseases. Prevalence of signs of aspergillosis, caused by the terrestrial fungus Aspergillus sydowii, was assessed in the Yucatan among three species of sea fan: Gorgonia ventalina, G. cf. mariae, and G. flabellum. The Yucatan is unusual in that ranges of all three sea fan species overlap at many sites along a cline of increasing depth, allowing us to evaluate potential causes of differing prevalence among species. Signs of aspergillosis were observed in all the three species. However, the prevalence of infection in G. cf. mariae, a deep-water species, was consistently low even at sites where G. ventalina was common and had moderate levels of infection. Because G. cf. mariae is a relatively small-stature sea fan, we compared the prevalence of signs in G. cf. mariae to a subset of comparatively sized G. ventalina. G. ventalina had a significantly higher prevalence of aspergillosis, indicating that size does not explain the lower prevalence in G. cf. mariae. Prevalence of disease signs on the shallow-water G. flabellum was also significantly higher than G. cf. mariae, but did not differ from G. ventalina. To test the hypothesis that higher chemical resistance accounts for the low prevalence of disease in G. cf. mariae, we measured the response of A. sydowii in culture to antifungal extracts from each sea fan species. Significantly lower fungal growth rates on extracts of G. cf. mariae than G. ventalina support the hypothesis that G. cf. mariae is more chemically resistant to aspergillosis. When comparing sea fan disease across different regions of the Yucatan, we detected significantly higher prevalence in G. ventalina near Akumal than further north near Cozumel and Puerto Morelos. In Akumal, there was a strong positive correlation between sea fan size and disease, with the largest fans showing the highest prevalence and severity in all three species. In addition, prevalence of aspergillosis in G. ventalina was density-dependent in Ak.
Similar content being viewed by others
References
Alker AP, Smith GW, Kim K (2001) Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen on Caribbean sea fan corals. Hydrobiologia 460:105–111
Anderson RM, May RM (1991) Infectious diseases of humans: dynamics and control. Oxford University Press, Oxford
Berger RD (1973) Infection rates of Cercospora apii in mixed populations of susceptible and tolerant celery. Phytopathology 63:535–537
Browning JA (1974) Relevance of knowledge about natural ecosystems to development of pest management programs for agro-ecosystems. Proc Amer Phytopath Soc 1:191–199
Burdon JJ (1982) The effect of fungal pathogens on plant communities. In: Newman EI (ed) The plant community as a working mechanism. British Ecological Society, pp 99–112
Burdon JJ (1992) The growth and regulation of pathogenic fungal populations. In: Carroll GC, Wicklow DT (eds) The fungal community: its organization and role in the ecosystem, 2nd edn. Mycology series, vol 9. Marcel Dekker, New York, NY, pp 173–181
Burdon JJ, Chilvers GA (1975) Epidemiology of damping off disease (Pythium irregulare) in relation to density of Lepidium sativum seedlings. Ann Appl Biol 81:135–143
Burdon JJ, Chilvers GA (1976) Controlled environment experiments on epidemics of barley mildew in different density host stands. Oecologia 26:61–72
Burdon JJ, Shattock RC (1980) Disease in plant communities. Appl Biol 5:145–219
Cleaveland S, Laurenson MK, Taylor LH (2001) Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Phil Trans R Soc Lond Ser B X:991–999
Colwell RR (1996) Global climate and infectious disease: The Cholera paradigm. Science 274:2025–2031
Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science (Wash DC) 287:443–449
Dobson A, Foufopoulos J (2001) Emerging infectious pathogens of wildlife. Phil Trans Roy Soc Lond B 356:1001–1021
Dube D, Kim K, Alker AP, Harvell CD (2002) Size structure and geographic variation in chemical resistance of sea fan corals (Gorgonia ventalina) against a fungal pathogen. Mar Ecol Prog Ser 231:139–150
Epstein PR, Sherman BH, Siegfried ES, Langston A, Prasad S, McKay B (eds) (1998) Marine ecosystems: emerging diseases as indicators of change: health of the oceans from Labrador to Venezuela. Year of the Ocean Special Report. The Center for Health and the Global Environment, Harvard Medical School, Boston, MA
Geiser DM, Taylor JW, Ritchie KB, Smith GW (1998) Cause of sea fan death in the West Indies. Nature 394:137–138
Goreau TJ, Cervino J, Goreau M, Hayes R, Hayes M, Richardson L, Smith GW, DeMeyer K, Nagelkerken I, Garzon-Ferrera J, Gil D, Garrison G, Williams EH, Bunkley-Williams L, Quirolo C, Patterson K, Porter JW, Porter K (1998) Rapid spread of diseases in Caribbean coral reefs. Rev Biol Trop 46(Suppl 5):157–171
Green EP, Bruckner AW (2000) The significance of coral disease epizootiology for coral reef conservation. Biol Conserv 96(3):347–361
Harper JL (1977) Population biology of plants. Academic, London
Harvell CD, Tollrian R (1999) Why inducible defenses?. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton NJ, pp 1–9
Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases: climate links and anthropogenic factors. Science 285:1505–1510
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162
Harvell CD, Aronson R, Baron N, Connel J, Dobson A, Ellner S, Gerber L, Kim K, Kuri A, McCallum H, Lafferty K, McKay B, Porter J, Pascual M, Smith G, Sutherland K, Ward J (2004) The rising tide of ocean diseases: unsolved problems and research priorities. Frontiers Ecol Environ 2:375–382
Heide-Jorgensen MP, Harkonen T, Dietz R, Thompson PM (1992) Retrospective of the 1988 European sea epizootic. Dis Aquat Org 13:37–62
Jennersten O, Nilsson SG, Wastljung U (1983) Local plant populations as ecological islands: The infection of Viscaria vulgaris by the fungus Ustilago violacea. OIKOS 41:391–395
Jolles AE, Sullivan P, Alker AP, Harvell CD (2002) Disease transmission of aspergillosis in sea fans: Inferring process from spatial pattern. Ecology 83(9):2373–2378
Karban R, IT Baldwin (1997) Induced responses to herbivory. University of Chicago Press, Chicago
Kim K, Harvell CD (2002) Aspergillosis of sea fan corals: disease dynamics in the Florida Keys. In: Porter JW, Porter K (eds) The Everglades, Florida Bay, and coral reefs of the Florida Keys: an Ecosystem Sourcebook. CRC Press, New York, pp 813–824
Kim K, Harvell CD (2004) The rise and fall of a six-year coral-fungal epizootic. Am Nat 164:S52–S63
Kim K, Harvell CD, Kim PD, Smith GW, Merkel SM (2000a) Fungal disease resistance of Caribbean sea fan corals (Gorgonia spp). Mar Biol 136:259–267
Kim K, Kim PD, Alker AP, Harvell CD (2000b) Antifungal properties of gorgonian corals. Mar Biol 137:393–401
Kim K, Dobson AP, Gulland FMD, Harvell CD (2004) Disease and the conservation of marine diversity. In: Crowder L, Norse E (eds) Conservation of marine ecosystems, Island Press
Lafferty KD, Gerber LR (2002) Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv Biol 16(3):593–604
McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10(5):190–194
Morris Jr JG, Potter M (1997) Emergence of new pathogens as a function of changes in host susceptibility. Emerg Inf Dis 3(4):435–441
Morse SS (1995) Factors in the emergence of infectious diseases. Emerg Inf Dis 1:7–15
Nagelkerken I, Buchan K, Smith GW, Bonair K, Bush P, Garzon-Ferreira J, Botero L, Gayle P, Herberer C, Petrovic C, Pors L, Yoshioka P (1996) Widespread disease in Caribbean sea fans: I Spreading and general characteristics. Proc 8th Int Coral Reef Symp 1:679–682
Nagelkerken I, Buchan K, Smith GW, Bonair K, Bush P, Garzon-Ferreira J, Botero L, Gayle P, Harvell CD, Herberer C, Kim K, Petrovic C, Pors L, Yoshioka P (1997) Widespread disease in Caribbean sea fans: II Patterns of infection and tissue loss. Mar Ecol Prog Ser 160:255–263
Porter JW, Dustan P, Jaap WC, Patterson KL, Kosmynin V, Meier OW, Patterson ME, Parsons M (2001) Patterns of spread of coral disease in the Florida Keys. Hydrobiologia 460:1–24
Raymundo LJ, Harvell CD, Reynolds T (2003) Porites ulcerative white spot disease: description, prevalence, and host range of a new coral disease impacting Indo-Pacific reefs. Dis Aquat Org 56:95–104
Richardson LL, Goldberg WM, Kuta K, Aronson RB, Smith GW, Ritchie KB, Halas JC, Feingold JS, Miller SL (1998) Florida’s mystery coral-killer identified. Nature 392:557–558
Roelke-Parker M, Munson L, Packer C, Kock R, Cleaveland S, Carpenter M, O’Brien SJ, Pospischil A, Hofmann LR, Lutz H, Mwamengele GLM, Mgasa MN, Machange GA, Summers BA, Appel MJG (1996) A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379(6564):441–445
Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Enviro Microbiol 4(6):318–326
Singer JD (1998) Using SAS PROC MIXED to fit multilevel models, hierarchical models, and individual growth models. J Educ Behavior Stat 24(4):323–355
Smith GW, Ives LD, Nagelkerken IA, Ritchie KB (1996) Caribbean sea fan mortalities. Nature 383:487
Smith GW, Harvell CD, Kim K (1998) Response of sea fans to infection with Aspergillus spp (Fungi). Rev Biol Trop 46:205–208
Sweeney JC, Migaki G, Vainik PM, Conklin RH (1976) Systemic mycoses in marine mammals. J Am Vet Med Assoc 169(9):946–948
Van der Plank (1969) Pathogenic races: Host resistance and an analysis of pathogenicity of fungi, wheat-M Tomato-D. J Plant Path 75(1/2):45–52
Ward JR, Lafferty K (2004) The elusive baseline of marine diseases: are diseases in ocean ecosystems increasing?. Pub Lib Sci 2:0542–0547
Weil E (2002) Coral disease epizootiology: status and research needs. Coral health and disease: developing a national research plan. Coral Health and Disease Consortium, Charleston, SC, January 22–25, 14p
Weil E, Urreiztieta I, Garzon-Ferreira J (2002) Geographic variability in the incidence of coral and octocoral diseases in the wider Caribbean. Proc 9th Int Coral Reef Symp 2:1231–1238
Williams EH, Bunkley-Williams L (1990) The world-wide coral reef bleaching cycle and related sources of coral mortality. Atoll Res Bull 335:1–72
Acknowledgements
We acknowledge NSF OCE-9818830 and an NSF International Programs Supplement for support of this project. We greatly appreciate logistical support and assistance by Centro Ecológico Akumal and the Akumal Dive Shop. Garriet Smith is acknowledged for providing us with A. sydowii, and Juan Sanchez for his assistance in identifying G. cf. mariae.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P.W. Sammarco, Chauvin
Rights and permissions
About this article
Cite this article
Mullen, K.M., Harvell, C.D., Alker, A.P. et al. Host range and resistance to aspergillosis in three sea fan species from the Yucatan. Mar Biol 149, 1355–1364 (2006). https://doi.org/10.1007/s00227-006-0275-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-006-0275-7