Skip to main content

Advertisement

SpringerLink
Log in

Differential modulation of eastern oyster (Crassostrea virginica) disease parasites by the El-Niño-Southern Oscillation and the North Atlantic Oscillation

  • Original Paper
  • Published:
International Journal of Earth Sciences Aims and scope Submit manuscript

Abstract

The eastern oyster (Crassostrea virginica) is affected by two protozoan parasites, Perkinsus marinus which causes Dermo disease and Haplosporidium nelsoni which causes MSX (Multinucleated Sphere Unknown) disease. Both diseases are largely controlled by water temperature and salinity and thus are potentially sensitive to climate variations resulting from the El Niño-Southern Oscillation (ENSO), which influences climate along the Gulf of Mexico coast, and the North Atlantic Oscillation (NAO), which influences climate along the Atlantic coast of the United States. In this study, a 10-year time series of temperature and salinity and P. marinus infection intensity for a site in Louisiana on the Gulf of Mexico coast and a 52-year time series of air temperature and freshwater inflow and oyster mortality from Delaware Bay on the Atlantic coast of the United States were analyzed to determine patterns in disease and disease-induced mortality in C. virginica populations that resulted from ENSO and NAO climate variations. Wavelet analysis was used to decompose the environmental, disease infection intensity and oyster mortality time series into a time–frequency space to determine the dominant modes of variability and the time variability of the modes. For the Louisiana site, salinity and Dermo disease infection intensity are correlated at a periodicity of 4 years, which corresponds to ENSO. The influence of ENSO on Dermo disease along the Gulf of Mexico is through its effect on salinity, with high salinity, which occurs during the La Niña phase of ENSO at this location, favoring parasite proliferation. For the Delaware Bay site, the primary correlation was between temperature and oyster mortality, with a periodicity of 8 years, which corresponds to the NAO. Warmer temperatures, which occur during the positive phase of the NAO, favor the parasites causing increased oyster mortality. Thus, disease prevalence and intensity in C. virginica populations along the Gulf of Mexico coast is primarily regulated by salinity, whereas temperature regulates the disease process along the United States east coast. These results show that the response of an organism to climate variability in a region is not indicative of the response that will occur over the entire range of a particular species. This has important implications for management of marine resources, especially those that are commercially harvested.

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. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Ackerman E, Elveback LR, Fox JP (1984) Simulation of infectious disease epidemics. Thomas, Springfield

    Google Scholar 

  • Andrews JD (1966) Oyster mortality studies in Virginia. V. Epizootiology of MSX, a protistian pathogen of oysters. Ecology 47:19–31. doi:10.2307/1935741

    Article  Google Scholar 

  • Andrews JD, Wood JL (1967) Oyster mortality studies in Virginia. VI. History and distribution of Minchinia nelsoni, a pathogen of oysters, in Virginia. Chesap Sci 8:1–13. doi:10.2307/1350351

    Article  Google Scholar 

  • Behrens EW (1965) Use of the Goldberg refractometer as a salinometer for biological and geological field work. J Mar Res 2:165–171

    Google Scholar 

  • Bergquist DC, Hale JA, Baker P, Baker SM (2006) Development of ecosystem indicators for the Sewanee River estuary: oyster reef habitat quality along a salinity gradient. Estuaries Coasts 29:353–360

    Google Scholar 

  • Bower SM, McGladdery SE, Price IM (1994) Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annu Rev Fish Dis 4:1–200. doi:10.1016/0959-8030(94)90028-0

    Article  Google Scholar 

  • Breitburg DL, Coen LD, Luckenbach MW, Mann R, Posey M, Wesson JA (2000) Oyster reef restoration: convergence of harvest and conservation strategies. J Shellfish Res 19:371–377

    Google Scholar 

  • Burreson EM, Ragone Calvo LM (1996) Epizootiology of Perkinsus marinus disease of oysters in Chesapeake Bay, with emphasis on data since 1985. J Shellfish Res 15:17–34

    Google Scholar 

  • Burreson EM, Alvarez RS, Martinez VV, Macedo LA (1994) Perkinsus marinus (Apicomplexa) as a potential source of oyster Crassostrea virginica mortality in the coastal lagoons of Tabasco, Mexico. Dis Aquat Organ 20:77–82. doi:10.3354/dao020077

    Article  Google Scholar 

  • Bushek D, Ford SE, Allen SK Jr (1994) Evaluation of methods using Ray’s fluid thioglycollate medium for the diagnosis of Perkinsus marinus infection in the eastern oyster, Crassostrea virginica. Annu Rev Fish Dis 4:210–217. doi:10.1016/0959-8030(94)90029-9

    Article  Google Scholar 

  • Chu FLE, Greene KH (1989) Effect of temperature and salinity on in vitro culture of the oyster pathogen Perkinsus marinus (Apicomplexa: Perkinsea). J Invertebr Pathol 53:260–268. doi:10.1016/0022-2011(89)90016-5

    Article  Google Scholar 

  • Coen LD, Luckenbach MW, Breitburg DL (1999) The role of oyster reefs as essential fish habitat: a review of current knowledge and some new perspectives. Am Fish Soc Symp 22:438–454

    Google Scholar 

  • Cook T, Folli M, Klinck J, Ford S, Miller J (1998) The relationship between increasing sea-surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuar Coast Shelf Sci 46:587–597. doi:10.1006/ecss.1997.0283

    Article  Google Scholar 

  • Craig A, Powell EN, Fay RR, Brooks JM (1989) Distribution of Perkinsus marinus in Gulf Coast oyster populations. Estuaries 12:82–91. doi:10.2307/1351499

    Article  Google Scholar 

  • Culloty SC, Cronin MA, Mulcahy MF (2003) Possible limitations of diagnostic methods recommended for the detection of the protistan, Bonamia ostrae in the European flat oyster, Ostrea edulis. Bull Eur Assoc Fish Pathol 23:67–71

    Google Scholar 

  • Daubechies I (1992) Ten lectures on wavelets. Society of Industrial and Applied Mathematics, Philadelphia, pp 1–357

    Google Scholar 

  • Douglas AV, Englehart PJ (1981) On a statistical relationship between autumn rainfall in the central Equatorial Pacific and subsequent winter precipitation in Florida. Mon Weather Rev 109:2377–2382. doi:10.1175/1520-0493(1981)109<2377:OASRBA>2.0.CO;2

    Article  Google Scholar 

  • Easterling DR, Horton B, Jones PD, Peterson TC, Karl TR, Parker DE et al (1997) Maximum and minimum temperature trends for the globe. Science 277:364–367. doi:10.1126/science.277.5324.364

    Article  Google Scholar 

  • Fegley SR, Ford SE, Kraeuter JN, Haskin HH (2003) The persistence of New Jersey’s oyster seedbeds in the presence of MSX disease and harvest: management’s role. J Shellfish Res 22:451–464

    Google Scholar 

  • Ford SE (1996) Range extension by the oyster parasite Perkinsus marinus into the northeastern United States: response to climate change. J Shellfish Res 15:45–56

    Google Scholar 

  • Ford SE, Chintala MM (2006) Northward expansion of a marine parasite: testing the role of temperature adaptation. J Exp Mar Biol Ecol 339:226–235. doi:10.1016/j.jembe.2006.08.004

    Article  Google Scholar 

  • Ford SE, Haskin HH (1982) History and epizootiology of Haplosporidium nelsoni (MSX), an oyster pathogen, in Delaware Bay, 1957–1980. J Invertebr Pathol 40:118–141. doi:10.1016/0022-2011(82)90043-X

    Article  Google Scholar 

  • Ford SE, Tripp MR (1996) Diseases and defense mechanisms. In: Newell RIE, Kennedy VS, Eble AF (eds) The eastern oyster Crassostrea virginica. Maryland Sea Grant College, College Park, pp 383–450

    Google Scholar 

  • Ford SE, Powell EN, Klinck JM, Hofmann EE (1999) Modeling the MSX in eastern oyster (Crassostrea virginica) populations. I. Model development, implementation and verification. J Shellfish Res 18:473–498

    Google Scholar 

  • Ford SE, Cummings MJ, Powell EN (2006) Estimating mortality in natural assemblages of oysters. Estuaries Coasts 29:361–374

    Google Scholar 

  • Gutiérrez JL, Jones CC, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90. doi:10.1034/j.1600-0706.2003.12322.x

    Article  Google Scholar 

  • Harding JM, Mann R (2000) Estimates of naked goby (Gobiosoma bosc), striped blenny (Chasmodes bosquianus) and eastern oyster (Crassostrea virginica) larval production around a restored Chesapeake Bay oyster reef. Bull Mar Sci 66:29–45

    Google Scholar 

  • Harding JM, Mann R (2001) Oyster reefs as fish habitats: opportunistic use of restored reefs by transient fishes. J Shellfish Res 20:951–959

    Google Scholar 

  • Hargis WJ Jr, Haven DS (1994) The precarious state of the Chesapeake public oyster resource. In: Toward a sustainable coastal watershed: the Chesapeake experiment. Proceedings of the conference, 1–3 June 1974, Norfolk, VA, Chesapeake Research Consortium Publication, vol 149, pp 559–584

  • Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ et al (1999) Emerging marine diseases—climate links and anthropogenic factors. Science 285:1505–1510. doi:10.1126/science.285.5433.1505

    Article  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS et al (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162. doi:10.1126/science.1063699

    Article  Google Scholar 

  • Haskin HH (1953) First annual report on the natural seed beds investigation. New Jersey Agricultural Experiment Station, Rutgers University, 75 p

  • Haskin HH (1972) Delaware River flow-bay salinity relationships. Report to the Delaware River Basin Commission. Phase III. Rutgers University, 12 p

  • Haskin HH, Andrews JD (1988) Uncertainties and speculations about the life cycle of the eastern oyster pathogen Haplosporidium nelsoni (MSX). In: Fisher WS (ed) Disease processes in marine bivalve molluscs. Special Publication 18, American Fish Society, Bethesda, pp 5–22

  • Haskin HH, Stauber LA, Mackin JG (1966) Minchinica nelsoni n. sp. (Haplosporida, haplosporidiidae): causative agent of the Delaware Bay oyster epizootic. Science 153:1414–1416. doi:10.1126/science.153.3742.1414

    Article  Google Scholar 

  • Hofmann EE, Powell EN, Klinck JM, Saunders G (1995) Modeling diseased oyster populations. I. Modeling Perkinsus marinus infections in oysters. J Shellfish Res 14:121–151

    Google Scholar 

  • Hofmann E, Ford S, Powell E, Klinck J (2001) Modeling studies of the effect of climate variability on MSX disease in eastern oyster (Crassostrea virginica) populations. Hydrobiologia 460:195–212. doi:10.1023/A:1013159329598

    Article  Google Scholar 

  • HSRL (2007) Report of the 2006 stock assessment workshop (9th SAW) for the New Jersey Delaware Bay Oyster Beds. Haskin Shellfish Research Laboratory, Rutgers University, Port Norris, 94 p

  • Hufnagel L, Brockmann D, Geisel T (2004) Forecast and control of epidemics in a globalized world. Proc Natl Acad Sci USA 101:15124–15129. doi:10.1073/pnas.0308344101

    Article  Google Scholar 

  • Hurrell JW, Kushnir Y, Ottersen G, Visbeck M (2003) An overview of the North Atlantic Oscillation. In: Hurrell JW, Kushnir Y, Ottersen G, Visbeck M (eds) The North Atlantic Oscillation: climatic significance and environmental impact. Geophysics Monographic Series, vol 134, pp 1–35

  • Jordan S (1995) Population and disease dynamics of Maryland oyster bars: a multivariate classification analysis. J Shellfish Res 14:459–468

    Google Scholar 

  • Kennedy VS (1990) Anticipated effects of climate change on estuarine and coastal fisheries. Fisheries 15(6):16–25. doi:10.1577/1548-8446(1990)015<0016:AEOCCO>2.0.CO;2

    Article  Google Scholar 

  • Kermack WO, McKendrick AG (1991) Contributions to the mathematical theory of epidemics. II. The problem of endemicity. Bull Math Biol 1:57–58

    Google Scholar 

  • Kim Y, Powell EN (1998) Influence of climate change on interannual variation in population attributes of Gulf of Mexico oysters. J Shellfish Res 17:265–274

    Google Scholar 

  • Kim Y, Powell EN (2006) Relationships among parasites and pathologies in sentinel bivalves: NOAA Status and Trends “Mussel Watch” Program. Bull Mar Sci 79:3–112

    Google Scholar 

  • Kleinschuster SJ, Parent J (1995) Sub-clinical infection of oysters Crassostrea virginica (Gmelin 1791) from Maine by species of the genus Perkinsus (Apicomplexa). J Shellfish Res 14:489–491

    Google Scholar 

  • Klinck JM, Powell EN, Kraeuter JN, Ford SE, Ashton-Alcox KA (2001) A fisheries model for managing the oyster fishery during times of disease. J Shellfish Res 20:977–989

    Google Scholar 

  • Klinck JM, Powell EN, Hofmann EE, Dekshenieks MM (2002) Impact of channelization on oyster production: a hydrodynamic-oyster population model for Galveston Bay, Texas. Environ Model Assess 7:273–289. doi:10.1023/A:1020954502355

    Article  Google Scholar 

  • La Peyre MK, Nickens AD, Volety AK, Tolley GS, La Peyre JF (2003) Environmental significance of freshets in reducing Perkinsus marinus infection in eastern oysters Crassostrea virginica: potential management applications. Mar Ecol Prog Ser 248:165–176. doi:10.3354/meps248165

    Article  Google Scholar 

  • Lafferty KD, Kuris AM (1993) Mass mortality of abalone Haliotis cracherodii on the California Channel Islands: tests of epidemiological hypothesis. Mar Ecol Prog Ser 96:239–248. doi:10.3354/meps096239

    Article  Google Scholar 

  • Larsen PF (1985) The benthic macrofauna associated with the oyster reefs of the James River Estuary, Virginia, USA. Int Rev Ges Hydrobiol 70:797–814. doi:10.1002/iroh.19850700605

    Article  Google Scholar 

  • Mackin JG (1956) Dermocystidium marinum and salinity. Proc Natl Shellfish Assoc 46:116–128

    Google Scholar 

  • Mackin JG (1962) Oyster disease caused by Dermocystidium marinum and other microorganisms in Louisiana. Publ Inst Mar Sci Univ Tex 7:132–229

    Google Scholar 

  • Mackin JG, Hopkins SH (1958) Results of Projects Nine and Twenty-three: a summary report. Texas A&M Res Foundation, College Station, pp 1–200

    Google Scholar 

  • Mackin JG, Hopkins SH (1962) Studies on oyster mortality in relation to natural environments and to oil fields in Louisiana. Publ Inst Mar Sci 7:1–131

    Google Scholar 

  • Mackin JG, Owen HM, Collier A (1950) Preliminary note on the occurrence of a new protistian parasite, Dermocystidium marinum n. sp. in Crassostrea virginica (Gmelin). Science 111:328–329. doi:10.1126/science.111.2883.328

    Article  Google Scholar 

  • Mann R (2000) Restoring the oyster reef communities in the Chesapeake Bay: a commentary. J Shellfish Res 19:335–339

    Google Scholar 

  • Marshall N (1954) Changes in the physiography of oyster bars in the James River, Virginia. Conv Add Proc Natl Shellfish Assoc 1953:113–122

    Google Scholar 

  • Nixon SW, Granger S, Buckley BA, Lamont M, Rowell B (2004) A one hundred and seventeen year coastal water temperature record from Woods Hole, Massachusetts. Estuaries 27:397–404

    Article  Google Scholar 

  • O’Farrell CL, La Peyre JF, Paynter KT, Burreson EM (2000) Osmotic tolerance and volume regulation in in vitro cultures of the oyster pathogen Perkinsus marinus. J Shellfish Res 19:139–145

    Google Scholar 

  • Paraso MC, Ford SE, Powell EN, Hofmann EE, Klinck JM (1999) Modeling the MSX parasite in eastern oyster (Crassostrea virginica) populations. II. Salinity effects. J Shellfish Res 18:501–516

    Google Scholar 

  • Powell EN, Gauthier JD, Wilson EA, Nelson A, Fay RR, Brooks JM (1992) Oyster disease and climate change. Are yearly changes in Perkinsus marinus parasitism in oysters (Crassostrea virginica) controlled by climatic cycles in the Gulf of Mexico? PSZNI Mar Ecol 13:243–270. doi:10.1111/j.1439-0485.1992.tb00354.x

  • Powell EN, Klinck JM, Hofmann EE (1996) Modeling diseased oyster populations. II. Triggering mechanisms for Perkinsus marinus epizootics. J Shellfish Res 15:141–165

    Google Scholar 

  • Powell EN, Klinck JM, Ford SE, Hofmann EE, Jordan SJ (1999) Modeling the MSX parasite in eastern oyster (Crassostrea virginica) populations. III. Regional application and the problem of transmisssion. J Shellfish Res 18:517–537

    Google Scholar 

  • Powell EN, Klinck JM, Hofmann EE, McManus MA (2003) The influence of water allocation and freshwater inflow on oyster populations: a hydrodynamic-oyster population model for Galveston Bay, Texas. Environ Manage 31:100–121. doi:10.1007/s00267-002-2695-6

    Article  Google Scholar 

  • Powell EN, Klinck JM (2007) Is oyster shell a sustainable estuarine resource? J Shellfish Res 26:181–194. doi:10.2983/0730-8000(2007)26[181:IOSASE]2.0.CO;2

    Article  Google Scholar 

  • Quayle RG, Peterson TC, Basist AN, Godfrey CS (1999) An operational near real time global temperature index. Geophys Res Lett 26:73–87. doi:10.1029/1998GL900297

    Article  Google Scholar 

  • Ragone Calvo LM, Wetzel RL, Burreson EM (2001) Development and verification of a model for the population dynamics of the protistan parasite, Perkinsus marinus, within its host, the eastern oyster, Crassostrea virginica, in Chesapeake Bay. J Shellfish Res 20:231–241

    Google Scholar 

  • Ray SM (1966) A review of the culture method for detecting Dermocystidium marinum, with suggested modifications and precautions. Proc Natl Shellfish Assoc 54:55–69

    Google Scholar 

  • Ray SM (1987) Appendix E. Salinity requirements of the American oyster, Crassostrea virginica. In: Mueller AJ, Matthews GA (eds) Freshwater inflow needs of the Matagorda Bay system with focus on the needs of penaeid shrimp. NOAA Tech. Mem. NMFS-SEFC-189

  • Ropelewski CF, Halpert MS (1986) North American precipitation and temperature patterns associated with the El Niño/Southern Oscillation (ENSO). Mon Weather Rev 114:2352–2362. doi:10.1175/1520-0493(1986)114<2352:NAPATP>2.0.CO;2

    Article  Google Scholar 

  • Rothschild BJ, Ault JS, Goulletquer P, Héral M (1994) Decline of the Chesapeake Bay oyster populations: a century of habitat destruction and overfishing. Mar Ecol Prog Ser 111:29–39. doi:10.3354/meps111029

    Article  Google Scholar 

  • Schöne BR, Page NA, Rodland DL, Fiebig J, Baier S, Helama SO et al (2007) ENSO-coupled precipitation records (1959–2004) based on shells of freshwater bivalve mollusks (Margaritifera falcata) from British Columbia. Int J Earth Sci 96:525–540. doi:10.1007/s00531-006-0109-3

    Article  Google Scholar 

  • Schoener A, Tufts DF (1987) Changes in oyster condition index with El Niño-Southern Oscillation events at 46°N in an eastern Pacific Bay. J Geophys Res 92:14420–14435. doi:10.1029/JC092iC13p14429

    Google Scholar 

  • Smith TM, Reynolds RW (2005) A global merged land air and sea surface temperature reconstruction based on historical observations (1880–1997). J Clim 18:2021–2036

    Article  Google Scholar 

  • Sokal RR, Oden NL (1978) Spatial autocorrelation in biology. 1. Methodology. Biol J Linn Soc 10:199–228. doi:10.1111/j.1095-8312.1978.tb00013.x

    Article  Google Scholar 

  • Soniat TM (1985) Changes in levels of infection of oysters by Perkinsus marinus, with special reference to the interaction of temperature and salinity upon parasitism. NE Gulf Sci 7:171–174

    Google Scholar 

  • Soniat TM (1996) Epizootiology of Perkinsus marinus disease of eastern oysters in the Gulf of Mexico. J Shellfish Res 15:35–43

    Google Scholar 

  • Soniat TM, Powell EN, Hofmann EE, Klinck JM (1998) Understanding the success and failure of oyster populations: the importance of sampled variables and sample timing. J Shellfish Res 17:1149–1165

    Google Scholar 

  • Soniat TM, Finelli CM, Ruiz JT (2004) Vertical structure and predator refuge mediate oyster reef development and community dynamics. J Exp Mar Biol Ecol 310:163–182. doi:10.1016/j.jembe.2004.04.007

    Article  Google Scholar 

  • Soniat TM, Klinck JM, Powell EN, Hofmann EE (2005) Understanding the success and failure of oyster populations: climatic cycles and Perkinsus marinus. J Shellfish Res 24:83–93

    Google Scholar 

  • Sprague V (1978) Comments on trends in research on parasitic diseases of shellfish and fish. Mar Fish Rev 40:26–30

    Google Scholar 

  • Strang G (1994) Wavelets. Am Sci 82:250–255

    Google Scholar 

  • Stephenson MF, McGladdery SE, Maillet M, Veniot A, Meyer G (2003) First reported occurrence of MSX in Canada. J Shellfish Res 22:355

    Google Scholar 

  • Stokes NA, Siddall ME, Burreson EM (1995) Detection of Haplosporidium nelsoni (Haplospodidia: Haplosporidiidae) in oysters by PCR amplification. Dis Aquat Organ 23:145–152. doi:10.3354/dao023145

    Article  Google Scholar 

  • Torrence C, Compo GP (1998) A practical guide to wavelet analysis. Bull Am Meteorol Soc 79:61–78. doi:10.1175/1520-0477(1998)079<0061:APGTWA>2.0.CO;2

    Article  Google Scholar 

  • Trenberth KE (1984) Signal versus noise in the Southern Oscillation. Mon Weather Rev 112:326–332. doi:10.1175/1520-0493(1984)112<0326:SVNITS>2.0.CO;2

    Article  Google Scholar 

  • van Sickle VR, Barrett BB, Ford TB, Gulick LJ (1976) Barataria Basin: salinity changes and oyster distribution. Sea Grant Publ LSU-T-76.02, LWFC Tech Bull No 20, 22 p

  • Visbeck MH, Hurrell JW, Polvani L, Cullen HM (2001) The North Atlantic Oscillation: past, present, and future. Proc Natl Acad Sci USA 98:12876–12877. doi:10.1073/pnas.231391598

    Article  Google Scholar 

  • Wong K-C (1995) On the relationship between long-term salinity variation and river discharge in the middle reach of the Delaware estuary. J Geophys Res 100:20705–20713. doi:10.1029/95JC01406

    Google Scholar 

  • Woods H, Hargis WJ Jr, Hershner CH, Mason P (2005) Disappearance of the natural emergent 3-dimensional oyster reef system of the James River, Virginia, 1871–1948. J Shellfish Res 24:139–142

    Google Scholar 

  • Yee A, Dungan C, Hamilton R, Goedken M, de Guise S, Sunila I (2005) Apoptosis of the protozoan pathogen Perkinsus marinus in vivo and in vitro in the Chesapeake Bay and Long Island Sound. J Shellfish Res 24:1035–1042

    Google Scholar 

Download references

Acknowledgments

This work was funded by the Nicholls State University and the Haskin Shellfish Research Laboratory of Rutgers University; computer resources and facilities were provided by the Center for Coastal Physical Oceanography at Old Dominion University. The Delaware Bay time series are provided by funds from the State of New Jersey. The series is funded under the aegis of the Oyster Industry Science Steering Committee, a standing subcommittee of the Delaware Bay section of the Shellfisheries Council. Susan Ford provided information on the distribution of parasites along the Atlantic coast. The paper was improved by the helpful suggestions of two anonymous reviewers. The authors appreciate this assistance.

Author information

Author notes

  1. Thomas M. Soniat

    Present address: Department of Biological Sciences, University of New Orleans, Lakefront, New Orleans, LA, 70148, USA

Authors and Affiliations

  1. Department of Biological Sciences, Nicholls State University, Thibodaux, LA, 70310, USA

    Thomas M. Soniat

  2. Center for Coastal Physical Oceanography, Old Dominion University, Norfolk, VA, 23529, USA

    Eileen E. Hofmann & John M. Klinck

  3. Haskin Shellfish Research Laboratory, Rutgers, The State University of New Jersey, Port Norris, NJ, 08349, USA

    Eric N. Powell

Authors
  1. Thomas M. Soniat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eileen E. Hofmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John M. Klinck
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric N. Powell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas M. Soniat.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soniat, T.M., Hofmann, E.E., Klinck, J.M. et al. Differential modulation of eastern oyster (Crassostrea virginica) disease parasites by the El-Niño-Southern Oscillation and the North Atlantic Oscillation. Int J Earth Sci (Geol Rundsch) 98, 99–114 (2009). https://doi.org/10.1007/s00531-008-0364-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00531-008-0364-6

Keywords

Search

Navigation