Oceanography The Official Magazine of
The Oceanography Society
Volume 31 Issue 02

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Volume 31, No. 2
Pages 182 - 193

Marine Host-Pathogen Dynamics: Influences of Global Climate Change

Rebecca E. CohenChase C. JamesAllison LeeMaurizio M. MartinelliWendy T. MuraokaMikayla OrtegaRachel SadowskiLark StarkeyAngela R. SzesciorkaSonya E. TimkoElliot L. WeissPeter J.S. Franks
Article Abstract

Host-pathogen relationships are an important subset of interspecies interactions that are capable of influencing population dynamics, community structure, and biogeochemical cycles. Relationships between hosts and pathogens are expected to shift in response to global climate change. Atmospheric and oceanic warming is already affecting many ecosystems, perhaps most markedly those in marine environments. Case studies illustrate some impacts ocean warming is having on marine host-pathogen dynamics, including: (1) increased host stress, (2) increased pathogen virulence, (3) pathogen range expansion, and (4) host range changes. Output from global climate models was used to calculate the number of additional months each year that various coastal regions around the globe may reach temperatures above a given threshold 50 and 100 years from now; for the Arctic region, we characterize changes in sea ice cover. Complex interactions between multiple ocean conditions that could also affect host-pathogen relationships, such as rising sea surface temperature, anoxia, ocean acidification, and stratification, should also be investigated.


Cohen, R.E., C.C. James, A. Lee, M.M. Martinelli, W.T. Muraoka, M. Ortega, R. Sadowski, L. Starkey, A.R. Szesciorka, S.E. Timko, E.L. Weiss, and P.J.S. Franks. 2018. Marine host-pathogen dynamics: Influences of global climate change. Oceanography 31(2):182–193, https://doi.org/10.5670/oceanog.2018.201.


Agatsuma, Y. 2007. Ecology of Strongylocentrotus intermedius. Pp. 427–441 in Edible Sea Urchins: Biology and Ecology, 2nd ed. J.M. Lawrence, ed., Elsevier Science, Amsterdam.

Auld, S., and M.C. Tinsley. 2015. The evolutionary ecology of complex lifecycle parasites: Linking phenomena with mechanisms. Heredity 114(2):125–132, https://doi.org/10.1038/hdy.2014.84.

Banks, P., M. Berrigan, A. Choudhury, L. Craig, D. Diaz, F. Kern, J. King, M. Marshall, L. Robinson, F. Steimle, and others. 2007. Status Review of the Eastern Oyster (Crassostrea virginica). Report to the National Marine Fisheries Service, Northeast Regional Office, Gloucester, MA, USA, NOAA Technical Memo NMFS F/SPO-88, 105 pp.

Becker, P.T., E. Egea, and I. Eeckhaut. 2008. Characterization of the bacterial communities associated with the bald sea urchin disease of the echinoid Paracentrotus lividus. Journal of Invertebrate Pathology 98(2):136–147, https://doi.org/10.1016/​j.jip.2007.12.002.

Ben-Haim, Y., F.L. Thompson, C.C. Thompson, M.C. Cnockaert, B. Hoste, J. Swings, and E. Rosenberg. 2003a. Vibrio coralliilyticus sp nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. International Journal of Systematic and Evolutionary Microbiology 53:309–315, https://doi.org/10.1099/ijs.0.02402-0.

Ben-Haim, Y., M. Zicherman-Keren, and E. Rosenberg. 2003b. Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Applied and Environmental Microbiology 69(7):4,236–4,242, https://doi.org/10.1128/AEM.69.7.4236-4242.2003.

Berkelmans, R. 2002. Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Marine Ecology Progress Series 229:73–82, https://doi.org/10.3354/meps229073.

Bidegain, G., E.N. Powell, T. Klinck, T. Ben-Horin, and E.E. Hofmann. 2016. Marine infectious disease dynamics and outbreak thresholds: Contact transmission, pandemic infection, and the potential role of filter feeders. Ecosphere 7(4):e01286, https://doi.org/10.1002/ecs2.1286.

Boudouresque, C.F., and M. Verlaque. 2007. Ecology of Paracentrotus lividus. Pp. 243–285 in Edible Sea Urchins: Biology and Ecology, 2nd ed. J.M. Lawrence, ed., Elsevier Science, Amsterdam.

Bourne, D.G., M. Garren, T.M. Work, E. Rosenberg, G.W. Smith, and C.D. Harvell. 2009. Microbial disease and the coral holobiont. Trends in Microbiology 17(12):554–562, https://doi.org/​10.1016/j.tim.2009.09.004.

Bourne, D.G., and C.B. Munn. 2005. Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environmental Microbiology 7(8):1,162–1,174.

Bower, S.M. 2013. Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: Perkinsus marinus (“Dermo” Disease) of Oysters. Fisheries and Oceans Canada, http://www.dfo-mpo.gc.ca/science/aah-saa/diseases-maladies/​pmdoy-eng.html.

Bower, S.M., S.E. McGladdery, and I.M. Price. 1994. Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annual Review of Fish Diseases 4(0):1–199, https://doi.org/​10.1016/0959-8030(94)90028-0.

Brothers, C.J., J. Harianto, J.B. McClintock, and M. Byrne. 2016. Sea urchins in a high-CO2 world: The influence of acclimation on the immune response to ocean warming and acidification. Proceedings of the Royal Society B, https://doi.org/​10.1098/rspb.2016.1501.

Burge, C.A., C.M. Eakin, C.S. Friedman, B. Froelich, P.K. Hershberger, E.E. Hofmann, L.E. Petes, K.C. Prager, E. Weil, B.L. Willis, and others. 2014. Climate change influences on marine infectious diseases: Implications for management and society. Annual Review of Marine Science 6:249–277, https://doi.org/10.1146/annurev-marine-010213-135029.

Combosch, D.J., and S.V. Vollmer. 2011. Population genetics of an ecosystem-defining reef coral Pocillopora damicornis in the tropical eastern Pacific. PLoS ONE 6(8): e21200, https://doi.org/​10.1371/journal.pone.0021200.

Cook, T., M. Folli, J. Klinck, S. Ford, and J. Miller. 1998. The relationship between increasing sea-surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuarine Coastal and Shelf Science 46(4):587–597, https://doi.org/10.1006/ecss.1997.0283.

Danovaro, R., C. Corinaldesi, A. Dell’Anno, J.A. Fuhrman, J.J. Middelburg, R.T. Noble, and C.A. Suttle. 2011. Marine viruses and global climate change. FEMS Microbiology Reviews 35(6):993–1,034, https://doi.org/10.1111/​j.1574-6976.2010.00258.x.

D’Croz, L., and J.L. Maté. 2004. Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama. Coral Reefs 23:473–483, https://doi.org/​10.1007/s00338-004-0397-7.

de Figueiredo, P., T.A. Ficht, A. Rice-Ficht, C.A. Rossetti, and L.G. Adams. 2015. Pathogenesis and immunobiology of Brucellosis: Review of Brucella-host interactions. The American Journal of Pathology 185(6):1,505–1,517, https://doi.org/​10.1016/​j.ajpath.2015.03.003.

de Montaudouin, X., I. Paul-Pont, C. Lambert, P. Gonzalez, N. Raymond, F. Jude, A. Legeay, M. Baudrimont, C. Dang, F. Le Grand, and others. 2010. Bivalve population health: Multistress to identify hot spots. Marine Pollution Bulletin 60(8):1,307–1,318, https://doi.org/10.1016/​j.marpolbul.2010.03.011.

Doney, S.C., M. Ruckelshaus, J.E. Duffy, J.P. Barry, F. Chan, C.A. English, H.M. Galindo, J.M. Grebmeier, A.B. Hollowed, N. Knowlton, and others. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science 4:11–37, https://doi.org/10.1146/annurev-marine-041911-111611.

Dove, S., and O. Hoegh-Guldberg. 2006. The cell physiology of coral bleaching. Pp. 55–71 in Coral Reefs and Climate Change: Science and Management. J.T. Phinney, O. Hoegh-Guldberg, J. Kleypas, W. Skirving, and A. Strong, eds, American Geophysical Union, Washington, DC.

Farmanfarmaian, A., and A.C. Giese. 1963. Thermal tolerance and acclimation in the western purple sea urchin, Strongylocentrotus purpuratus. Physical and Biochemical Zoology 36(3):237–243, https://doi.org/10.1086/physzool.36.3.30152309.

Ford, S.E., and E. Smolowitz. 2007. Infection dynamics of an oyster parasite in its newly expanded range. Marine Biology 151(1):119–133, https://doi.org/​10.1007/s00227-006-0454-6.

Fuhrman, J.A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548, https://doi.org/10.1038/21119.

Garren, M., K. Son, J.B. Raina, R. Rusconi, F. Menolascina, O.H. Shapiro, J. Tout, D.G. Bourne, J.R. Seymour, and R. Stocker. 2014. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME Journal 8(5):999–1,007, https://doi.org/10.1038/ismej.2013.210.

Garren, M., K. Son, J. Tout, J.R. Seymour, and R. Stocker. 2016. Temperature-induced behavioral switches in a bacterial coral pathogen. ISME Journal 10(6):1,363–1,372, https://doi.org/10.1038/ismej.2015.216.

Girard, D., S. Clemente, K. Toledo-Guedes, A. Brito, and J.C. Hernandez. 2012. A mass mortality of subtropical intertidal populations of the sea urchin Paracentrotus lividus: Analysis of potential links with environmental conditions. Marine Ecology 33(3):377–385, https://doi.org/​10.1111/j.1439-0485.2011.00491.x.

Gnanadesikan, A., K.W. Dixon, S.M. Griffies, V. Balaji, M. Barreiro, J.A. Beesley, W.F. Cooke, T.L. Delworth, R. Gerdes, M.J. Harrison, and others. 2006. GFDL’s CM2 global coupled climate models: Part II. The baseline ocean simulation. Journal of Climate 19(5):675–697, https://doi.org/10.1175/JCLI3630.1.

Grenfell, B.T., and A.P. Dobson, eds. 1995. Ecology of Infectious Diseases in Natural Populations. Cambridge University Press, 536 pp.

Harvell, C.D., C.E. Mitchell, J.R. Ward, S. Altizer, A.P. Dobson, R.S. Ostfeld, and M.D. Samuel. 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296(5576):2,158–2,162, https://doi.org/10.1126/science.1063699.

Heron, S.F., J.A. Maynard, R. van Hooidoin, and C.M. Eakin. 2016. Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Scientific Reports 6:38402, https://doi.org/10.1038/srep38402.

Hoeksema, B.W., A. Rogers, and M.C. Quibilan. 2014. Pocillopora damicornis. The IUCN Red List of Threatened Species, https://doi.org/10.2305/IUCN.UK.2014-1.RLTS.T133222A54216898.en.

Hughes, T.P., J.T. Kerry, M. Alvarez-Noriega, J.G. Alvarez-Romero, K.D. Anderson, A.H. Baird, R.C. Babcock, M. Beger, D.R. Bellwood, R. Berkelmans, and others. 2017. Global warming and recurrent mass bleaching of corals. Nature 543(7645):373–377, https://doi.org/10.1038/nature21707.

Holt, R.A., A. Amandi, J.S. Rohovec, and J.L. Fryer. 1989. Relation of water temperature to bacterial cold-water disease in coho salmon, Chinook salmon, and rainbow trout. Journal of Aquatic Animal Health 1(2):94–101, https://doi.org/​10.1577/​1548-8667(1989)001<0094:ROWTTB>2.3.CO;2.

IPCC. 2007. Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Core Writing Team, R.K. Pachauri, and A. Reisinger, eds, IPCC, Geneva, Switzerland, 104 pp.

IPCC. 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Core Writing Team, R.K. Pachauri, and L.A. Meyer, eds, IPCC, Geneva, Switzerland, 151 pp.

Jangoux, M. 1987. Diseases of Echinodermata: Part 1. Agents, microorganisms and protistans. Diseases of Aquatic Organisms 2(2):147–162, https://doi.org/​10.3354/dao002147.

Jangoux, M. 1990. Diseases of Echinodermata. Chapter 5 in Diseases of Marine Animals. Volume III. Introduction. Cephalopoda, Annelida, Crustacea, Chaetognatha, Echinodermata, Urochordata. O. Kinne, ed., Biologische Anstalt Helgoland, Hamburg.

Jenkins, C., P. Hick, M. Gabor, Z. Spiers, S.A. Fell, X.N. Gu, A. Read, J. Go, M. Dove, W. O’Connor, and others. 2013. Identification and characterisation of an ostreid herpesvirus-1 microvariant (OsHV-1 mu-var) in Crassostrea gigas (Pacific oysters) in Australia. Diseases of Aquatic Organisms 105(2):109–126, https://doi.org/10.3354/dao02623.

Karvonen, A., P. Rintamaki, J. Jokela, and E.T. Valtonen. 2010. Increasing water temperature and disease risks in aquatic systems: Climate change increases the risk of some, but not all, diseases. International Journal for Parasitology 40(13):1,483–1,488, https://doi.org/​10.1016/j.ijpara.2010.04.015.

Kimes, N.E., C.J. Grim, W.R. Johnson, N.A. Hasan, B.D. Tall, M.H. Kothary, H. Kiss, A.C. Munk, R. Tapia, R. Green, and others. 2012. Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME Journal 6(4):835–846, https://doi.org/10.1038/ismej.2011.154.

Kordas, R.L., C.D.G. Harley, and M.I. O’Connor. 2011. Community ecology in a warming world: The influence of temperature on interspecific interactions in marine systems. Journal of Experimental Marine Biology and Ecology 400(1–2):218–226, https://doi.org/10.1016/j.jembe.2011.02.029.

Kovacs, K.M., C. Lydersen, J.E. Overland, and S.E. Moore. 2011. Impacts of changing sea-ice conditions on Arctic marine mammals. Marine Biodiversity 41(1):181–194, https://doi.org/10.1007/s12526-010-0061-0.

La Peyre, M.K., S.M. Casas, A. Villalba, and J.F. La Peyre. 2008. Determination of the effects of temperature on viability, metabolic activity and proliferation of two Perkinsus species, and its significance to understanding seasonal cycles of perkinsosis. Parasitology 135(4):505–519, https://doi.org/​10.1017/​S0031182008004150.

Lambourn, D., M. Garner, D. Ewalt, S. Raverty, I. Sidor, S.J. Jeffries, J. Rhyan, and J.K. Gaydos. 2013. Brucella pinnipedialis infections in Pacific harbor seals (Phoca vitulina Richardsi) from Washington state, USA. Journal of Wildlife Diseases 49(4):802–815, https://doi.org/​10.7589/​2012-05-137.

Lester, S.E., E.D. Tobin, and M.D. Behrens. 2007. Disease dynamics and the potential role of thermal stress in the sea urchin, Strongylocentrotus purpuratus. Canadian Journal of Fisheries and Aquatic Sciences 64(2)314–323, https://doi.org/10.1139/f07-010.

Maes, P., and M. Jangoux. 1984. The bald-sea-urchin disease: A biopathological approach. Helgolander Meeresuntersuchungen 37(1–4):217–224, https://doi.org/10.1007/BF01989306.

Maynard, J., R. van Hooidonk, C.D. Harvell, C.M. Eakin, G. Liu, B.L. Willis, G.J. Williams, M.L. Groner, A. Dobson, S.F. Heron, and others. 2016. Improving marine disease surveillance through sea temperature monitoring, outlooks and projections. Philosophical Transactions of the Royal Society B 371:20150208, https://doi.org/​10.1098/​rstb.2015.0208.

Meehl, G.A., C. Covey, K.E. Taylor, T. Delworth, R.J. Stouffer, M. Latif, B. McAvaney, and J.F. Mitchell. 2007. The WCRP CMIP3 multimodel dataset: A new era in climate change research. Bulletin of the American Meteorological Society 88(9):1,383–1,394, https://doi.org/10.1175/BAMS-88-9-1383.

Nymo, I.H., M. Tryland, and J. Godfroid. 2011. A review of Brucella infection in marine mammals, with special emphasis on Brucella pinnipedialis in the hooded seal (Cystophora cristata). Veterinary Research 42:13, https://doi.org/​10.1186/​1297-9716-42-93.

Pollock, F.J., B. Wilson, W.R. Johnson, P.J. Morris, B.L. Willis, and D.G. Bourne. 2010. Phylogeny of the coral pathogen Vibrio coralliilyticus. Environmental Microbiology Reports 2(1):172–178, https://doi.org/​10.1111/j.1758-2229.2009.00131.x.

Pompa, S., P.R. Ehrlich, and G. Ceballos. 2011. Global distribution and conservation of marine mammals. Proceedings of the National Academy of Sciences of the United States of America 108(38):13,600–13,605, https://doi.org/10.1073/pnas.1101525108.

Roeckner, E., R. Brokopf, M. Esch, M. Giorgetta, S. Hagemann, L. Kornblueh, E. Manzini, U. Schlese, and U. Schulzweida. 2004. The Atmospheric General Circulation Model ECHAM5 Part II. Max-Planck Institut für Meterologie, Hamburg, Germany, 127 pp.

Scheibling, R.E., and R.L. Stephenson. 1984. Mass mortality of Strongylocentrotus droebachiensis (echinodermata, echinoidea) off Nova Scotia, Canada. Marine Biology 78(2):153–164, https://doi.org/​10.1007/​BF00394695.

Scholz, H.C., Z. Hubalek, J. Nesvadbova, H. Tomaso, G. Vergnaud, P. Le Fleche, A.M. Whatmore, S. Al Dahouk, M. Kruger, C. Lodri, and M. Pfeffer. 2008. Isolation of Brucella microti from soil. Emerging Infectious Diseases 14(8):1,316–1,317, https://doi.org/10.3201/eid1408.080286.

Segarra, A., J.F. Pepin, I. Arzul, B. Morga, N. Faury, and T. Renault. 2010. Detection and description of a particular Ostreid herpesvirus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Research 153(1):92–99, https://doi.org/​10.1016/​j.virusres.2010.07.011.

Simpkins, M.A., L.M. Hiruki-Raring, G. Sheffield, J.M. Grebmeier, and J.L. Bengtson. 2003. Habitat selection by ice-associated pinnipeds near St. Lawrence Island, Alaska in March 2001. Polar Biology 26(9):577–­586, https://doi.org/10.1007/s00300-003-0527-7.

Soudant, P., F.L.E. Chu, and A. Volety. 2013. Host-parasite interactions: Marine bivalve molluscs and protozoan parasites, Perkinsus species. Journal of Invertebrate Pathology 114(2):196–216, https://doi.org/​10.1016/j.jip.2013.06.001.

Spickler, A.R. 2009. Brucellosis in Marine Mammals. Last updated July 2009, 7 pp., http://www.cfsph.iastate.edu/Factsheets/pdfs/brucellosis_marine.pdf.

Sunila, I. 2007. Dermo Disease, http://www.ct.gov/doag/lib/doag/aquaculture/dermo.pdf.

Suttle, C.A. 2007. Marine viruses: Major players in the global ecosystem. Nature Reviews Microbiology 5(10):801–812, https://doi.org/10.1038/nrmicro1750.

Sweet, M., M. Bulling, and J.E. Williamson. 2016. New disease outbreak affects two dominant sea urchin species associated with Australian temperate reefs. Marine Ecology Progress Series 551:171–183, https://doi.org/10.3354/meps11750.

Thakur, S.D., R.K. Vaid, A.K. Panda, and Y. Saini. 2012. Marine mammal brucellosis: A new dimension to an old zoonosis. Current Science 103(8):902–910.

The Center for Food Security & Public Health. 2009. Brucellosis in Marine Mammals. The Center for Food Security & Public Health, Iowa State University, 7 pp., http://www.cfsph.iastate.edu/Factsheets/pdfs/brucellosis_marine.pdf.

Thompson, C.C., F.L. Thompson, A.C.P. Vicente, and J. Swings. 2007. Phylogenetic analysis of Vibrios and related species by means of atpA gene sequences. International Journal of Systematic and Evolutionary Microbiology 57:2,480–2,484, https://doi.org/10.1099/ijs.0.65223-0.

Tout, J., N. Siboni, L.F. Messer, M. Garren, R. Stocker, N.S. Webster, P.J. Ralph, and J.R. Seymour. 2015. Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis. Frontiers in Microbiology 6:432, https://doi.org/10.3389/fmicb.2015.00432.

Towell, R., and R. Ream. 2015. Bogoslof Island Research: 2015. National Oceanic and Atmospheric Administration, NOAA Alaska Fisheries Science Center Quarterly Report.

Vezzulli, L., R.R. Colwell, and C. Pruzzo. 2013. Ocean warming and spread of pathogenic Vibrios in the aquatic environment. Microbial Ecology 65(4):817–825, https://doi.org/10.1007/s00248-012-0163-2.

Vizcaino, M.I., W.R. Johnson, N.E. Kimes, K. Williams, M. Torralba, K.E. Nelson, G.E. Smith, E. Weil, P.D.R. Moeller, and P.J. Morris. 2010. Antimicrobial resistance of the coral pathogen Vibrio coralliilyticus and Caribbean sister phylotypes isolated from a diseased octocoral. Microbial Ecology 59(4):646–657, https://doi.org/10.1007/s00248-010-9644-3.

Ward, J.R., and K.D. Lafferty. 2004. The elusive baseline of marine disease: Are diseases in ocean ecosystems increasing? PLoS Biology 2(4):542–547, https://doi.org/10.1371/journal.pbio.0020120.

Xu, F., N. Gonzalez-Escalona, J. Haendiges, R.A. Myers, J. Ferguson, T. Stiles, E. Hickey, M. Moore, J.M. Hickey, C. Schillaci, and others. 2017. Sequence type 631 Vibrio parahaemolyticus, an emerging foodborne pathogen in North America. Journal of Clinical Microbiology 55(2):645–648, https://doi.org/​10.1128/JCM.02162-16.

Young, B.G., S.H. Ferguson, and N.J. Lunn. 2015. Variation in ringed seal density and abundance in western Hudson Bay estimated from aerial surveys, 1995 to 2013. Arctic 68(3):301–309, https://doi.org/​10.14430/arctic4503.