1932

Abstract

Climate change affects ecological processes and interactions, including parasitism. Because parasites are natural components of ecological systems, as well as agents of outbreak and disease-induced mortality, it is important to summarize current knowledge of the sensitivity of parasites to climate and identify how to better predict their responses to it. This need is particularly great in marine systems, where the responses of parasites to climate variables are less well studied than those in other biomes. As examples of climate's influence on parasitism increase, they enable generalizations of expected responses as well as insight into useful study approaches, such as thermal performance curves that compare the vital rates of hosts and parasites when exposed to several temperatures across a gradient. For parasites not killed by rising temperatures, some simple physiological rules, including the tendency of temperature to increase the metabolism of ectotherms and increase oxygen stress on hosts, suggest that parasites’ intensity and pathologies might increase. In addition to temperature, climate-induced changes in dissolved oxygen, ocean acidity, salinity, and host and parasite distributions also affect parasitism and disease, but these factors are much less studied. Finally, because parasites are constituents of ecological communities, we must consider indirect and secondary effects stemming from climate-induced changes in host–parasite interactions, which may not be evident if these interactions are studied in isolation.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-031920-100429
2021-01-03
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/marine/13/1/annurev-marine-031920-100429.html?itemId=/content/journals/10.1146/annurev-marine-031920-100429&mimeType=html&fmt=ahah

Literature Cited

  1. Altman I, Byers JE. 2014. Large-scale spatial variation in parasite communities influenced by anthropogenic factors. Ecology 95:1876–87
    [Google Scholar]
  2. Baker-Austin C, Trinanes JA, Taylor NGH, Hartnell R, Siitonen A, Martinez-Urtaza J 2013. Emerging Vibrio risk at high latitudes in response to ocean warming. Nat. Clim. Change 3:73–77
    [Google Scholar]
  3. Bates AE, Hilton BJ, Harley CDG 2009. Effects of temperature, season and locality on wasting disease in the keystone predatory sea star Pisaster ochraceus. Dis. Aquat. Organ 86:245–51
    [Google Scholar]
  4. Ben-Horin T, Lenihan HS, Lafferty KD 2013. Variable intertidal temperature explains why disease endangers black abalone. Ecology 94:161–68
    [Google Scholar]
  5. Berkhout BW, Lloyd MM, Poulin R, Studer A 2014. Variation among genotypes in responses to increasing temperature in a marine parasite: evolutionary potential in the face of global warming. ? Int. J. Parasitol. 44:1019–27
    [Google Scholar]
  6. Bermingham ML, Mulcahy MF. 2004. Environmental risk factors associated with amoebic gill disease in cultured salmon, Salmo salar L., smolts in Ireland. J. Fish Dis. 27:555–71
    [Google Scholar]
  7. Bibby R, Widdicombe S, Parry H, Spicer J, Pipe R 2008. Effects of ocean acidification on the immune response of the blue mussel Mytilus edulis. Aquat. Biol 2:67–74
    [Google Scholar]
  8. Birkbeck TH, Feist SW, Verner-Jeffreys DW 2011. Francisella infections in fish and shellfish. J. Fish Dis. 34:173–87
    [Google Scholar]
  9. Blakeslee AMH, Byers JE. 2008. Using parasites to inform ecological history: comparisons among three congeneric marine snails. Ecology 89:1068–78
    [Google Scholar]
  10. Blakeslee AMH, Byers JE, Lesser MP 2008. Solving cryptogenic histories using host and parasite molecular genetics: the resolution of Littorina littorea’s North American origin. Mol. Ecol. 17:3684–96
    [Google Scholar]
  11. Blakeslee AMH, Fowler AE, Keogh CL 2013. Marine invasions and parasite escape: updates and new perspectives. Adv. Mar. Biol. 66:87–169
    [Google Scholar]
  12. Blanar CA, Marcogliese DJ, Couillard CM 2011. Natural and anthropogenic factors shape metazoan parasite community structure in mummichog (Fundulus heteroclitus) from two estuaries in New Brunswick, Canada. Folia Parasitol 58:240–48
    [Google Scholar]
  13. Boyett HV, Bourne DG, Willis BL 2007. Elevated temperature and light enhance progression and spread of black band disease on staghorn corals of the Great Barrier Reef. Mar. Biol. 151:1711–20
    [Google Scholar]
  14. Breitburg DL, Hondorp DW, Audemard C, Carnegie RB, Burrell RB et al. 2015. Landscape-level variation in disease susceptibility related to shallow-water hypoxia. PLOS ONE 10:e0116223
    [Google Scholar]
  15. Breitburg DL, Hondorp DW, Davias LA, Diaz RJ 2009. Hypoxia, nitrogen, and fisheries: integrating effects across local and global landscapes. Annu. Rev. Mar. Sci. 1:329–49
    [Google Scholar]
  16. Bricknell IR, Dalesman SJ, O'Shea B, Pert CC, Luntz AJM 2006. Effect of environmental salinity on sea lice Lepeophtheirus salmonis settlement success. Dis. Aquat. Organ. 71:201–12
    [Google Scholar]
  17. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL et al. 2007. Thermal stress and coral cover as drivers of coral disease outbreaks. PLOS Biol 5:e124
    [Google Scholar]
  18. Burge CA, Eakin CM, Friedman CS, Froelich B, Hershberger PK et al. 2014. Climate change influences on marine infectious diseases: implications for management and society. Annu. Rev. Mar. Sci. 6:249–77
    [Google Scholar]
  19. Burkholder JM, Glasgow HB. 1997. Pfiesteria piscicida and other Pfiesteria-like dinoflagellates: behavior, impacts, and environmental controls. Limnol. Oceanogr. 42:1052–75
    [Google Scholar]
  20. Byers JE, Altman I, Grosse AM, Huspeni TC, Maerz JC 2011. Using parasitic trematode larvae to quantify an elusive vertebrate host. Conserv. Biol. 25:85–93
    [Google Scholar]
  21. Byers JE, Blakeslee AMH, Linder E, Cooper AB, Maguire TJ 2008. Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89:439–51
    [Google Scholar]
  22. Byers JE, Cuddington K, Jones CG, Talley TS, Hastings A et al. 2006. Using ecosystem engineers to restore ecological systems. Trends Ecol. Evol. 21:493–500
    [Google Scholar]
  23. Byers JE, Holmes ZC, Blakeslee AMH 2016. Consistency of trematode infection prevalence in host populations across large spatial and temporal scales. Ecology 97:1643–49
    [Google Scholar]
  24. Byers JE, Malek AJ, Quevillon LE, Altman I, Keogh CL 2015a. Opposing selective pressures decouple pattern and process of parasitic infection over small spatial scale. Oikos 124:1511–19
    [Google Scholar]
  25. Byers JE, Smith RS, Pringle JM, Clark GF, Gribben PE et al. 2015b. Invasion expansion: time since introduction best predicts global ranges of marine invaders. Sci. Rep. 5:12436
    [Google Scholar]
  26. Callaway R, Shinn AP, Grenfell SE, Bron JE, Burnell G et al. 2012. Review of climate change impacts on marine aquaculture in the UK and Ireland. Aquat. Conserv. 22:389–421
    [Google Scholar]
  27. Carlson CJ, Burgio KR, Dougherty ER, Phillips AJ, Bueno VM et al. 2017. Parasite biodiversity faces extinction and redistribution in a changing climate. Sci. Adv. 3:e1602422
    [Google Scholar]
  28. Carroll JM, O'Shaughnessy KA, Diedrich GA, Finelli CM 2015. Are oysters being bored to death? Influence of Cliona celata on Crassostrea virginica condition, growth and survival. Dis. Aquat. Organ. 117:31–44
    [Google Scholar]
  29. Christensen OB, Christensen JH, Machenhauer B, Botzet M 1998. Very high-resolution regional climate simulations over Scandinavia—present climate. J. Clim. 11:3204–29
    [Google Scholar]
  30. Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J et al. 2015. Biodiversity inhibits parasites: broad evidence for the dilution effect. PNAS 112:8667–71
    [Google Scholar]
  31. Cizauskas CA, Carlson CJ, Burgio KR, Clements CF, Dougherty ER et al. 2017. Parasite vulnerability to climate change: an evidence-based functional trait approach. R. Soc. Open Sci. 4:160535
    [Google Scholar]
  32. Coffey AH, Li CW, Shields JD 2012. The effect of salinity on experimental infections of a Hematodinium sp. in blue crabs. Callinectes sapidus. J. Parasitol. 98:536–42
    [Google Scholar]
  33. Cohen AN, Carlton JT. 1998. Accelerating invasion rate in a highly invaded estuary. Science 279:555–58
    [Google Scholar]
  34. Cohen RE, James CC, Lee A, Martinelli MM, Muraoka WT et al. 2018. Marine host-pathogen dynamics: influences of global climate change. Oceanography 31:2182–93
    [Google Scholar]
  35. Dobson AP, Carper R. 1992. Global warming and potential changes in host-parasite and disease-vector relationships.. Global Warming and Biological Diversity RL Peters, TE Lovejoy 201–17 New Haven, CT: Yale Univ. Press
    [Google Scholar]
  36. Doney SC, Fabry VJ, Feely RA, Kleypas JA 2009. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1:169–92
    [Google Scholar]
  37. Dungan ML, Miller TE, Thomson DA 1982. Catastrophic decline of a top carnivore in the Gulf of California rocky inter-tidal zone. Science 216:989–91
    [Google Scholar]
  38. Dunn RP, Eggleston DB, Lindquist N 2014. Oyster-sponge interactions and bioerosion of reef-building substrate materials: implications for oyster restoration. J. Shellfish Res. 33:727–38
    [Google Scholar]
  39. Durack PJ, Wijffels SE, Matear RJ 2012. Ocean salinities reveal strong global water cycle intensification during 1950 to 2000. Science 336:455–58
    [Google Scholar]
  40. Eisenlord ME, Groner ML, Yoshioka RM, Elliott J, Maynard J et al. 2016. Ochre star mortality during the 2014 wasting disease epizootic: role of population size structure and temperature. Philos. Trans. R. Soc. B 371:20150212
    [Google Scholar]
  41. Ellis RP, Widdicombe S, Parry H, Hutchinson TH, Spicer JI 2015. Pathogenic challenge reveals immune trade-off in mussels exposed to reduced seawater pH and increased temperature. J. Exp. Mar. Biol. Ecol. 462:83–89
    [Google Scholar]
  42. Fels D, Kaltz O. 2006. Temperature-dependent transmission and latency of Holospora undulata, a micronucleus-specific parasite of the ciliate Paramecium caudatum. Proc. R. Soc. B 273:1031–38
    [Google Scholar]
  43. 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]
  44. Frischer ME, Fowler AE, Brunson JF, Walker AN, Powell SA et al. 2018. Pathology, effects, and transmission of black gill in commercial penaeid shrimp from the South Atlantic Bight. J. Shellfish Res. 37:149–58
    [Google Scholar]
  45. Frischer ME, Lee RF, Price AR, Walters TL, Bassette MA et al. 2017. Causes, diagnostics, and distribution of an ongoing penaeid shrimp black gill epidemic in the US South Atlantic Bight. J. Shellfish Res. 36:487–500
    [Google Scholar]
  46. Galaktionov KV. 2016. Transmission of parasites in the coastal waters of the Arctic seas and possible effect of climate change. Biol. Bull. 43:1129–47
    [Google Scholar]
  47. Galaktionov KV, Irwin SWB, Prokofiev VV, Saville DH, Nikolaev KE, Levakin IA 2006. Trematode transmission in coastal communities – temperature dependence and climate change perspectives. 11th International Congress of Parasitology – ICOPA XI85–90 Bologna, Italy: Medimond
    [Google Scholar]
  48. Gandy RL, Crowley CE, Machniak AM, Crawford CR 2011. Review of the biology and population dynamics of the blue crab, Callinectes sapidus, in relation to salinity and freshwater inflow Rep., Fla. Fish Wildl. Conserv. Comm St. Petersburg, FL:
    [Google Scholar]
  49. Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP et al. 2015. Ocean acidification through the lens of ecological theory. Ecology 96:3–15
    [Google Scholar]
  50. Gehman AM, Byers JE. 2017. Non-native parasite enhances susceptibility of host to native predators. Oecologia 183:919–26
    [Google Scholar]
  51. Gehman AM, Hall RJ, Byers JE 2018. Host and parasite thermal ecology jointly determine the effect of climate warming on epidemic dynamics. PNAS 115:744–49
    [Google Scholar]
  52. GEPD (Ga. Environ. Prot. Div.) 2003. Water quality in Georgia Rep., GEPD Atlanta, GA:
    [Google Scholar]
  53. Goedknegt MA, Welsh JE, Drent J, Thieltges DW 2015. Climate change and parasite transmission: how temperature affects parasite infectivity via predation on infective stages. Ecosphere 6:96
    [Google Scholar]
  54. Gooding EL, Kendrick MR, Brunson JF, Kingsley-Smith PR, Fowler AE et al. 2020. Black gill increases the susceptibility of white shrimp, Penaeus setiferus (Linnaeus, 1767), to common estuarine predators. J. Exp. Mar. Biol. Ecol. 524:151284
    [Google Scholar]
  55. Groner ML, Hoenig JM, Pradel R, Choquet R, Vogelbein WK et al. 2018. Dermal mycobacteriosis and warming sea surface temperatures are associated with elevated mortality of striped bass in Chesapeake Bay. Ecol. Evol. 8:9384–97
    [Google Scholar]
  56. Guilloteau P, Poulin R, MacLeod CD 2016. Impacts of ocean acidification on multiplication and caste organisation of parasitic trematodes in their gastropod host. Mar. Biol. 163:96
    [Google Scholar]
  57. Hakalahti T, Karvonen A, Valtonen ET 2006. Climate warming and disease risks in temperate regions – Argulus coregoni and Diplostomum spathaceum as case studies. J. Helminthol. 80:93–98
    [Google Scholar]
  58. Harland H, MacLeod CD, Poulin R 2015. Non-linear effects of ocean acidification on the transmission of a marine intertidal parasite. Mar. Ecol. Prog. Ser. 536:55–64
    [Google Scholar]
  59. Harland H, MacLeod CD, Poulin R 2016. Lack of genetic variation in the response of a trematode parasite to ocean acidification. Mar. Biol. 163:1
    [Google Scholar]
  60. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR et al. 1999. Emerging marine diseases—climate links and anthropogenic factors. Science 285:1505–10
    [Google Scholar]
  61. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP et al. 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–62
    [Google Scholar]
  62. Hastings A, Byers JE, Crooks JA, Cuddington K, Jones CG et al. 2007. Ecosystem engineering in space and time. Ecol. Lett. 10:153–64
    [Google Scholar]
  63. Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS 2008. Five potential consequences of climate change for invasive species. Conserv. Biol. 22:534–43
    [Google Scholar]
  64. Hines AH, Alvarez F, Reed SA 1997. Introduced and native populations of a marine parasitic castrator: variation in prevalence of the rhizocephalan Loxothylacus panopaei in xanthid crabs. Bull. Mar. Sci. 61:197–214
    [Google Scholar]
  65. 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
    [Google Scholar]
  66. Holman JD, Burnett KG, Burnett LE 2004. Effects of hypercapnic hypoxia on the clearance of Vibrio campbelli in the Atlantic blue crab, Callinectes sapidus rathbun. Biol. Bull. 206:188–96
    [Google Scholar]
  67. Hopkins SH. 1956. Notes on the boring sponges in Gulf Coast estuaries and their relation to salinity. Bull. Mar. Sci. 6:44–58
    [Google Scholar]
  68. Hopper JV, Kuris AM, Lorda J, Simmonds SE, White C, Hechinger RF 2014. Reduced parasite diversity and abundance in a marine whelk in its expanded geographical range. J. Biogeogr. 41:1674–84
    [Google Scholar]
  69. Huspeni TC, Lafferty KD. 2004. Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Ecol. Appl. 14:795–804
    [Google Scholar]
  70. IPCC (Intergov. Panel Clim. Change) 2007. Summary for policymakers. Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change S Solomon, D Qin, M Manning, Z Chen, M Marquis et al.1–18 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  71. Jensen KT, Mouritsen KN. 1992. Mass mortality in two common soft-bottom invertebrates, Hydrobia ulvae and Corophium volutator—the possible role of trematodes. Helgol. Meeresunters. 46:329–39
    [Google Scholar]
  72. Kane AS, Stine CB, Hungerford L, Matsche M, Driscoll C, Baya AM 2007. Mycobacteria as environmental portent in Chesapeake Bay fish species. Emerg. Infect. Dis. 13:329–31
    [Google Scholar]
  73. Karvonen A, Rintamaki P, Jokela J, Valtonen ET 2010. Increasing water temperature and disease risks in aquatic systems: Climate change increases the risk of some, but not all, diseases. Int. J. Parasitol. 40:1483–88
    [Google Scholar]
  74. Kim K, Harvell CD. 2004. The rise and fall of a six-year coral-fungal epizootic. Am. Nat. 164:S52–63
    [Google Scholar]
  75. Kirk D, Jones N, Peacock S, Phillips J, Molnár PK et al. 2018. Empirical evidence that metabolic theory describes the temperature dependency of within-host parasite dynamics. PLOS Biol 16:e2004608
    [Google Scholar]
  76. Kohl WT, McClure TI, Miner BG 2016. Decreased temperature facilitates short-term sea star wasting disease survival in the keystone intertidal sea star Pisaster ochraceus. . PLOS ONE 11:e0153670
    [Google Scholar]
  77. Koprivnikar J, Lim D, Fu C, Brack SHM 2010. Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitol. Res. 106:1167–77
    [Google Scholar]
  78. Korkea-Aho TL, Partanen JM, Kukkonen JVK, Taskinen J 2008. Hypoxia increases intensity of epidermal papillomatosis in roach Rutilus rutilus. Dis. Aquat. Organ 78:235–41
    [Google Scholar]
  79. Kritsky DC, Bullard SA, Bakenhaster MD 2011. First report of gastrocotylinean post-oncomiracidia (Platyhelminthes: Monogenoidea: Heteronchoinea) on gills of flyingfish (Exocoetidae), snapper (Lutjanidae), dolphinfish (Coryphaenidae), and amberjack (Carangidae) from the Gulf of Mexico: decoy hosts and the dilution effect. Parasitol. Int. 60:274–82
    [Google Scholar]
  80. Krkošek M. 2017. Population biology of infectious diseases shared by wild and farmed fish. Can. J. Fish. Aquat. Sci. 74:620–28
    [Google Scholar]
  81. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L et al. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19:1884–96
    [Google Scholar]
  82. Kroeker KJ, Sanford E, Jellison BM, Gaylord B 2014. Predicting the effects of ocean acidification on predator-prey interactions: a conceptual framework based on coastal molluscs. Biol. Bull. 226:211–22
    [Google Scholar]
  83. Kruse I, Hare MP. 2007. Genetic diversity and expanding nonindigenous range of the rhizocephalan Loxothylacus panopaei parasitizing mud crabs in the western North Atlantic. J. Parasitol. 93:575–82
    [Google Scholar]
  84. Kube J, Kube S, Dierschke V 2002. Spatial and temporal variations in the trematode component community of the mudsnail Hydrobia ventrosa in relation to the occurrence of waterfowl as definitive hosts. J. Parasitol. 88:1075–86
    [Google Scholar]
  85. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L et al. 2008. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–18
    [Google Scholar]
  86. Lafferty KD. 2017. Marine infectious disease ecology. Annu. Rev. Ecol. Evol. Syst. 48:473–96
    [Google Scholar]
  87. Lafferty KD, Dobson AP, Kuris AM 2006. Parasites dominate food web links. PNAS 103:11211–16
    [Google Scholar]
  88. Lafferty KD, Holt RD. 2003. How should environmental stress affect the population dynamics of disease. ? Ecol. Lett. 6:654–64
    [Google Scholar]
  89. Lafferty KD, Porter JW, Ford SE 2004. Are diseases increasing in the ocean. ? Annu. Rev. Ecol. Evol. Syst. 35:31–54
    [Google Scholar]
  90. Landers SC, Lee RF, Walters TL, Walker AN, Powell SA et al. 2020. Hyalophysa lynni n. sp. (Ciliophora, Apostomatida), a new pathogenic ciliate and causative agent of shrimp black gill in penaeid shrimp. Eur. J. Protistol. 73:125673
    [Google Scholar]
  91. Larsen MH, Mouritsen KN. 2009. Increasing temperature counteracts the impact of parasitism on periwinkle consumption. Mar. Ecol. Prog. Ser. 383:141–49
    [Google Scholar]
  92. Latour RJ, Gauthier DT, Gartland J, Bonzek CF, McNamee KA, Vogelbein WK 2012. Impacts of mycobacteriosis on the growth of striped bass (Morone saxatilis) in Chesapeake Bay. Can. J. Fish. Aquat. Sci. 69:247–58
    [Google Scholar]
  93. Le Moullac G, Soyez C, Saulnier D, Ansquer D, Avarre JC, Levy P 1998. Effect of hypoxic stress on the immune response and the resistance to vibriosis of the shrimp Penaeus stylirostris. . Fish Shellfish Immun 8:621–29
    [Google Scholar]
  94. Lee RFD, Frischer ME. 2004. The decline of the blue crab: Changing weather patterns and a suffocating parasite may have reduced the numbers of this species along the eastern seaboard. Am. Sci. 92:548–53
    [Google Scholar]
  95. Leiva NV, Manriquez PH, Aguilera VM, Gonzalez MT 2019. Temperature and pCO2 jointly affect the emergence and survival of cercariae from a snail host: implications for future parasitic infections in the Humboldt Current system. Int. J. Parasitol. 49:49–61
    [Google Scholar]
  96. Lenihan HS, Peterson CH, Byers JE, Grabowski JH, Thayer GW, Colby DR 2001. Cascading of habitat degradation: oyster reefs invaded by refugee fishes escaping stress. Ecol. Appl. 11:764–82
    [Google Scholar]
  97. Lohmus M, Bjorklund M. 2015. Climate change: What will it do to fish-parasite interactions. ? Biol. J. Linn. Soc. 116:397–411
    [Google Scholar]
  98. MacLeod CD. 2017. Parasitic infection: a missing piece of the ocean acidification puzzle. ICES J. Mar. Sci. 74:929–33
    [Google Scholar]
  99. MacLeod CD, Poulin R. 2015. Differential tolerances to ocean acidification by parasites that share the same host. Int. J. Parasitol. 45:485–93
    [Google Scholar]
  100. MacLeod CD, Poulin R. 2016a. Parasitic infection: a buffer against ocean acidification. ? Biol. Lett. 12:20160007
    [Google Scholar]
  101. MacLeod CD, Poulin R. 2016b. Parasitic infection alters the physiological response of a marine gastropod to ocean acidification. Parasitology 143:1397–408
    [Google Scholar]
  102. Macnab V, Barber I. 2012. Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences. Glob. Change Biol. 18:1540–48
    [Google Scholar]
  103. Magalhães L, de Montaudouin X, Figueira E, Freitas R 2018. Trematode infection modulates cockles biochemical response to climate change. Sci. Total Environ. 637:30–40
    [Google Scholar]
  104. Mann W, Burge C, Mydlarz L 2013. The effects of climate change on the immunocompetence of the Caribbean Sea fan coral. Integr. Comp. Biol. 53:E135
    [Google Scholar]
  105. Marcogliese DJ. 2001. Implications of climate change for parasitism of animals in the aquatic environment. Can. J. Zool. 79:1331–52
    [Google Scholar]
  106. Marcogliese DJ. 2008. The impact of climate change on the parasites and infectious diseases of aquatic animals. Rev. Sci. Tech. 27:467–84
    [Google Scholar]
  107. Marcogliese DJ. 2016. The distribution and abundance of parasites in aquatic ecosystems in a changing climate: more than just temperature. Integr. Comp. Biol. 56:611–19
    [Google Scholar]
  108. Marcogliese DJ, Cone DK. 2001. Myxozoan communities parasitizing Notropis hudsonius (Cyprinidae) at selected localities on the St. Lawrence River, Quebec: possible effects of urban effluents. J. Parasitol. 87:951–56
    [Google Scholar]
  109. McCallum HI, Kuris A, Harvell CD, Lafferty KD, Smith GW, Porter J 2004. Does terrestrial epidemiology apply to marine systems. ? Trends Ecol. Evol. 19:585–91
    [Google Scholar]
  110. McLean EL, Katenka NV, Seibel BA 2018. Decreased growth and increased shell disease in early benthic phase Homarus americanus in response to elevated CO2. Mar. Ecol. Prog. Ser. 596:113–26
    [Google Scholar]
  111. Mellergaard S, Nielsen E. 1997. Epidemiology of lymphocystis, epidermal papilloma and skin ulcers in common dab Limanda limanda along the west coast of Denmark. Dis. Aquat. Organ. 30:151–63
    [Google Scholar]
  112. Mikheev VN, Pasternak AF, Valtonen ET, Taskinen J 2014. Increased ventilation by fish leads to a higher risk of parasitism. Parasite Vector 7:281
    [Google Scholar]
  113. Möller H. 1978. Effects of salinity and temperature on development and survival of fish parasites. J. Fish Biol. 12:311–23
    [Google Scholar]
  114. Molnár PK, Sckrabulis JP, Altman KA, Raffel TR 2017. Thermal performance curves and the metabolic theory of ecology—a practical guide to models and experiments for parasitologists. J. Parasitol. 103:423–39
    [Google Scholar]
  115. Mordecai EA, Caldwell JM, Grossman MK, Lippi CA, Johnson LR et al. 2019. Thermal biology of mosquito-borne disease. Ecol. Lett. 22:1690–708
    [Google Scholar]
  116. Mouritsen KN, Jensen T, Jensen KT 1997. Parasites on an intertidal Corophium-bed: factors determining the phenology of microphallid trematodes in the intermediate host populations of the mud snail Hydrobia ulvae and the amphipod Corophium volutator. . Hydrobiologia 355:61–70
    [Google Scholar]
  117. Mouritsen KN, Mouritsen LT, Jensen KT 1998. Change of topography and sediment characteristics on an intertidal mud-flat following mass-mortality of the amphipod Corophium volutator. J. Mar. Biol. Assoc. UK 78:1167–80
    [Google Scholar]
  118. Mouritsen KN, Poulin R. 2002. Parasitism, climate oscillations and the structure of natural communities. Oikos 97:462–68
    [Google Scholar]
  119. Mouritsen KN, Tompkins DM, Poulin R 2005. Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146:476–83
    [Google Scholar]
  120. Paterson RA, Townsend CR, Tompkins DM, Poulin R 2012. Ecological determinants of parasite acquisition by exotic fish species. Oikos 121:1889–95
    [Google Scholar]
  121. Phillips BL, Kelehear C, Pizzatto L, Brown GP, Barton D, Shine R 2010. Parasites and pathogens lag behind their host during periods of host range advance. Ecology 91:872–81
    [Google Scholar]
  122. Pohley WJ. 1976. Relationships among three species of Littorina and their larval digenea. Mar. Biol. 37:179–86
    [Google Scholar]
  123. Pörtner HO, Farrell AP. 2008. Physiology and climate change. Science 322:690–92
    [Google Scholar]
  124. Posey MH, Alphin TD, Harwell H, Allen B 2005. Importance of low salinity areas for juvenile blue crabs, Callinectes sapidus Rathbun, in river-dominated estuaries of southeastern United States. J. Exp. Mar. Biol. Ecol. 319:81–100
    [Google Scholar]
  125. Raffel TR, Romansic JM, Halstead NT, McMahon TA, Venesky MD, Rohr JR 2013. Disease and thermal acclimation in a more variable and unpredictable climate. Nat. Clim. Change 3:146–51
    [Google Scholar]
  126. Reipschlager A, Pörtner HO. 1996. Metabolic depression during environmental stress: the role of extracellular versus intracellular pH in Sipunculus nudus. J. Exp. . Biol 199:1801–7
    [Google Scholar]
  127. Rosell D, Uriz MJ, Martin D 1999. Infestation by excavating sponges on the oyster (Ostrea edulis) populations of the Blanes littoral zone (north-western Mediterranean Sea). J. Mar. Biol. Assoc. UK 79:409–13
    [Google Scholar]
  128. Ruiz GM, Carlton JT 2003. Invasive Species: Vectors and Management Strategies Washington, DC: Island. , 2nd ed..
    [Google Scholar]
  129. Samsing F, Oppedal F, Johansson D, Bui S, Dempster T 2014. High host densities dilute sea lice Lepeophtheirus salmonis loads on individual Atlantic salmon, but do not reduce lice infection success. Aquacult. Environ. Interact. 6:81–89
    [Google Scholar]
  130. Schmidt KA, Ostfeld RS. 2001. Biodiversity and the dilution effect in disease ecology. Ecology 82:609–19
    [Google Scholar]
  131. Schmidtko S, Stramma L, Visbeck M 2017. Decline in global oceanic oxygen content during the past five decades. Nature 542:335–39
    [Google Scholar]
  132. Sheppard M, Walker A, Frischer ME, Lee RF 2003. Histopathology and prevalence of the parasitic dinoflagellate, Hematodinium sp, in crabs (Callinectes sapidus, Callinectes similis, Neopanope sayi, Libinia emarginata, Menippe mercenaria) from a Georgia estuary. J. Shellfish Res 22:873–80
    [Google Scholar]
  133. Shields JD. 2019. Climate change enhances disease processes in crustaceans: case studies in lobsters, crabs, and shrimps. J. Crustacean Biol. 39:673–83
    [Google Scholar]
  134. Strathmann RR. 1990. Why life histories evolve differently in the sea. Am. Zool. 30:197–207
    [Google Scholar]
  135. Stubler AD, Robertson H, Styron HJ, Carroll JM, Finelli CM 2017. Reproductive and recruitment dynamics of clionaid sponges on oyster reefs in North Carolina. Invertebr. Biol. 136:365–78
    [Google Scholar]
  136. Studer A, Thieltges DW, Poulin R 2010. Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Mar. Ecol. Prog. Ser. 415:11–22
    [Google Scholar]
  137. Tanner CA, Burnett LE, Burnett KG 2006. The effects of hypoxia and pH on phenoloxidase activity in the Atlantic blue crab. Callinectes sapidus. Comp. Biochem. Phys. A 144:218–23
    [Google Scholar]
  138. Taylor RA, White A, Sherratt JA 2015. Seasonal forcing in a host-macroparasite system. J. Theor. Biol. 365:55–66
    [Google Scholar]
  139. Thieltges DW, Bordalo MD, Hernandez AC, Prinz K, Jensen KT 2008. Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135:1111–16
    [Google Scholar]
  140. Tolley SG, Winstead JT, Haynes L, Volety AK 2006. Influence of salinity on prevalence of the parasite Loxothylacus panopaei in the xanthid Panopeus obesus in SW Florida. Dis. Aquat. Organ. 70:243–50
    [Google Scholar]
  141. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM 2003. Introduced species and their missing parasites. Nature 421:628–30
    [Google Scholar]
  142. Valenzuela A, Silva V, Tarifeno E, Klempau A 2005. Effect of acute hypoxia in trout (Oncorhynchus mykiss) on immature erythrocyte release and production of oxidative radicals. Fish Physiol. Biochem. 31:65–72
    [Google Scholar]
  143. Van Engel WA, Dillon WA, Zwerner D, Eldridge D 1966. Loxothylacus panopaei (Cirripedia, Sacculinidae) an introduced parasite on a xanthid crab in Chesapeake Bay, U.S.A. Crustaceana 10:110–12
    [Google Scholar]
  144. Vogelbein WK, Zwerner DE, Kator H, Rhodes MW, Cardinal J 1999. 24th Annual Eastern Fish Health Workshop, Atlantic Beach, NC, 1999 Rep., Natl. Fish Health Res. Lab., Biol. Resour. Div., US Geol. Surv Washington, DC:
    [Google Scholar]
  145. Ward JR, Kim K, Harvell CD 2007. Temperature affects coral disease resistance and pathogen growth. Mar. Ecol. Prog. Ser. 329:115–21
    [Google Scholar]
  146. Welker TL, McNulty ST, Klesius PH 2007. Effect of sublethal hypoxia on the immune response and susceptibility of channel catfish, Ictalurus punctatus, to enteric septicemia. J. World Aquacult. Soc. 38:12–23
    [Google Scholar]
  147. Wells JV. 1994. Correlates of the distribution and abundance of wintering gulls in Maine. J. Field Ornithol. 65:283–94
    [Google Scholar]
  148. Welsh JE, van der Meer J, Brussaard CPD, Thieltges DW 2014. Inventory of organisms interfering with transmission of a marine trematode. J. Mar. Biol. Assoc. UK 94:697–702
    [Google Scholar]
  149. Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AMH 2007. Parasites alter community structure. PNAS 104:9335–39
    [Google Scholar]
  150. Zell R, Krumbholz A, Wutzler P 2008. Impact of global warming on viral diseases: What is the evidence. ? Curr. Opin. Biotechnol. 19:652–60
    [Google Scholar]
/content/journals/10.1146/annurev-marine-031920-100429
Loading
/content/journals/10.1146/annurev-marine-031920-100429
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error