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How have fisheries affected parasite communities?

Published online by Cambridge University Press:  03 March 2014

CHELSEA L. WOOD  and
KEVIN D. LAFFERTY Open the ORCID record for KEVIN D. LAFFERTY [Opens in a new window]
CHELSEA L. WOOD*
Affiliation:
Hopkins Marine Station of Stanford University, 120 Oceanview Blvd., Pacific Grove, CA 93950, USA Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, N122, Campus Box 334, Boulder, CO 80309, USA
KEVIN D. LAFFERTY
Affiliation:
US Geological Survey, Western Ecological Research Center, c/o Marine Science Institute, University of California, Santa Barbara, California 93106, USA
*
*Corresponding author. Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, N122, Campus Box 334, Boulder, CO 90309, USA. E-mail: Chelsea.Wood@colorado.edu
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Summary

To understand how fisheries affect parasites, we conducted a meta-analysis of studies that contrasted parasite assemblages in fished and unfished areas. Parasite diversity was lower in hosts from fished areas. Larger hosts had a greater abundance of parasites, suggesting that fishing might reduce the abundance of parasites by selectively removing the largest, most heavily parasitized individuals. After controlling for size, the effect of fishing on parasite abundance varied according to whether the host was fished and the parasite's life cycle. Parasites of unfished hosts were more likely to increase in abundance in response to fishing than were parasites of fished hosts, possibly due to compensatory increases in the abundance of unfished hosts. While complex life cycle parasites tended to decline in abundance in response to fishing, directly transmitted parasites tended to increase. Among complex life cycle parasites, those with fished hosts tended to decline in abundance in response to fishing, while those with unfished hosts tended to increase. However, among directly transmitted parasites, responses did not differ between parasites with and without fished hosts. This work suggests that parasite assemblages are likely to change substantially in composition in increasingly fished ecosystems, and that parasite life history and fishing status of the host are important in predicting the response of individual parasite species or groups to fishing.

Keywords

biodiversitydiseasefishingfreshwatermarinemeta-analysis
Type
Fisheries
Information
Parasitology , Volume 142 , Special Issue 1: Parasites in fisheries and mariculture , January 2015 , pp. 134 - 144
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Amundsen, P. A. and Kristoffersen, R. (1990). Infection of whitefish Coregonus-lavaretus L. sensu lato by Triaenophorus-crassus Forel Cestoda Psuedophyllidea: a case study in parasite control. Canadian Journal of Zoology 68, 1187–1192.CrossRefGoogle Scholar
Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94.CrossRefGoogle Scholar
Arneberg, P., Skorping, A., Grenfell, B. and Read, A. F. (1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London Series B – Biological Sciences 265, 1283–1289.CrossRefGoogle Scholar
Baum, J. K. and Worm, B. (2009). Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology 78, 699–714. doi: 10.1111/j.1365-2656.2009.01531.x.CrossRefGoogle ScholarPubMed
Behrens, M. D. and Lafferty, K. D. (2004). Effects of marine reserves and urchin disease on southern Californian rocky reef communities. Marine Ecology Progress Series 279, 129–139.CrossRefGoogle Scholar
Bender, M. G., Floeter, S. R., Mayer, F. P., Vila-Nova, D. A., Longo, G. O., Hanazaki, N., Carvalho-Filho, A. and Ferreira, C. E. L. (2013). Biological attributes and major threats as predictors of the vulnerability of species: a case study with Brazilian reef fishes. Oryx 47, 259–265.CrossRefGoogle Scholar
Bianchi, G. (2000). Impact of fishing on size composition and diversity of demersal fish communities. ICES Journal of Marine Science 57, 558–571. doi: 10.1006/jmsc.2000.0727.CrossRefGoogle Scholar
Casini, M., Hjelm, J., Molinero, J.-C., Lovgren, J., Cardinale, M., Bartolino, V., Belgrano, A. and Kornilovs, G. (2009). Trophic cascades promote threshold-like shifts in pelagic marine ecosystems. Proceedings of the National Academy of Sciences USA 106, 197–202.CrossRefGoogle ScholarPubMed
deMeeus, T. and Renaud, F. (2002). Parasites within the new phylogeny of eukaryotes. Trends in Parasitology 18, 247–251.CrossRefGoogle Scholar
Dobson, A. P. and May, R. M. (1987). The effects of parasites on fish populations – theoretical aspects. International Journal for Parasitology 17, 363–370.CrossRefGoogle ScholarPubMed
Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. and Jetz, W. (2008). Homage to Linnaeus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences USA 105, 11482–11489.CrossRefGoogle ScholarPubMed
Dunne, J. A., Williams, R. J. and Martinez, N. D. (2002). Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecology Letters 5, 558–567.CrossRefGoogle Scholar
Fowler, S. L., Cavanagh, R. D., Camhi, M., Burgess, G. H., Cailliet, G. M., Fordham, S. V., Simpfendorfer, C. A. and Musick, J. A. (2005). Sharks, rays and chimaeras: the status of the chondrichthyan fishes. IUCN/SSC Shark Specialist Group.Google Scholar
Frank, K. T., Petrie, B., Choi, J. S. and Leggett, W. C. (2005). Trophic cascades in a formerly cod-dominated ecosystem. Science 308, 1621–1623.CrossRefGoogle Scholar
Freeman, D. J. and MacDiarmid, A. B. (2009). Healthier lobsters in a marine reserve: effects of fishing on disease incidence in the spiny lobster, Jasus edwardsii . Marine and Freshwater Research 60, 140–145.CrossRefGoogle Scholar
Gomez, A., Nichols, E. and Perkins, S. L. (2012). Parasite conservation, conservation medicine, and ecosystem health. In New Directions in Conservation Medicine: Applied Cases of Ecological Health (ed. Aguirre, A. A., Ostfeld, R. S. and Daszak, P.), pp. 67–81. Oxford University Press, New York, NY, USA.Google Scholar
Hamner, W. M., Colin, P. L. and Hamner, P. P. (2007). Export-import dynamics of zooplankton on a coral reef in Palau. Marine Ecology Progress Series 334, 83–92.CrossRefGoogle Scholar
Harvell, D., Connell, J., Aronson, R., Smith, G., Baron, N., McKay, B., Ward, J., Sutherland, K., Kuris, A., Gerber, L., Lafferty, K., Kim, K., Porter, J., Dobson, A., Ellner, S., Pascual, M. and McCallum, H. (2004). The rising tide of ocean diseases: unsolved problems and research priorities. Frontiers in Ecology and the Environment 2, 375–382.CrossRefGoogle Scholar
Hechinger, R. and Lafferty, K. (2005). Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London Series B – Biological Sciences 272, 1059–1066.Google ScholarPubMed
Hudson, P. J., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle ScholarPubMed
Jennings, S. and Blanchard, J. (2004). Fish abundance with no fishing: predictions based on macroecological theory. Journal of Animal Ecology 73, 632–642.CrossRefGoogle Scholar
Johnson, M. B., Lafferty, K. D., van Oosterhout, C. and Cable, J. (2011). Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS ONE 6, e22634. doi: 10.1371/journal.pone.0022634.CrossRefGoogle ScholarPubMed
Kuris, A. M., Hechinger, R. F., Shaw, J. C., Whitney, K. L., Aguirre-Macedo, L., Boch, C. A., Dobson, A. P., Dunham, E. J., Fredensborg, B. L., Huspeni, T. C., Lorda, J., Mababa, L., Mancini, F. T., Mora, A. B., Pickering, M., Talhouk, N. L., Torchin, M. E. and Lafferty, K. D. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.CrossRefGoogle ScholarPubMed
Lafferty, K. (2012). Biodiversity loss decreases parasite diversity: theory and patterns. Philosophical Transactions of the Royal Society of London B Biological Sciences 367, 2814–2827.CrossRefGoogle ScholarPubMed
Lafferty, K. D. (2004). Fishing for lobsters indirectly increases epidemics in sea urchins. Ecological Applications 14, 1566–1573.CrossRefGoogle Scholar
Lafferty, K. D. (2008). Ecosystem consequences of fish parasites. Journal of Fish Biology 73, 2083–2093. doi: 10.1111/j.1095-8649.2008.02059.x.CrossRefGoogle Scholar
Lafferty, K. D. and Morris, A. K. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390–1397.CrossRefGoogle Scholar
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences USA 103, 11211–11216.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., De Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T. J., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, P. A., McLaughlin, J. P., Mordecai, E. A., Pascual, M., Poulin, R. and Thieltges, D. W. (2008 a). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Shaw, J. C. and Kuris, A. M. (2008 b). Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kiritimati Island. EcoHealth 5, 338–345.CrossRefGoogle ScholarPubMed
Leichter, J. J., Shellenbarger, G., Genovese, S. J. and Wing, S. R. (1998). Breaking internal waves on a Florida (USA) coral reef: a plankton pump at work? Marine Ecology Progress Series 166, 83–97.CrossRefGoogle Scholar
Lester, S. E., Halpern, B. S., Grorud-Colvert, K., Lubchenco, J., Ruttenberg, B. I., Gaines, S. D., Airame, S. and Warner, R. R. (2009). Biological effects within no-take marine reserves: a global synthesis. Marine Ecology Progress Series 384, 33–46.CrossRefGoogle Scholar
Lo, C. M., Morand, S. and Galzin, R. (1998). Parasite diversity/host age and size relationship in three coral-reef fishes from French Polynesia. International Journal for Parasitology 28, 1695–1708.CrossRefGoogle ScholarPubMed
Loot, G., Aldana, M. and Navarrete, S. A. (2005). Effects of human exclusion on parasitism in intertidal food webs of central Chile. Conservation Biology 19, 203–212.CrossRefGoogle Scholar
Marcogliese, D. (2002 a). Food webs and the transmission of parasites to marine fish. Parasitology 124, S83–S99.CrossRefGoogle ScholarPubMed
Marcogliese, D. J. (2002 b). Food webs and the transmission of parasites to marine fish. Parasitology 124 (Suppl.), S83–99.CrossRefGoogle ScholarPubMed
Marzoug, D., Boutiba, Z., Kostadinova, A. and Perez-del-Olmo, A. (2012). Effects of fishing on parasitism in a sparid fish: contrasts between two areas of the Western Mediterranean. Parasitology International 61, 414–420.CrossRefGoogle Scholar
McCallum, H., Gerber, L. and Jani, A. (2005). Does infectious disease influence the efficacy of marine protected areas? A theoretical framework. Journal of Applied Ecology 42, 688–698. doi: 10.1111/j.1365-2664.2005.01043.x.CrossRefGoogle Scholar
McClanahan, T. R. (1989). Kenyan coral reef-associated gastropod fauna: a comparison between protected and unprotected reefs. Marine Ecology Progress Series 53, 11–20.CrossRefGoogle Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, New York, NY, USA.CrossRefGoogle Scholar
Morand, S. and Poulin, R. (1998). Density, body mass and parasite richness of terrestrial mammals. Evolutionary Ecology 12, 717–727.CrossRefGoogle Scholar
Mouritsen, K. N. and Poulin, R. (2005). Parasitism can influence the intertidal zonation of non-host organisms. Marine Biology 148, 1–11.CrossRefGoogle Scholar
Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P. and Peterson, C. H. (2007). Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.CrossRefGoogle ScholarPubMed
Pacala, S. W. and Dobson, A. P. (1988). The relation between the number of parasites/host and host age: population dynamic causes and maximum likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle ScholarPubMed
Pauly, D. and Watson, R. (2005). Background and interpretation of the ‘Marine Trophic Index’ as a measure of biodiversity. Proceedings of the Royal Society of London B – Biological Sciences 360, 415–423.CrossRefGoogle ScholarPubMed
Pauly, D., Alder, J. and Watson, R. (2005). Global trends in world fisheries: impacts on marine ecosystems and food security. Philosophical Transactions of the Royal Society of London B Biological Sciences 360, 5–12.CrossRefGoogle ScholarPubMed
Poulin, R. (1998). Evolutionary Ecology of Parasites: From Individuals to Communities. Chapman & Hall, London, UK.Google Scholar
Poulin, R. (2000). Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. Journal of Fish Biology 56, 123–137. doi: 10.1111/j.1095-8649.2000.tb02090.x.CrossRefGoogle Scholar
Poulin, R. and Morand, S. (2000). The diversity of parasites. Quarterly Review of Biology 75, 277–293.CrossRefGoogle ScholarPubMed
Preston, D. L., Orlofske, S. A., Lambden, J. P. and Johnson, P. T. J. (2013). Biomass and productivity of trematode parasites in pond ecosystems. Journal of Animal Ecology 82, 509–517.CrossRefGoogle ScholarPubMed
Rudolf, V. H. W. and Lafferty, K. D. (2011). Stage structure alters how complexity affects stability of ecological networks. Ecology Letters 14, 75–79. doi: 10.1111/j.1461-0248.2010.01558.x.CrossRefGoogle ScholarPubMed
Sala-Bozano, M., van Oosterhout, C. and Mariani, S. (2012). Impact of a mouth parasite in a marine fish differs between geographical areas. Biological Journal of the Linnean Society 105, 842–852.CrossRefGoogle Scholar
Sasal, P., Faliex, E. and Morand, S. (1996). Parasitism of Gobius bucchichii Steindachner, 1870 (Teleostei, Gobiidae) in protected and unprotected marine environments. Journal of Wildlife Diseases 32, 607–613.CrossRefGoogle ScholarPubMed
Sasal, P., Desdevises, Y., Durieux, E., Lenfant, P. and Romans, P. (2004). Parasites in marine protected areas: success and specificity of monogeneans. Journal of Fish Biology 64, 370–379.CrossRefGoogle Scholar
Sato, T., Watanabe, K., Kanaiwa, M., Niizuma, Y., Harada, Y. and Lafferty, K. D. (2011). Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology 92, 201–207.CrossRefGoogle ScholarPubMed
Sonnenholzner, J. I., Lafferty, K. D. and Ladah, L. B. (2011). Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galapagos. Ecology 92, 2276–2284.CrossRefGoogle ScholarPubMed
Stevens, J. D., Bonfil, R., Dulvy, N. K. and Walker, P. A. (2000). The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494.CrossRefGoogle Scholar
Suttle, C. A. (2005). Viruses in the sea. Nature 437, 356–361.CrossRefGoogle ScholarPubMed
Ternengo, S., Levron, C., Mouillot, D. and Marchand, B. (2009). Site influence in parasite distribution from fishes of the Bonifacio Strait Marine Reserve (Corsica Island, Mediterranean Sea). Parasitology Research 104, 1279–1287.CrossRefGoogle ScholarPubMed
Wood, C. L., Byers, J. E., Cottingham, K. L., Altman, I., Donahue, M. J. and Blakeslee, A. M. H. (2007). Parasites alter community structure. Proceedings of the National Academy of Sciences USA 104, 9335–9339.CrossRefGoogle ScholarPubMed
Wood, C. L., Lafferty, K. D. and Micheli, F. (2010). Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecology Letters 13, 761–775. doi: 10.1111/j.1461-0248.2010.01467.x.CrossRefGoogle ScholarPubMed
Wood, C. L., Micheli, F., Fernandez, M., Gelcich, S., Castilla, J. C. and Carvajal, J. (2013). Marine protected areas facilitate parasite populations among four fished host species of central Chile. Journal of Animal Ecology 82, 1276–1287. doi: 10.1111/1365-2656.12104.CrossRefGoogle ScholarPubMed
Wood, C. L., Sandin, S., Zgliczynski, B., Guerra, A. S. and Micheli, F. (in press). Fishing drives declines in fish parasite diversity and has variable effects on parasite abundance: evidence from fished and unfished coral atolls of the Line Islands. Ecology.Google Scholar
Wootton, E. C., Woolmer, A. P., Vogan, C. L., Pope, E. C., Hamilton, K. M. and Rowley, A. F. (2012). Increased disease calls for a costs–benefits review of marine reserves. PLoS ONE 7, e51615. doi: 10.1371/journal.pone.0051615.CrossRefGoogle ScholarPubMed
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