Book contents
- Wildlife Disease Ecology
- Ecological Reviews
- Wildlife Disease Ecology
- Copyright page
- Contents
- Contributors
- Preface: Wildlife Disease Ecology
- Glossary of Terms
- Part I Understanding within-host processes
- Part II Understanding between-host processes
- Part III Understanding wildlife disease ecology at the community and landscape level
- Chapter Fifteen The ecological and evolutionary trajectory of oak powdery mildew in Europe
- Chapter Sixteen Healthy herds or predator spreaders? Insights from the plankton into how predators suppress and spread disease
- Chapter Seventeen Multi-trophic interactions and migration behaviour determine the ecology and evolution of parasite infection in monarch butterflies
- Chapter Eighteen When chytrid fungus invades: integrating theory and data to understand disease-induced amphibian declines
- Chapter Nineteen Ecology of a marine ectoparasite in farmed and wild salmon
- Chapter Twenty Mycoplasmal conjunctivitis in house finches: the study of an emerging disease
- Chapter Twenty-one Processes generating heterogeneities in infection and transmission in a parasite–rabbit system
- Chapter Twenty-two Sylvatic plague in Central Asia: a case study of abundance thresholds
- Index
- Plate Section (PDF Only)
- References
Chapter Sixteen - Healthy herds or predator spreaders? Insights from the plankton into how predators suppress and spread disease
from Part III - Understanding wildlife disease ecology at the community and landscape level
Published online by Cambridge University Press: 28 October 2019
Book contents
- Wildlife Disease Ecology
- Ecological Reviews
- Wildlife Disease Ecology
- Copyright page
- Contents
- Contributors
- Preface: Wildlife Disease Ecology
- Glossary of Terms
- Part I Understanding within-host processes
- Part II Understanding between-host processes
- Part III Understanding wildlife disease ecology at the community and landscape level
- Chapter Fifteen The ecological and evolutionary trajectory of oak powdery mildew in Europe
- Chapter Sixteen Healthy herds or predator spreaders? Insights from the plankton into how predators suppress and spread disease
- Chapter Seventeen Multi-trophic interactions and migration behaviour determine the ecology and evolution of parasite infection in monarch butterflies
- Chapter Eighteen When chytrid fungus invades: integrating theory and data to understand disease-induced amphibian declines
- Chapter Nineteen Ecology of a marine ectoparasite in farmed and wild salmon
- Chapter Twenty Mycoplasmal conjunctivitis in house finches: the study of an emerging disease
- Chapter Twenty-one Processes generating heterogeneities in infection and transmission in a parasite–rabbit system
- Chapter Twenty-two Sylvatic plague in Central Asia: a case study of abundance thresholds
- Index
- Plate Section (PDF Only)
- References
Summary
How and why do predators sometimes fuel disease outbreaks but other times thwart them? Answering this could help explain spatial and temporal variation in disease and could explain why attempts to control disease by manipulating predators sometimes fail. We give eight mechanisms by which predators can suppress/spread disease in prey populations, exploring each generally and reviewing evidence from the study system that has been the focus of much of our research. This system focuses on Daphnia dentifera, a dominant herbivore in lake food webs in the Midwestern United States. D. dentifera is prey to bluegill sunfish and phantom midge larvae, as well as host to a virulent fungal pathogen. We review evidence for bluegill sunfish as ‘healthy herds’ predators that reduce disease, and for midge larvae as ‘predator spreaders’ that fuel disease outbreaks. We find that both predators can impact disease via multiple mechanisms. Bluegill feed selectively on infected hosts and also depress disease in Daphnia by reducing the density of midge larvae which spread disease. They also increase the abundance of Ceriodaphnia, which reduce disease. Midge larvae increase disease in their hosts, in part by releasing spores into the water column where they can be consumed by additional hosts.
Keywords
- Type
- Chapter
- Information
- Wildlife Disease EcologyLinking Theory to Data and Application, pp. 458 - 479Publisher: Cambridge University PressPrint publication year: 2019
References
Auld, S.K., Hall, S.R., Ochs, J.H., Sebastian, M. & Duffy, M.A. (2014) Predators and patterns of within-host growth can mediate both among-host competition and evolution of transmission potential of parasites. American Naturalist, 18, S77–S90.CrossRefGoogle Scholar
Bertram, C.R., Pinkowski, M., Hall, S.R., Duffy, M.A. & Cáceres, C.E. (2013) Trait-mediated indirect effects, predators, and disease: test of a size-based model. Oecologia, 173, 1023–1032.Google Scholar
Bidegain, G., Powell, E.N., Klinck, J.M., Ben-Horin, T. & Hofmann, E.E. (2016) Marine infectious disease dynamics and outbreak thresholds: contact transmission, pandemic infection, and the potential role of filter feeders. Ecosphere, 7, e01286.CrossRefGoogle Scholar
Brooks, J.L. & Dodson, S.I. (1965) Predation, body size, and composition of plankton. Science, 150, 28–35.CrossRefGoogle ScholarPubMed
Buck, J., Truong, L. & Blaustein, A. (2011) Predation by zooplankton on Batrachochytrium dendrobatidis: biological control of the deadly amphibian chytrid fungus? Biodiversity and Conservation, 20, 3549–3553.Google Scholar
Byers, J.E., Malek, A.J., Quevillon, L.E., Altman, I. & Keogh, C.L. (2015) Opposing selective pressures decouple pattern and process of parasitic infection over small spatial scale. Oikos, 124, 1511–1519.Google Scholar
Cáceres, C.E., Hall, S.R., Duffy, M.A., Tessier, A.J., Helmle, C. & MacIntyre, S. (2006) Physical structure of lakes constrains epidemics in Daphnia populations. Ecology, 87, 1438–1444.Google Scholar
Cáceres, C.E., Knight, C.J. & Hall, S.R. (2009) Predator spreaders: predation can enhance parasite success in a planktonic host–parasite system. Ecology, 90, 2850–2858.CrossRefGoogle Scholar
Cáceres, C.E., Tessier, A.J., Duffy, M.A. & Hall, S.R. (2014) Disease in freshwater zooplankton: what have we learned and where are we going? Journal of Plankton Research, 36, 326–333.CrossRefGoogle Scholar
Choisy, M. & Rohani, P. (2006) Harvesting can increase severity of wildlife disease epidemics. Proceedings of the Royal Society of London Series B, 273, 2025–2034.Google Scholar
Civitello, D.J., Pearsall, S., Duffy, M.A. & Hall, S.R. (2013) Parasite consumption and host interference can inhibit disease spread in dense populations. Ecology Letters, 16, 626–634.Google Scholar
Civitello, D.J., Penczykowski, R.M., Smith, A.N., et al. (2015) Resources, key traits, and the size of fungal epidemics in Daphnia populations. Journal of Animal Ecology, 84, 1010–1017.CrossRefGoogle ScholarPubMed
Coors, A. & De Meester, L. (2011) Fitness and virulence of a bacterial endoparasite in an environmentally stressed crustacean host. Parasitology, 138, 122–131.Google Scholar
Cressler, C.E., Nelson, W.A., Day, T. & McCauley, E. (2014) Disentangling the interaction among host resources, the immune system and pathogens. Ecology Letters, 17, 284–293.Google Scholar
de Roos, A.M. & Persson, L. (2013) Population and Community Ecology of Ontogenetic Development. Princeton, NJ: Princeton University Press.Google Scholar
Decaestecker, E., De Meester, L. & Ebert, D. (2002) In deep trouble: habitat selection constrained by multiple enemies in zooplankton. Proceedings of the National Academy of Science of the United States of America, 99, 5481–5485.CrossRefGoogle ScholarPubMed
Department for Environment Food and Rural Affairs (2016) Summary of badger control monitoring during 2016. www.gov.uk/government/uploads/system/uploads/attachment_data/file/578436/summary-badger-control-monitoring-2016.pdfGoogle Scholar
Donnelly, C.A., Woodroffe, R., Cox, D.R., et al. (2003) Impact of localized badger culling on tuberculosis incidence in British cattle. Nature, 426, 834–837.Google Scholar
Duffy, M.A. (2007) Selective predation, parasitism, and trophic cascades in a bluegill–Daphnia–parasite system. Oecologia, 153, 453–460.Google Scholar
Duffy, M.A. (2009) Staying alive: the post-consumption fate of parasite spores and its implications for disease dynamics. Limnology and Oceanography, 54, 770–773.CrossRefGoogle Scholar
Duffy, M.A., Cáceres, C.E., Hall, S.R., Tessier, A.J. & Ives, A.R. (2010) Temporal, spatial, and between-host comparisons of patterns of parasitism in lake zooplankton. Ecology, 91, 3322–3331.Google Scholar
Duffy, M.A. & Hall, S.R. (2008) Selective predation and rapid evolution can jointly dampen effects of virulent parasites on Daphnia populations. American Naturalist, 171, 499–510.Google Scholar
Duffy, M.A., Hall, S.R., Cáceres, C.E. & Ives, A.R. (2009) Rapid evolution, seasonality and the termination of parasite epidemics. Ecology, 90, 1441–1448.CrossRefGoogle ScholarPubMed
Duffy, M.A., Hall, S.R., Tessier, A.J. & Huebner, M. (2005) Selective predators and their parasitized prey: are epidemics in zooplankton under top-down control? Limnology and Oceanography, 50, 412–420.Google Scholar
Duffy, M.A., Housley, J.M., Penczykowski, R.M., Cáceres, C.E. & Hall, S.R. (2011) Unhealthy herds: indirect effects of predators enhance two drivers of disease spread. Functional Ecology, 25, 945–953.Google Scholar
Duffy, M.A., James, T.Y. & Longworth, A. (2015) Ecology, virulence, and phylogeny of Blastulidium paedophthorum, a widespread brood parasite of Daphnia spp. Applied & Environmental Microbiology, 81, 5486–5496.Google Scholar
Duffy, M.A., Ochs, J.H., Penczykowski, R.M., et al. (2012) Ecological context influences epidemic size and parasite-mediated selection. Science, 335, 1636–1638.Google Scholar
Elser, M.M., Vonende, C.N., Sorrano, P. & Carpenter, S.R. (1987) Chaoborus populations: response to food web manipulation and potential effects on zooplankton communities. Canadian Journal of Zoology, 65, 2846–2852.Google Scholar
González, M.J. & Tessier, A.J. (1997) Habitat segregation and interactive effects of multiple predators on a prey assemblage. Freshwater Biology, 38, 179–191.Google Scholar
Goren, L. & Ben-Ami, F. (2017) To eat or not to eat infected food: a bug’s dilemma.Hydrobiologia, 798, 25–32.Google Scholar
Groner, M.L. & Relyea, R.A. (2015) Predators reduce Batrachochytrium dendrobatidis infection loads in their prey. Freshwater Biology, 60, 1699–1704.Google Scholar
Hall, S.R., Becker, C.R., Simonis, J.L., et al. (2009) Friendly competition: evidence for a dilution effect among competitors in a planktonic host–parasite system. Ecology, 90, 791–801.Google Scholar
Hall, S.R., Duffy, M.A. & Cáceres, C.E. (2005) Selective predation and productivity jointly drive complex behavior in host–parasite systems. American Naturalist, 165, 70–81.Google Scholar
Hall, S.R., Sivars-Becker, L., Becker, C., et al. (2007) Eating yourself sick: transmission of disease as a function of feeding biology of hosts. Ecology Letters, 10, 207–218.CrossRefGoogle Scholar
Hall, S.R., Smyth, R., Becker, C.R., et al. (2010) Why are Daphnia in some lakes sicker? Disease ecology, habitat structure, and the plankton. BioScience, 60, 363–375.Google Scholar
Hall, S.R., Tessier, A.J., Duffy, M.A., Huebner, M. & Cáceres, C.E. (2006) Warmer does not have to mean sicker: temperature and predators can jointly drive timing of epidemics. Ecology, 87, 1684–1695.Google Scholar
Harvell, D., Aronson, R., Baron, N., et al. (2004) The rising tide of ocean diseases: unsolved problems and research priorities. Frontiers in Ecology and the Environment, 2, 375–382.Google Scholar
Hesse, O., Engelbrecht, W., Laforsch, C. & Wolinska, J. (2012) Fighting parasites and predators: how to deal with multiple threats? BMC Ecology, 12, 12.Google Scholar
Hite, J.L., Bosch, J., Fernández-Beaskoetxea, S., Medina, D. & Hall, S.R. (2016) Joint effects of habitat, zooplankton, host stage structure and diversity on amphibian chytrid. Proceedings of the Royal Society of London B, 283, 20160832.Google Scholar
Holt, R.D. & Roy, M. (2007) Predation can increase the prevalence of infectious disease. American Naturalist, 169, 690–699.Google Scholar
Hudson, P.J. (1986) The effect of a parasitic nematode on the breeding production of red grouse. Journal of Animal Ecology, 55, 85–92.Google Scholar
Hudson, P.J., Dobson, A.P. & Newborn, D. (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. Journal of Animal Ecology, 61, 681–692.CrossRefGoogle Scholar
Johnson, A. & Brunner, J. (2014) Persistence of an amphibian ranavirus in aquatic communities. Diseases of Aquatic Organisms, 111, 129–138.CrossRefGoogle ScholarPubMed
Johnson, P.T.J., Dobson, A., Lafferty, K.D., et al. (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology & Evolution, 25, 362–371.Google Scholar
Johnson, P.T.J., Stanton, D.E., Preu, E.R., Forshay, K.J. & Carpenter, S.R. (2006) Dining on disease: how interactions between parasite infection and environmental conditions affect host predation risk. Ecology, 87, 1973–1980.Google Scholar
Kagami, M., Van Donk, E., de Bruin, A., Rijkeboer, M. & Ibelings, B.W. (2004) Daphnia can protect diatoms from fungal parasitism. Limnology and Oceanography, 49, 680–685.Google Scholar
Keeling, M.J. & Rohani, P. (2008) Modeling Infectious Diseases in Humans and Animals. Princeton, NJ: Princeton University Press.Google Scholar
Keesing, F., Belden, L.K., Daszak, P., et al. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature, 468, 647–652.CrossRefGoogle ScholarPubMed
Keymer, A., Crompton, D.W.T. & Walters, D.E. (1983) Parasite population biology and host nutrition – dietary fructose and Moniliformis (Acanthocephala). Parasitology, 87, 265–278.Google Scholar
Kistler, R.A. (1985) Host-age structure and parasitism in a laboratory system of two hymenopterous parasitoids and larvae of Zabrotes subfasciatus (Coleoptera, Bruchidae). Environmental Entomology, 14, 507–511.Google Scholar
Lafferty, K.D. (2004) Fishing for lobsters indirectly increases epidemics in sea urchins. Ecological Applications, 14, 1566–1573.Google Scholar
Lafferty, K.D., Harvell, C.D., Conrad, J.M., et al. (2015) Infectious diseases affect marine fisheries and aquaculture economics. Annual Review of Marine Science, 7, 471–496.Google Scholar
Lass, S. & Bittner, K. (2002) Facing multiple enemies: parasitised hosts respond to predator kairomones. Oecologia, 132, 344–349.CrossRefGoogle ScholarPubMed
Levi, T., Kilpatrick, A.M., Mangel, M. & Wilmers, C.C. (2012) Deer, predators, and the emergence of Lyme disease. Proceedings of the National Academy of Sciences of the United States of America, 109, 10,942–10,947.Google Scholar
Li, J., Kolivras, K.N., Hong, Y., et al. (2014) Spatial and temporal emergence pattern of Lyme disease in Virginia. The American Journal of Tropical Medicine and Hygiene, 91, 1166–1172.Google Scholar
Lindeque, P.M. & Turnbull, P.C.B. (1994) Ecology and epidemiology of anthrax in the Etosha National Park, Namibia. Onderstepoort Journal of Veterinary Research, 61, 71–83.Google Scholar
Michael, E. & Bundy, D.A.P. (1992) Nutrition, immunity and helminth infection: effect of dietary protein on the dynamics of the primary antibody response to Trichuris muris (Nematoda) in CBA/Ca mice. Parasite Immunology, 14, 169–183.Google Scholar
Mittelbach, G.G. (1981) Patterns of invertebrate size and abundance in aquatic habitats. Canadian Journal of Fisheries and Aquatic Sciences, 38, 896–904.Google Scholar
Morters, M.K., Restif, O., Hampson, K., et al. (2013) Evidence-based control of canine rabies: a critical review of population density reduction. Journal of Animal Ecology, 82, 6–14.Google Scholar
Navarro, C., de Lope, F., Marzal, A. & Møller, A.P. (2004) Predation risk, host immune response, and parasitism. Behavioral Ecology, 15, 629–635.Google Scholar
Orlofske, S.A., Jadin, R.C., Preston, D.L. & Johnson, P.T.J. (2012) Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology, 93, 1247–1253.Google Scholar
Ostfeld, R.S. & Holt, R.D. (2004) Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic disease reservoirs. Frontiers in Ecology and the Environment, 2, 13–20.Google Scholar
Ostfeld, R.S. & Keesing, F. (2000) Biodiversity and disease risk: the case of Lyme disease [Biodiversidad y Riesgo de Enfermedades: El Caso de la Enfermedad de Lyme]. Conservation Biology, 14, 722–728.Google Scholar
Pace, M.L., Cole, J.J., Carpenter, S.R. & Kitchell, J.F. (1999) Trophic cascades revealed in diverse ecosystems. Trends in Ecology and Evolution, 14, 483–488.Google Scholar
Packer, C., Holt, R.D., Hudson, P.J., Lafferty, K.D. & Dobson, A.P. (2003) Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecology Letters, 6, 797–802.CrossRefGoogle Scholar
Pastorok, R.A. (1981) Prey vulnerability and size selection by Chaoborus larvae. Ecology, 62, 1311–1324.CrossRefGoogle Scholar
Penczykowski, R.M., Hall, S.R., Civitello, D.J. & Duffy, M.A. (2014) Habitat structure and ecological drivers of disease. Limnology and Oceanography, 59, 340–348.Google Scholar
Ramirez, R.A. & Snyder, W.E. (2009) Scared sick? Predator–pathogen facilitation enhances exploitation of a shared resource. Ecology, 90, 2832–2839.CrossRefGoogle ScholarPubMed
Rapti, Z. & Cáceres, C.E. (2016) Effects of intrinsic and extrinsic host mortality on disease spread. Bulletin of Mathematical Biology, 78, 235–253.Google Scholar
Rohr, J.R., Civitello, D.J., Crumrine, P.W., et al. (2015) Predator diversity, intraguild predation, and indirect effects drive parasite transmission. Proceedings of the National Academy of Sciences of the United States of America, 112, 3008–3013.Google Scholar
Salkeld, D.J., Padgett, K.A. & Jones, J.H. (2013) A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecology Letters, 16, 679–686.Google Scholar
Searle, C.L., Mendelson, J.R., Green, L.E. & Duffy, M.A. (2013) Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles. Ecology and Evolution, 3, 4129–4138.Google Scholar
Smith, V. (2007) Host resource supplies influence the dynamics and outcome of infectious disease. Integrative and Comparative Biology, 47, 310–316.Google Scholar
Snyder, W.E. & Ives, A.R. (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology, 82, 705–716.Google Scholar
Spitze, K. (1985) Functional response of an ambush predator: Chaoborus americanus predation on Daphnia pulex. Ecology, 66, 938–949.Google Scholar
Strauss, A.T., Civitello, D.J., Cáceres, C.E. & Hall, S.R. (2015) Success, failure and ambiguity of the dilution effect among competitors. Ecology Letters, 18, 916–926.Google Scholar
Strauss, A.T., Shocket, M.S., Civitello, D.J., et al. (2016) Habitat, predators, and hosts regulate disease in Daphnia through direct and indirect pathways. Ecological Monographs, 86, 393–411.Google Scholar
Tessier, A.J. & Woodruff, P. (2002) Cryptic trophic cascade along a gradient of lake size. Ecology, 83, 1263–1270.Google Scholar
Thomas, S.H., Bertram, C., van Rensburg, K., Caceres, C.E. & Duffy, M.A. (2011) Spatiotemporal dynamics of free-living stages of a bacterial parasite of zooplankton. Aquatic Microbial Ecology, 63, 265–272.Google Scholar
Turney, S., Gonzalez, A. & Millien, V. (2014) The negative relationship between mammal host diversity and Lyme disease incidence strengthens through time. Ecology, 95, 3244–3250.Google Scholar
Valois, A.E. & Burns, C.W. (2016) Parasites as prey: Daphnia reduce transmission success of an oomycete brood parasite in the calanoid copepod Boeckella. Journal of Plankton Research, 38, 1281–1288.Google Scholar
Williamson, C.E., Overholt, E.P., Pilla, R.M., et al. (2015) Ecological consequences of long-term browning in lakes. Scientific Reports, 5, 18666.Google Scholar
Wilson, K. & Cotter, S.C. (2009) Density-dependent prophylaxis in insects. In: Whitman, D.W. & Ananthakrishnan, T.N. (eds.), Phenotypic Plasticity of Insects: Mechanisms and Consequences (pp. 137–176). Boca Raton, FL: CRC Press.Google Scholar
Wood, C.L. & Lafferty, K.D. (2013) Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology & Evolution, 28, 239–247.Google Scholar
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