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Predators indirectly reduce the prevalence of an insect-vectored plant pathogen independent of predator diversity

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Abstract

A widely cited benefit of predator diversity is greater suppression of insect herbivores, with corresponding increases in plant biomass. In the context of a vector-borne pathogen system, predator species richness may also influence plant disease risk via the direct effects of predators on the abundance and behavior of herbivores that also act as pathogen vectors. Using an assemblage of generalist insect predators, we examined the relationship between predator species richness and the prevalence of the aphid-vectored cereal yellow dwarf virus in wheat. We found that increasing predator richness enhanced suppression of the vector population and that pathogen prevalence was reduced when predators were present, but the reduction in prevalence was independent of predator species richness. To determine the mechanism(s) by which predator species richness contributes to vector suppression, but not pathogen prevalence, we evaluated vector movement and host plant occupancy in response to predator treatments. We found that pathogen prevalence was unrelated to vector suppression because host plant occupancy by vectors did not vary as a function of vector abundance. However, the presence of predators reduced pathogen prevalence because predators stimulated greater plant-to-plant movement by vectors, which likely diminished vector feeding time and reduced the transmission efficiency of this persistent pathogen. We conclude that community structure (i.e., the presence of predators), but not predator diversity, is a potential factor influencing local plant infection by this insect-vectored pathogen.

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References

  • Bailey SM, Irwin ME, Kampmeier GE, Eastman CE, Hewings AD (1995) Physical and biological pertubations: their effect on the movement of apterous Rhophalosiphum padi (Homoptera: Aphididae) and localized spread of Barley yellow dwarf virus. Environ Entomol 24:24–33

    Article  Google Scholar 

  • Belliure B, Amorós-Jiménez R, Fereres A, Marcos-García M (2011) Antipredator behaviour of Myzus persicae affects transmission efficiency of Broad bean wilt virus 1. Virus Res 159:206–214

    Article  CAS  PubMed  Google Scholar 

  • Borer ET, Hosseini PR, Seabloom EW, Dobson AP (2007) Pathogen-induced reversal of native dominance in a grassland community. Proc Natl Acad Sci USA 104:5473–5478

  • Brewer MJ, Elliott NC (2004) Biological control of cereal aphids in North America and mediating effects of host plant and habitat manipulations. Annu Rev Entomol 49:219–242

    Article  CAS  PubMed  Google Scholar 

  • Cardinale BJ et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67

    Article  CAS  PubMed  Google Scholar 

  • Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–112

    Article  CAS  PubMed  Google Scholar 

  • Dáder B, Moreno A, Vinuela E, Fereres A (2012) Spatio-temporal dynamics of viruses are differentially affected by parasitoids depending on the mode of transmission. Viruses 4:3069–3090

    Article  PubMed Central  PubMed  Google Scholar 

  • D’Arcy CJ, Burnett PA (1995) Barley yellow dwarf: 40 years of progress. American Phytopathological Society, St Paul

    Google Scholar 

  • Deb M, Anderson JM (2007) Development of a multiplexed PCR detection method for Barley and Cereal yellow dwarf viruses, Wheat spindle streak virus, Wheat streak mosaic virus and Soil-borne wheat mosaic virus. J Virol Methods 148:17–24

    Article  PubMed  Google Scholar 

  • Finke DL (2012) Contrasting the consumptive and non-consumptive cascading effects of natural enemies on vector-borne pathogens. Entomol Exp Appl 144:45–55

    Article  Google Scholar 

  • Finke DL, Snyder WE (2008) Niche partitioning increases resource exploitation by diverse communities. Science 321:1488–1490

    Article  CAS  PubMed  Google Scholar 

  • Finke DL, Snyder WE (2010) Conserving the benefits of predator biodiversity. Biol Conserv 143:2260–2269

    Article  Google Scholar 

  • Gray SM, Gildow FE (2003) Luteovirus-aphid interactions. Annu Rev Phytopathol 41:539–566

    Article  CAS  PubMed  Google Scholar 

  • Gray SM, Power AG, Smith DM, Seaman AJ, Altman NS (1991) Aphid transmission of barley yellow dwarf virus: acquisition access periods and virus concentration requirements. Phytopathology 81:539–545

    Article  Google Scholar 

  • Griffin JN, Byrnes JEK, Cardinale BJ (2013) Effects of predator richness on prey suppression: a meta-analysis. Ecology 94:2180–2187

    Article  PubMed  Google Scholar 

  • Hodge S, Powell G (2008) Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection. Oecologia 157:387–397

    Article  PubMed  Google Scholar 

  • Hodge S, Hardie J, Powell G (2011) Parasitoids aid dispersal of a nonpersistently transmitted plant virus by disturbing the aphid vector. Agric For Entomol 13:83–88

    Article  Google Scholar 

  • Irwin ME, Thresh JM (1990) Epidemiology of barley yellow dwarf: a study in ecological complexity. Annu Rev Phytopathol 28:393–424

    Article  Google Scholar 

  • Jeger MJ, Chen Z, Powell G, Hodge S, van den Bosch F (2011) Interactions in a host plant-virus-vector-parasitoid system: modelling the consequences for virus transmission and disease dynamics. Virus Res 159:183–193

    Article  CAS  PubMed  Google Scholar 

  • Landis DA, Van der Werf W (1997) Early-season predation impacts the establishment of aphids and spread of Beet yellows virus in sugar beet. Entomophaga 42:499–516

    Article  Google Scholar 

  • Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40:573–592

    Article  Google Scholar 

  • Long EY, Finke DL (2014) The contribution of predator identity to the suppression of herbivores by a diverse predator assemblage. Environ Entomol 43:569–576

    Article  PubMed  Google Scholar 

  • Loreau M et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  CAS  PubMed  Google Scholar 

  • Malmstrom CM, Hughes CC, Newton LA, Stoner CJ (2005a) Virus infection in remnant native bunchgrasses from invaded California grasslands. New Phytol 168:217–230

    Article  CAS  PubMed  Google Scholar 

  • Malmstrom CM, McCullough AJ, Newton LA, Johnson HA, Borer ET (2005b) Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145:153–164

    Article  PubMed  Google Scholar 

  • Montgomery ME, Nault LR (1977) Comparative response of aphids to the alarm pheromone, (E)-ß-farnesene. Entomol Exp Appl 22:236–242

    Article  CAS  Google Scholar 

  • Moore SM, Borer ET, Hosseini PR (2009) Predators indirectly control vector-borne disease: linking predator–prey and host–pathogen models. J R Soc Interface 7:161–176

    Article  PubMed Central  PubMed  Google Scholar 

  • Northfield TD, Snyder GB, Ives AR, Snyder WE (2010) Niche saturation reveals resource partitioning among consumers. Ecol Lett 13:338–348

    Article  PubMed  Google Scholar 

  • Plumb RT (1983) Barley yellow dwarf virus—a global problem. In: Plumb RT, Thresh JM (eds) Plant virus epidemiology. Blackwell Science, London, pp 185–198

    Google Scholar 

  • Power AG (1991) Virus spread and vector dynamics in genetically diverse plant populations. Ecology 72:232–241

    Article  Google Scholar 

  • Power AG, Gray SM (1995) Aphid transmission of Barley yellow dwarf viruses: interactions between viruses, vectors, and host plants. In: D’Arcy CJ, Burnett PA (eds) Barley yellow dwarf: 40 years of progress. American Phytopathological Society, St Paul, p 374

    Google Scholar 

  • Power AG, Seaman AJ, Gray SM (1991) Aphid transmission of Barley yellow dwarf virus: inoculation access periods and epidemiological implications. Phytopathology 81:545–548

    Article  Google Scholar 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509

    Article  Google Scholar 

  • Preisser EL, Orrock JL, Schmitz OJ (2007) Predator hunting mode and habitat domain alter nonconsumptive effects in predator-prey interactions. Ecology 88:2744–2751

    Article  PubMed  Google Scholar 

  • Rochow WF (1970) Barley yellow dwarf virus: phenotypic mixing and vector specificity. Science 167:875–878

    Article  CAS  PubMed  Google Scholar 

  • Roitberg BD, Myers JH (1978) Effect of adult Coccinellidae on the spread of a plant virus by an aphid. J Appl Ecol 15:775–779

    Article  Google Scholar 

  • Salkeld DJ, Padgett KA, Jones JH (2013) A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecol Lett 16:679–686

    Article  PubMed  Google Scholar 

  • Schmitz OJ (2005) Behaviors of predators and prey and links with population-level processes. In: Barbosa P, Castellanos I (eds) Ecology of predator-prey interactions. Oxford University Press, New York, pp 256–278

    Google Scholar 

  • Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399

    Article  Google Scholar 

  • Smyrnioudis I, Harrington R, Clark S, Katis N (2001) The effect of natural enemies on the spread of Barley yellow dwarf virus (BYDV) by Rhopalosiphum padi (Hemiptera: Aphididae). Bull Entomol Res 91:301–306

    Article  CAS  PubMed  Google Scholar 

  • Snyder WE, Snyder GB, Finke DL, Straub CS (2006) Predator biodiversity strengthens herbivore suppression. Ecol Lett 9:789–796

    Article  PubMed  Google Scholar 

  • Steffan SA, Snyder WE (2010) Cascading diversity effects transmitted exclusively by behavioral interactions. Ecology 91:2242–2252

    Article  PubMed  Google Scholar 

  • Straub CS, Snyder WE (2006) Species identity dominates the relationship between predator biodiversity and herbivore suppression. Ecology 87:277–282

    Article  PubMed  Google Scholar 

  • Straub CS, Snyder WE (2008) Increasing enemy biodiversity strengthens herbivore suppression on two plant species. Ecology 89:1605–1615

    Article  PubMed  Google Scholar 

  • Straub CS, Finke DL, Snyder WE (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol Control 45:225–237

    Article  Google Scholar 

  • Tilman D et al (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284

    Article  CAS  PubMed  Google Scholar 

  • Weber CA, Godfrey LD, Mauk PA (1996) Effects of parasitism by Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) on transmission of Beet yellows closterovirus by bean aphid (Homoptera: Aphididae). J Econ Entomol 89:1431–1437

    Article  Google Scholar 

  • Wood CL, Lafferty KD (2012) Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol Evol 28:239–247

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Candace Galen, Richard Houseman, and James Schoelz for comments on the manuscript, Joseph Anderson for providing CYDV-RPV inoculum, Charles Mitchell and Marty Dekkers for sharing acquisition/inoculation protocols, Carlos Angel for laboratory training, and Lauren Diepenbrock for greenhouse assistance. We also thank Jennifer Thaler and two anonymous reviewers for helpful comments on the manuscript. This project was supported by the Agriculture and Food Research Initiative of the US Department of Agriculture National Institute of Food and Agriculture grant no. 2009-02083 and the University of Missouri Research Board (D. L. F.), and a University of Missouri Life Sciences Fellowship awarded to E. Y. L. Both E. Y. L. and D. L. F. declare that they have no conflict of interest, and all experiments were conducted in accordance with current laws in the USA.

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Correspondence to Elizabeth Y. Long.

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Communicated by Jennifer Thaler.

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Long, E.Y., Finke, D.L. Predators indirectly reduce the prevalence of an insect-vectored plant pathogen independent of predator diversity. Oecologia 177, 1067–1074 (2015). https://doi.org/10.1007/s00442-014-3194-1

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