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Influence of nonhost plant diversity and natural enemies on the potato leafhopper, Empoasca fabae, and pea aphid, Acyrthosiphon pisum, in alfalfa

Abstract

We examined the effects of nonhost plant diversity and predators on the potato leafhopper, Empoasca fabae (Harris), the pea aphid, Acyrthosiphon pisum (Harris), and their primary host plant, alfalfa, Medicago sativa L. Potato leafhopper intensity (i.e., leafhoppers/alfalfa stem density) and plant damage (i.e., hopperburn) were significantly greater in alfalfa mono- than in polycultures of alfalfa mixed with nonhost plant species. There was no significant effect of nonhost plant diversity on pea aphid intensity or on predator abundance. Predator:prey ratios were higher in poly- than in monoculture. One predator, Nabis sp., was selected for further study. A microcosm experiment indicated that Nabis is an effective predator of both herbivores, and suggested that nonhost plant diversity may enhance the predation of leafhoppers by Nabis. These results suggest that nonhost plant diversity and Nabis limit leafhopper populations and protect alfalfa from herbivory. The potential for nonhost plants to increase herbivore movement and vulnerability to predation is discussed.

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References

  • Ahrens WH, Cox DJ, Budhwar G (1990) Use of the arcsine and square root transformations for subjectively determined percentage data. Weed Sci 38:452–458

    Google Scholar 

  • Altieri MA, Wilson RC, Schmidt LL (1985) The effects of living mulches and weed cover on the dynamics of foliage- and soil-arthropod communities in three crop systems. Crop Prot 4:201–213

    Article  Google Scholar 

  • Andow DA (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36:561–586

    Article  Google Scholar 

  • Andow DA, Nicholson AG, Wien HC, Willson HR (1986) Insect populations on cabbage grown with living mulches. Environ Entomol 15:293–299

    Google Scholar 

  • Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234

    Article  Google Scholar 

  • Aquilino KM, Cardinale BJ, Ives AR (2005) Reciprocal effects of host plant and natural enemy diversity on herbivore suppression: an empirical study of a model tritrophic system. Oikos 108:275–282

    Article  Google Scholar 

  • Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20

    Article  Google Scholar 

  • Bommarco R, Banks JE (2003) Scale as modifier in vegetation diversity experiments: effects on herbivores and predators. Oikos 102:440–448

    Article  Google Scholar 

  • Caillaud MC (1999) Behavioural correlates of genetic divergence due to host specialization in the pea aphid, Acyrthosiphon pisum. Entomol Exp Appl 91:227–232

    Article  Google Scholar 

  • Cartwright B, Roberts BW, Hartz TK, Edelson JV (1990) Effects of mulches on the population increase of Myzus persicae (Sulzer) on bell peppers. Southwest Entomol 15:475–479

    Google Scholar 

  • Coll M, Bottrell DG (1994) Effects of nonhost plants on an insect herbivore in diverse habitats. Ecology 75:723–731

    Article  Google Scholar 

  • Costello MJ (1995) Spectral reflectance from a broccoli crop with vegetation or soil as background: influence on immigration by Brevicoryne brassicae and Myzus persicae. Entomol Exp Appl 75:109–118

    Article  Google Scholar 

  • Cronin JT (2009) Habitat edges, within-patch dispersion of hosts, and parasitoid oviposition behavior. Ecology 90:196–207

    PubMed  Article  Google Scholar 

  • Davis PM, Fick GW (1995) Potato leafhopper management: effects on production and quality of alfalfa-timothy mixtures. Agron J 87:795–804

    Article  Google Scholar 

  • Degooyer TA, Pedico LP, Rice ME (1999) Effect of alfalfa-grass intercrops on insect populations. Environ Entomol 28:703–710

    Google Scholar 

  • Dempster JP, Coaker TH (1974) Diversification of crop ecosystems as a means of controlling pests. In: Price-Jones D, Solomon ME (eds) Biology in pest and disease control. Blackwell, Oxford, pp 106–114

    Google Scholar 

  • Finch S, Collier RH (2000) Host-plant selection by insects—a theory based on ‘appropriate/inappropriate landings’ by pest insects on cruciferous plants. Entomol Exp Appl 96:91–102

    Article  Google Scholar 

  • Flinn PW, Hower AA, Kneivel DP (1990) Physiological response of alfalfa to injury by Empoasca fabae (Homoptera: Cicadellidae). Environ Entomol 19:176–181

    Google Scholar 

  • Granovsky AA (1928) Alfalfa “yellow top” and leafhoppers. J Econ Entomol 21:261–267

    Google Scholar 

  • Gratton C, Denno RF (2003) Seasonal shift from bottom-up to top-down impact in phytophagous insect populations. Oecologia 134:487–495

    PubMed  Google Scholar 

  • Grevstad FS, Klepetka BW (1992) The influence of plant architecture on the foraging efficiencies of a suite of ladybird beetles feeding on aphids. Oecologia 92:399–404

    Article  Google Scholar 

  • Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JMH, Tilman D (2009) Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett 12:1029–1039

    PubMed  Article  Google Scholar 

  • Harmon JP, Ives AR, Losey JE, Olson AC (2000) Coleomegilla maculata (Coleoptera: Coccinellidae) predation on pea aphids promoted by proximity to dandelions. Oecologia 125:543–548

    Article  Google Scholar 

  • Hom DJ (1988) Parasitism of cabbage aphid and green peach aphid (Homoptera: Aphididae) on collards in relation to weed management. Environ Entomol 17:354–358

    Google Scholar 

  • Hoy MD, Moore KJ, George JR, Brummer EC (2002) Alfalfa yield and quality as influenced by establishment method. Agron J 94:65–71

    Article  Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • Hutchins SH, Pedigo LP (1990) Phenological disruption and economic consequence of injury to alfalfa induced by potato leafhopper (Homoptera: Cicadellidae). J Econ Entomol 83:1587–1594

    Google Scholar 

  • Hutchinson WD, Hogg DB (1984) Demographic statistics for the pea aphid (Homoptera: Aphididae) in Wisconsin and a comparison with other populations. Environ Entomol 13:1173–1181

    Google Scholar 

  • Jannsen AM, Sabelis W, Magalhaes S, Montserrat M, van der Hammen T (2007) Habitat structure affects intraguild predation. Ecology 88:2713–2719

    Article  Google Scholar 

  • Kareiva P, Sahakian R (1990) Tritrophic effects of a single architectural mutation in pea plants. Nature 345:433–434

    Article  Google Scholar 

  • Koricheva J, Mulder CPH, Schmid B, Joshi J, Huss-Dannell K (2000) Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia 125:271–282

    Article  Google Scholar 

  • Lamp WO (1991) Reduced Empoasca fabae (Homoptera: Cicadellidae) density in oat-alfalfa intercrop systems. Environ Entomol 20:118–126

    Google Scholar 

  • Lamp WO, Morris MJ, Armbrust EJ (1984a) Suitability of common weed species as host plants for Potato leafhopper. Entomol Exp Appl 36:125–131

    Article  Google Scholar 

  • Lamp WO, Barney RJ, Armbrust EJ, Kapusta G (1984b) Selective weed control in spring-planted alfalfa: effect on leafhoppers and planthoppers (Auchenorrhyncha) with emphasis on potato leafhopper. Environ Entomol 13:207–213

    Google Scholar 

  • Lamp WO, Nielson GR, Danielson SD (1994) Patterns among host plants of potato leafhopper, Empoasca fabae (Homoptera: Cicadellidae). J Kans Entomol Soc 67:354–368

    Google Scholar 

  • Lancashire PD, Bleiholder H, Van Den Boom T, Langelüdeke P, Stauss R, Weber E, Witzenberger A (1979) A uniform decimal code for growth stages of crops and weeds. Ann Appl Biol 93:221–234

    Article  Google Scholar 

  • Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    PubMed  Article  CAS  Google Scholar 

  • Letourneau DK, Armbrecht I, Rivera BS, Lerma JM, Carmona EJ, Daza MC, Escobar S, Galindo V, Gutierrez C, Lopez SD, Mejia JL, Rangel AMA, Rangel JH, Rivera L, Saavedra CA, Torres AM, Trujillo AR (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21

    PubMed  Article  Google Scholar 

  • Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions. Bioscience 48:25–34

    Article  Google Scholar 

  • Losey JE, Eubanks MD (2000) Implications of pea aphid host-plant specialization for the potential colonization of vegetables following post-harvest emigration from forage crops. Environ Entomol 29:1283–1288

    Article  Google Scholar 

  • Martinez DG, Pienkowski RL (1982) Laboratory studies on insect predators of potato leafhopper eggs, nymphs, and adults. Environ Entomol 11:361–362

    Google Scholar 

  • McNamara JM, Houston AI (1987) Starvation and predation as factors limiting population size. Ecology 68:1515–1519

    Article  Google Scholar 

  • Nielson GR, Lamp WO, Stutte GW (1990) Potato leafhopper (Homoptera: Cicadellidae) feeding disruption of phloem translocation in alfalfa. J Econ Entomol 83:807–813

    Google Scholar 

  • Oloumi-Sadeghi H, Zavaleta LR, Lamp WO, Armbrust EJ, Kapusta G (1987) Interactions of the potato leafhopper (Homoptera: Cicadellidae) with weeds in an alfalfa ecosystem. Environ Entomol 16:1175–1180

    Google Scholar 

  • Otway SJ, Hector A, Lawton JH (2005) Resource dilution effects on specialist insect herbivores in a grassland biodiversity experiment. J Anim Ecol 74:234–240

    Article  Google Scholar 

  • Rensner PE, Lamp WO, Barney RJ, Armbrust EJ (1983) Feeding tests of Nabis roseipennis (Hemiptera: Nabidae) on potato leafhopper, Empoasca fabae (Homoptera: Cicadellidae) and their movement into spring-planted alfalfa. J Kans Entomol Soc 56:446–453

    Google Scholar 

  • Risch SJ, Andow D, Altieri MA (1983) Agroecosystem diversity and pest control: data, tentative conclusions, and new research directions. Environ Entomol 12:625–629

    Google Scholar 

  • Roda AL, Landis DA, Coggins ML (1997a) Forage grasses elicit emigration of adult potato leafhopper (Homoptera: Cicadellidae) from alfalfa-grass mixtures. Environ Entomol 26:745–753

    Google Scholar 

  • Roda AL, Landis DA, Miller JR (1997b) Contact-induced emigration of potato leafhopper (Homoptera: Cicadellidae) from alfalfa-forage grass mixtures. Environ Entomol 26:754–762

    Google Scholar 

  • Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleraceae). Ecol Monogr 43:95–124

    Article  Google Scholar 

  • Russell EP (1989) Enemies hypothesis: a review of the effect of vegetational diversity on predatory insects and parasitoids. Environ Entomol 18:590–599

    Google Scholar 

  • SAS Institute Inc (2008) JMP 8 Introductory Guide. Cary, NC, SAS Institute Inc

  • Scherber C, Mwangi PN, Temperton VM, Roscher C, Schumacher J, Schmid B, Weisser WW (2006) Effects of plant diversity on invertebrate herbivory in experimental grassland. Oecologia 147:489–500

    PubMed  Article  Google Scholar 

  • Scherber C et al (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468:553–556

    PubMed  Article  CAS  Google Scholar 

  • Sheehan W (1986) Response by specialist and generalist natural enemies to agroecosystem diversification: a selective review. Environ Entomol 15:456–461

    Google Scholar 

  • Smith JG (1976) Influence of crop background on natural enemies of aphids on Brussels sprouts. Ann Appl Biol 83:15–29

    Article  Google Scholar 

  • Tahvanianen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta crucifera (Coleoptera: Chrysomelidae). Oecologia 10:321–346

    Article  Google Scholar 

  • Thiery D, Visser JH (1986) Masking of host plant odor in the olfactory orientation of the Colorado potato beetle. Entomol Exp Appl 41:165–172

    Article  Google Scholar 

  • Tylianakis JM, Didham RK, Wratten SD (2004) Improved fitness of aphid parasitoids receiving resource subsidies. Ecology 85:658–666

    Article  Google Scholar 

  • Visser JH, Taanman JW (1987) Odor-conditioned anemotaxis of apterous aphids (Cryptomyzus korschelti) in response to host plants. Physiol Entomol 12:473–479

    Article  Google Scholar 

  • Weiser Relandson LA, Obrycki JJ (2010) Predation of immature and adult Empoasca fabae (Harris) (Hemiptera: Cicadellidae) by three species of predatory insects. J Kans Entomol Soc 83:1–6

    Article  Google Scholar 

  • Wilkinson TL, Douglas AE (1998) Plant penetration by pea aphids (Acyrthosiphon pisum) of different plant range. Entomol Exp Appl 87:43–50

    Article  Google Scholar 

  • Wilson MR, Leather SR (2012) The effect of past natural enemy activity on host-plant preference of two aphid species. Entomol Exp Appl 144:216–222

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Inc, Englewood Cliffs

    Google Scholar 

Download references

Acknowledgments

The authors thank the Ursinus College Department of Biology and the UC Summer Fellows Program for financial support. The authors also offer their thanks to Matthew Wismer of Northern Star Farm for providing access to his alfalfa field, Cody Nagy for field assistance, George Didden Greenhouses, Inc. for the pots used in the experiment, and William Snyder, Mattias Jonsson, and two anonymous reviewers for providing valuable comments on the manuscript.

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Correspondence to Cory S. Straub.

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Communicated by T. Haye.

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Straub, C.S., Simasek, N.P., Gapinski, M.R. et al. Influence of nonhost plant diversity and natural enemies on the potato leafhopper, Empoasca fabae, and pea aphid, Acyrthosiphon pisum, in alfalfa. J Pest Sci 86, 235–244 (2013). https://doi.org/10.1007/s10340-012-0465-7

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Keywords

  • Predator
  • Parasitoid
  • Pest
  • Diversity