Oecologia

, Volume 182, Issue 1, pp 189–202 | Cite as

Inter-varietal interactions among plants in genotypically diverse mixtures tend to decrease herbivore performance

Plant-microbe-animal interactions - original research

Abstract

Much research has explored the effects of plant species diversity on herbivore populations, but far less has considered effects of plant genotypic diversity, or how abiotic stressors, like drought, can modify effects. Mechanisms by which plant genotypic diversity affects herbivore populations remain largely unresolved. We used greenhouse studies with a model system of wheat (Triticum aestivum L.) and bird cherry-oat aphid (Rhopalosiphum padi L.) to determine whether the genotypic diversity of a plant’s neighborhood influences performance and fitness of herbivores on a focal plant and if drought changes the influence of neighborhood diversity. Taken across all varieties we tested, plant–plant interactions in diverse neighborhoods reduced aphid performance and generated associational resistance, although effects on aphids depended on variety identity. In diverse mixtures, drought stress greatly diminished the genotypic diversity-driven reduction in aphid performance. Neighborhood diversity influenced mother aphid size, and appeared to partially explain how plant–plant interactions reduced the number of offspring produced in mixtures. Plant size did not mediate effects on aphid performance, although neighborhood diversity reduced plant mass across varieties and watering treatments. Our results suggest inter-varietal interactions in genotypic mixtures can affect herbivore performance in the absence of herbivore movement and that abiotic stress may diminish any effects. Accounting for how neighborhood diversity influences resistance of an individual plant to herbivores will help aid development of mixtures of varieties for managing insect pests and clarify the role of plant genotypic diversity in ecosystems.

Keywords

Associational resistance Drought Genotypic diversity Intraspecific diversity Stress 

Supplementary material

442_2016_3651_MOESM1_ESM.docx (3 mb)
Supplementary material (DOCX 3073 kb)

References

  1. Andow DA (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36:561–586. doi:10.1146/annurev.en.36.010191.003021 CrossRefGoogle Scholar
  2. Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543. doi:10.1093/jxb/ers100 CrossRefPubMedGoogle Scholar
  3. Barbosa P, Hines J, Kaplan I et al (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20. doi:10.1146/annurev.ecolsys.110308.120242 CrossRefGoogle Scholar
  4. Behmer ST, Simpson SJ, Raubenheimer D (2014) Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 83:2489–2501. doi:10.1890/0012-9658(2002)083[2489:HFICHE]2.0.CO;2Google Scholar
  5. Biedrzycki ML, Bais HP (2010) Kin recognition in plants: a mysterious behaviour unsolved. J Exp Bot 61:4123–4128. doi:10.1093/jxb/erq250 CrossRefPubMedGoogle Scholar
  6. Cahill JF Jr (2002) Interactions between root and shoot competition vary among species. Oikos 99:101–112. doi:10.1034/j.1600-0706.2002.990111.x CrossRefGoogle Scholar
  7. Chen BJW, During HJ, Anten NPR (2012) Detect thy neighbor: identity recognition at the root level in plants. Plant Sci 195:157–167. doi:10.1016/j.plantsci.2012.07.006 CrossRefPubMedGoogle Scholar
  8. Cook-Patton SC, McArt SH, Parachnowitsch AL et al (2011) A direct comparison of the consequences of plant genotypic and species diversity on communities and ecosystem function. Ecology 92:915–923. doi:10.1890/10-0999.1 CrossRefPubMedGoogle Scholar
  9. Cowger C, Weisz R (2008) Winter wheat blends (mixtures) produce a yield advantage in North Carolina. Agron J 100:169–177. doi:10.2134/agronj2007.0128 CrossRefGoogle Scholar
  10. Crutsinger GM, Collins MD, Fordyce JA et al (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968. doi:10.1126/science.1128326 CrossRefPubMedGoogle Scholar
  11. Crutsinger GM, Reynolds WN, Classen AT, Sanders NJ (2008) Disparate effects of plant genotypic diversity on foliage and litter arthropod communities. Oecologia 158:65–75. doi:10.1007/s00442-008-1130-y CrossRefPubMedGoogle Scholar
  12. Delory BM, Delaplace P, Fauconnier M-L, du Jardin P (2016) Root-emitted volatile organic compounds: can they mediate belowground plant–plant interactions? Plant Soil 402:1–26. doi:10.1007/s11104-016-2823-3 CrossRefGoogle Scholar
  13. Dı́az S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. doi:10.1016/S0169-5347(01)02283-2 CrossRefGoogle Scholar
  14. Dixon AFG (1976) Timing of egg hatch and viability of the sycamore aphid, Drepanosiphum platanoidis (Schr.), at bud burst of sycamore, Acer pseudoplatanus L. J Anim Ecol 45:593–603. doi:10.2307/3893 CrossRefGoogle Scholar
  15. Dudley S, File A (2007) Kin recognition in an annual plant. Biol Lett 3:435–438. doi:10.1098/rsbl.2007.0232 CrossRefPubMedPubMedCentralGoogle Scholar
  16. File AL, Murphy GP, Dudley SA (2012) Fitness consequences of plants growing with siblings: reconciling kin selection, niche partitioning and competitive ability. Proc R Soc B 279:209–218. doi:10.1098/rspb.2011.1995 CrossRefPubMedGoogle Scholar
  17. Finch S, Collier RH (2000) Host-plant selection by insects—a theory based on “appropriate/inappropriate landings” by pest insects of cruciferous plants. Entomol Exp Appl 96:91–102. doi:10.1023/A:1004058518179 CrossRefGoogle Scholar
  18. Foster W, Benton T (1992) Sex ratio, local mate competition and mating behaviour in the aphid Pemphigus spyrothecae. Behav Ecol Sociobiol 30:297–307CrossRefGoogle Scholar
  19. Genung MA, Crutsinger GM, Bailey JK et al (2012) Aphid and ladybird beetle abundance depend on the interaction of spatial effects and genotypic diversity. Oecologia 168:167–174. doi:10.1007/s00442-011-2080-3 CrossRefPubMedGoogle Scholar
  20. Glinwood R, Pettersson J, Ahmed E et al (2003) Change in acceptability of barley plants to aphids after exposure to allelochemicals from couch-grass (Elytrigia repens). J Chem Ecol 29:261–274. doi:10.1023/A:1022687025416 CrossRefPubMedGoogle Scholar
  21. Glinwood R, Ahmed E, Qvarfordt E et al (2009) Airborne interactions between undamaged plants of different cultivars affect insect herbivores and natural enemies. Arthropod Plant Interact 3:215–224. doi:10.1007/s11829-009-9072-9 CrossRefGoogle Scholar
  22. Glinwood R, Ninkovic V, Pettersson J (2011) Chemical interaction between undamaged plants—effects on herbivores and natural enemies. Phytochemistry 72:1683–1689. doi:10.1016/j.phytochem.2011.02.010 CrossRefPubMedGoogle Scholar
  23. Grettenberger I, Tooker J (2015) Moving beyond resistance management toward an expanded role for seed mixtures in agriculture. Agric Ecosyst Environ 208:29–36. doi:10.1016/j.agee.2015.04.019 CrossRefGoogle Scholar
  24. Hambäck PA, Inouye B, Andersson P, Underwood N (2014) Effects of plant neighborhoods on plant–herbivore interactions: resource dilution and associational effects. Ecology 95:1370–1383. doi:10.1890/13-0793.1 CrossRefPubMedGoogle Scholar
  25. Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85:1383–1398. doi:10.1890/03-0352 CrossRefGoogle Scholar
  26. Hughes AR, Inouye BD, Johnson MTJ et al (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623. doi:10.1111/j.1461-0248.2008.01179.x CrossRefPubMedGoogle Scholar
  27. Johnson MTJ, Agrawal AA (2005) Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874–885. doi:10.1890/04-1068 CrossRefGoogle Scholar
  28. Johnson MTJ, Lajeunesse MJ, Agrawal AA (2006) Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol Lett 9:24–34. doi:10.1111/j.1461-0248.2005.00833.x PubMedGoogle Scholar
  29. Karban R, Yang LH, Edwards KF (2014) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52. doi:10.1111/ele.12205 CrossRefPubMedGoogle Scholar
  30. Karley SJ, Douglas AE, Parker WE (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. J Exp Biol 205:3009–3018PubMedGoogle Scholar
  31. Kellner M, Brantestam AK, Ahman I, Ninkovic V (2010) Plant volatile-induced aphid resistance in barley cultivars is related to cultivar age. Theor Appl Genet 121:1133–1139. doi:10.1007/s00122-010-1377-7 CrossRefPubMedGoogle Scholar
  32. Kiær L, Skovgaard I, Østergård H (2006) Meta-analysis is a powerful tool to summarize variety mixture effects—exemplified by grain yield and weed suppression of spring barley. In: Proceedings of the COST SUSVAR workshop on cereal crop diversity: implications for production and products, La Besse, France, pp 49–52Google Scholar
  33. Kieckhefer RW, Kantack BH (1988) Yield losses in winter grains caused by cereal aphids (Homoptera: Aphididae) in South Dakota. J Econ Entomol 81:317–321. doi:10.1093/jee/81.1.317 CrossRefGoogle Scholar
  34. Kotowska AM, Cahill JF Jr, Keddie BA (2010) Plant genetic diversity yields increased plant productivity and herbivore performance. J Ecol 98:237–245. doi:10.1111/j.1365-2745.2009.01606.x CrossRefGoogle Scholar
  35. Letourneau DK, Armbrecht I, Rivera BS et al (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl 21:9–21. doi:10.1890/09-2026.1 CrossRefPubMedGoogle Scholar
  36. McArt SH, Thaler JS (2013) Plant genotypic diversity reduces the rate of consumer resource utilization. Proc R Soc B 280:20130639. doi:10.1098/rspb.2013.0639 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mulder CP, Uliassi DD, Doak DF (2001) Physical stress and diversity–productivity relationships: the role of positive interactions. Proc Natl Acad Sci 98:6704–6708. doi:10.1073/pnas.111055298 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Mundt CC (2002) Use of multiline cultivars and cultivar mixtures for disease management. Annu Rev Phytopathol 40:381–410. doi:10.1146/annurev.phyto.40.011402.113723 CrossRefPubMedGoogle Scholar
  39. Nicol CMY, Mackauer M (1999) The scaling of body size and mass in a host parasitoid association: influence of host species and stage. Entomol Exp Appl 90:83–92. doi:10.1046/j.1570-7458.1999.00425.x CrossRefGoogle Scholar
  40. Ninkovic V, Glinwood R, Dahlin I (2009) Weed–barley interactions affect plant acceptance by aphids in laboratory and field experiments. Entomol Exp Appl 133:38–45. doi:10.1111/j.1570-7458.2009.00900.x CrossRefGoogle Scholar
  41. Peltonen-Sainio P, Karjalainen R (1991) Agronomic evaluation of growing oat cultivar mixtures under various stress conditions in Finland. Acta Agric Scand 41:47–53. doi:10.1080/00015129109438582 CrossRefGoogle Scholar
  42. Poveda K, Gómez M, Martínez E (2008) Diversification practices: their effect on pest regulation and production. Rev Colomb Entomol 34:131–144Google Scholar
  43. Power AG (1988) Leafhopper response to genetically diverse maize stands. Entomol Exp Appl 49:213–219. doi:10.1111/j.1570-7458.1988.tb01182.x CrossRefGoogle Scholar
  44. Power AG (1991) Virus spread and vector dynamics in genetically diverse plant populations. Ecology 72:232–241. doi:10.2307/1938917 CrossRefGoogle Scholar
  45. Prieto I, Violle C, Barre P et al (2015) Complementary effects of species and genetic diversity on productivity and stability of sown grasslands. Nat Plants 1:1–5. doi:10.1038/nplants.2015.33 Google Scholar
  46. Reusch TBH, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci 102:2826–2831. doi:10.1073/pnas.0500008102 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Schädler M, Brandl R, Haase J (2007) Antagonistic interactions between plant competition and insect herbivory. Ecology 88:1490–1498. doi:10.1890/06-0647 CrossRefPubMedGoogle Scholar
  48. Schlapfer F, Schmid B (1999) Ecosystem effects of biodiversity: a classification of hypotheses and exploration of empirical results. Ecol Appl 9:893–912. doi:10.1890/1051-0761(1999)009[0893:EEOBAC]2.0.CO;2Google Scholar
  49. Schmelz EA, Engelberth J, Alborn HT et al (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Natl Acad Sci 100:10552–10557. doi:10.1073/pnas.1633615100 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Schmelz EA, Engelberth J, Tumlinson JH et al (2004) The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant J 39:790–808. doi:10.1111/j.1365-313X.2004.02168.x CrossRefPubMedGoogle Scholar
  51. Shoffner AV, Tooker JF (2013) The potential of genotypically diverse cultivar mixtures to moderate aphid populations in wheat (Triticum aestivum L.). Arthropod Plant Interact 7:33–43. doi:10.1007/s11829-012-9226-z CrossRefGoogle Scholar
  52. Simpson SJ, Raubenheimer D (2001) The geometric analysis of nutrient–allelochemical interactions: a case study using locusts. Ecology 82:422–439. doi:10.1890/0012-9658(2001)082[0422:TGAONA]2.0.CO;2Google Scholar
  53. Smithson JB, Lenné JM (1996) Varietal mixtures: a viable strategy for sustainable productivity in subsistence agriculture. Ann Appl Biol 128:127–158. doi:10.1111/j.1744-7348.1996.tb07096.x CrossRefGoogle Scholar
  54. Sokal R, Rohlf F (1995) Biometry, 3rd edn. W. H. Freeman and Company, New YorkGoogle Scholar
  55. Steudel B, Hautier Y, Hector A, Kessler M (2011) Diverse marsh plant communities are more consistently productive across a range of different environmental conditions through functional complementarity. J Appl Ecol 48:1117–1124. doi:10.1111/j.1365-2664.2011.01986.x CrossRefGoogle Scholar
  56. Tahvanainen JO, Root RB (1972) The influence of vegetational diversity on the population ecology of a specialized herbivore, Phyllotreta cruciferae (Coleoptera: Chrysomelidae). Oecologia 10:321–346. doi:10.1007/BF00345736 CrossRefGoogle Scholar
  57. Tonhasca A, Byrne DN (1994) The effects of crop diversification on herbivorous insects: a meta-analysis approach. Ecol Entomol 19:239–244. doi:10.1111/j.1365-2311.1994.tb00415.x CrossRefGoogle Scholar
  58. Tooker JF, Frank SD (2012) Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. J Appl Ecol 49:974–985. doi:10.1111/j.1365-2664.2012.02173.x CrossRefGoogle Scholar
  59. Underwood N, Halpern S, Klein C (2011) Effect of host-plant genotype and neighboring plants on strawberry aphid movement in the greenhouse and field. Am Midl Nat 165:38–49. doi:10.1674/0003-0031-165.1.38 CrossRefGoogle Scholar
  60. Utsumi S, Ando Y, Craig TP, Ohgushi T (2011) Plant genotypic diversity increases population size of a herbivorous insect. Proc R Soc B 278:3108–3115. doi:10.1098/rspb.2011.0239 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Walling L (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216. doi:10.1007/s003440000026 PubMedGoogle Scholar
  62. Wolfe M (1985) The current status and prospects of multiline cultivars and variety mixtures for disease. Annu Rev Phytopathol 23:251–273. doi:10.1146/annurev.py.23.090185.001343 CrossRefGoogle Scholar
  63. Zadok JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421. doi:10.1111/j.1365-3180.1974.tb01084.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of EntomologyThe Pennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of EntomologyUniversity of CaliforniaDavisUSA

Personalised recommendations