BioEnergy Research

, Volume 8, Issue 3, pp 1275–1283 | Cite as

Bioenergy Crops and Natural Enemies: Host Plant-Mediated Effects of Miscanthus on the Aphid Parasitoid Lysiphlebus testaceipes

  • G. Doury
  • J. Pottier
  • A. Ameline
  • A. Mennerat
  • F. Dubois
  • C. Rambaud
  • A. Couty


Miscanthus spp. are biofuel crops that are triggering growing interest worldwide due to their numerous agronomic advantages. Though breeding programs take into account usual key plant traits of agronomic interest (e.g., biomass production, adaptation to broader climatic range), they generally overlook plant attributes relating to pest and pathogen resistance and even more those that may favor or improve the combined use of biological control agents of pests. A recent study showed that the parental species, Miscanthus sacchariflorus and, to a lesser extent, Miscanthus sinensis, were less suitable and acceptable host plants for the corn leaf aphid Rhopalosiphum maidis, one of the main pests of Miscanthus × giganteus in the USA, than the hybrid M. × giganteus. In the present laboratory study, we investigated the host plant-mediated effects of these three miscanthus species on various life history traits of the aphid parasitoid Lysiphlebus testaceipes. A clear host plant effect was shown on aphid size and, consequently, on parasitoid fitness parameters. High plant resistance to aphids was shown to be more detrimental to the parasitoid than partial resistance, with M. sacchariflorus being the least suitable host plant to both aphid and parasitoid development. Selection of partial resistance, such as the one exhibited by M. sinensis, should then be preferred to support efficient aphid regulation by parasitoids. This study provides the first contribution to the evaluation of bottom-up effects of a biofuel crop on beneficial insects. It also underlines the need to conduct additional research when considering the implementation of new biomass crops.


Biofuel crop Miscanthus spp Host plant resistance Tritrophic interactions Rhopalosiphum maidis Lysiphlebus testaceipes 



We would like to acknowledge the financial support from the Picardie region (research project MISC PIC). We also thank Gérard Labonne (UMR BGPI, Montpellier, France) for providing the R. maidis population. Viridaxis (Gosselies, Belgium) is thanked for providing the L. testaceipes mummies for the experiments. Andrew Roots is thanked for critical reading of the manuscript, especially concerning the English language.


  1. 1.
    Bonnin C, Lal R (2012) Agronomic and ecological implications of biofuels. In: Sparks DL (ed) Advances in agronomy. Elsevier pp 1-50. doi: 10.1016/B978-0-12-394278-4.00001-5
  2. 2.
    Landis DA, Gardiner MM, Van Der Werf W, Swinton SM (2008) Increasing corn for biofuel production reduces biocontrol services in agricultural landscapes. Proc Natl Acad Sci U S A 105:20552–20557PubMedCentralCrossRefPubMedGoogle Scholar
  3. 3.
    Thomson LJ, Hoffmann AA (2011) Pest management challenges for biofuel crop production. Curr Opin Environ Sustain 3:95–99. doi: 10.1016/j.cosust.2010.11.00.3 CrossRefGoogle Scholar
  4. 4.
    Cook JH, Beyea J, Keeler KH (1991) Potential impacts of biomass production in the United States on biological diversity. Annu Rev Energ Environ 16:401–431CrossRefGoogle Scholar
  5. 5.
    Naylor RL, Liska AJ, Burke MB, Falcon WP, Gaskell JC, Rozelle SD, Cassman K (2007) The ripple effect: biofuels, food security, and the environment. Environment 49:30–43CrossRefGoogle Scholar
  6. 6.
    Tilman D, Socolow R, Foley JA et al (2009) Beneficial biofuels—the food, energy, and environment trilemma. Science 325:270–271CrossRefPubMedGoogle Scholar
  7. 7.
    Danielsen F, Beukema H, Burgess ND et al (2009) Biofuel plantations on forested lands: double jeopardy for biodiversity and climate. Conserv Biol 23:348–358CrossRefPubMedGoogle Scholar
  8. 8.
    Fletcher RJ Jr, Robertson BA, Evans J, Doran PJ, Alavalapati JRR, Schemske DW (2011) Biodiversity conservation in the era of biofuels: risks and opportunities. Front Ecol Environ 9:161–168CrossRefGoogle Scholar
  9. 9.
    Landis DA, Wherling BP (2010) Arthropods and biofuel production systems in North America. Insect Sci 17:220–236. doi: 10.1111/j.1744-7917.2009.01310.x CrossRefGoogle Scholar
  10. 10.
    Frank SD, Shrewsbury PM, Esiekpe O (2008) Spatial and temporal variation in natural enemy assemblages on Maryland native plant species. Environ Entomol 37:478–486CrossRefPubMedGoogle Scholar
  11. 11.
    Carmona DM, Menalled FD, Landis DA (1999) Gryllus pennsylvanicus (Orthoptera: Gryllidae): laboratory weed seed predation and within field activity-density. J Econ Entomol 92:825–829CrossRefGoogle Scholar
  12. 12.
    Menalled FD, Lee JC, Landis DA (2001) Herbaceous filter strips in agroecosystems: implications for ground beetle (Coleoptera: Carabidae) conservation and invertebrate weed seed predation. Great Lakes Entomol 34:77–91Google Scholar
  13. 13.
    Gardiner MM, Tuell JK, Isaacs R, Gibbs J, Ascher JS, Landis DA (2010) Implications of three model biofuel crops for beneficial arthropods in agricultural landscapes. Bioenerg Res 3:6–19. doi: 10.1007/s12155-009-9065-7 CrossRefGoogle Scholar
  14. 14.
    Jakob K, Zhou F, Paterson AH (2009) Genetic improvement of C4 grasses as cellulosic biofuel feedstocks. In Vitro Cell Dev Biol Plant 45:291–305CrossRefGoogle Scholar
  15. 15.
    Zub HW, Arnoult S, Brancourt-Hulmel M (2011) Key traits for biomass production identified in different Miscanthus species at two harvest dates. Biomass Bioenerg 35:637–651. doi: 10.1016/j.biombioe.2010.10.020 CrossRefGoogle Scholar
  16. 16.
    Lewandowski I, Clifton-Brown JC, Scurlockc JMO, Huismand W (2000) Miscanthus: European experience with a novel energy crop. Biomass Bioenerg 19:209–227CrossRefGoogle Scholar
  17. 17.
    Prasifka JR, Bradshaw JD, Meagher RL, Nagoshi RN, Steffey KL, Gray ME (2009) Development and feeding of fall armyworm on Miscanthus × giganteus and switchgrass. J Econ Entomol 102:2154–2159CrossRefPubMedGoogle Scholar
  18. 18.
    Spencer JL, Raghu S (2009) Refuge or reservoir? The potential impacts of the biofuel crop Miscanthus x giganteus on a major pest of maize. PLoS ONE 4:e8336. doi: 10.1371/journal.pone.0008336 PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Gloyna K, Thieme T, Zellner M (2011) Miscanthus, a host for larvae of a European population of Diabrotica v. virgifera. J. Appl Entomol 135:780–785. doi: 10.1111/j.1439-0418.2010.01599.x CrossRefGoogle Scholar
  20. 20.
    Bradshaw JD, Prasifka JR, Steffey KL, Gray ME (2010) First report of field populations of two potential aphid pests of the bioenergy crop Miscanthus x giganteus. Fla Entomol 93:135–137. doi: 10.1653/024.093.0123 CrossRefGoogle Scholar
  21. 21.
    Semere T, Slater FM (2007) Invertebrate populations in miscanthus (Miscanthus x giganteus) and reed canary-grass (Phalaris arundinacea) fields. Biomass Bioenerg 31:30–39. doi: 10.1016/j.biombioe.2006.07.002 CrossRefGoogle Scholar
  22. 22.
    Stanley DA, Stout JC (2013) Quantifying the impacts of bioenergy crops on pollinating insect abundance and diversity: a field-scale evaluation reveals taxon-specific responses. J Appl Ecol 50:335–344. doi: 10.1111/1365-2664.12060 CrossRefGoogle Scholar
  23. 23.
    Takahashi K (1997) Use of Coccinella septempunctata brucki Mulsant as a biological agent for controlling alfalfa aphids. Jpn Agric Res Q 31:101–108Google Scholar
  24. 24.
    Gordon R, Davidson J (2008) A new prey record and range extension for Hyperaspis paludicola Schwarz and a new prey record for Microwesia misella (LeConte) (Coleoptera: Coccinellidae). Insect Mundi 43:1–2Google Scholar
  25. 25.
    Gottwald R, Adam L (1998) Ergebnisse zu entomologischen erhebungen und zur unkrautbekämpfung bei miscanthus und anderen c4‐pflanzen. Arch Phytopathol Plant Protect 31:377–386. doi: 10.1080/03235409809383248 CrossRefGoogle Scholar
  26. 26.
    Thomas M, Waage J (1996) Integration of biological control and host-plant resistance breeding: a scientific and literature review. CTA-CAB International, Wageningen, 71 ppGoogle Scholar
  27. 27.
    Bottrell DG, Barbosa P, Gould F (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annu Rev Entomol 43:347–367. doi: 10.1146/annurev.ento.43.1.347 CrossRefPubMedGoogle Scholar
  28. 28.
    Cortesero AM, Stapel JO, Lewis WJ (2000) Understanding and manipulating plant attributes to enhance biological control. Biol Control 17:35–49CrossRefGoogle Scholar
  29. 29.
    Pointeau S, Jaguenet E, Couty A, Dubois F, Rambaud C, Ameline A (2014) Differential performance and behavior of the corn leaf aphid Rhopalosiphum maidis, on three species of the biomass crop Miscanthus. Ind Crop Prod 54:135–141. doi: 10.1016/j.indcrop.2014.01.018 CrossRefGoogle Scholar
  30. 30.
    van Emden HF (1995) Host-plant aphidophaga interactions. Agric Ecosyst Environ 52:3–11CrossRefGoogle Scholar
  31. 31.
    Holt RD, Lawton JH, Polis GA, Martinez ND (1999) Trophic-rank and the species-area relationship. Ecology 80:1495–1504. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  32. 32.
    Tscharntke T, Brandl R (2004) Plant-insect interactions in fragmented landscapes. Annu Rev Entomol 49:405–430. doi: 10.1146/annurev.ento.49.061802.123339 CrossRefPubMedGoogle Scholar
  33. 33.
    Hopkinson JE, Zalucki MP, Murray DAF (2013) Host selection and parasitism behavior of Lysiphlebus testaceipes: role of plant, aphid species and instar. Biol Control 64:283–290. doi: 10.1016/j.biocontrol.2012.11.01 CrossRefGoogle Scholar
  34. 34.
    da Silva RE, Paes Bueno VH, Silva DB, Sampaio MV (2008) Tabela de vida de fertilidade de Lysiphlebus testaceipes (Cresson) Hymenoptera, Braconidae, Aphidiinae) em Rhopalosiphum maidis (Fitch) e Aphis gossypii Glover (Hemiptera, Aphididae). Rev Bras Entomologia 52:124–130Google Scholar
  35. 35.
    Zub HW, Rambaud C, Béthencourt L, Brancourt-Hulmel M (2012) Late emergence and rapid growth maximize the plant development of Miscanthus clones. Bioenerg Res 5:841–854. doi: 10.1007/s12155-012-9194-2 CrossRefGoogle Scholar
  36. 36.
    Rambaud C, Arnoult S, Bluteau A, Mansard MC et al (2013) Shoot organogenesis in three Miscanthus species and evaluation for genetic uniformity using AFLP analysis. Plant Cell Tiss Organ Cult 113:437–448. doi: 10.1007/s11240-012-0284-9 CrossRefGoogle Scholar
  37. 37.
    Down RE, Gatehouse AMR, Hamilton WDO, Gatehouse JA (1996) Snowdrop lectin inhibits development and decreases fecundity of the glasshouse potato aphid (Aulacorthum solani) when administered in vivo and via transgenic plants both in laboratory and glasshouse trials. J Insect Physiol 42:1035–1045CrossRefGoogle Scholar
  38. 38.
    Development Core Team R (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  39. 39.
    Kaiser-Arnaud L, Couty A, Cortesero AM (2013) La plante, un biotope de choix pour les entomophages. In: Sauvion N, Calatayud PA, Thiery D, Marion-Poll F (eds) Interactions insectes-plantes. Editions Quae, Versailles, FRA, p 461–481Google Scholar
  40. 40.
    Vinson SB, Iwantsch GF (1980) Host suitability for insect parasitoids. Annu Rev Entomol 25:397–419CrossRefGoogle Scholar
  41. 41.
    Sequeira R, Mackauer M (1992) Covariance of adult size and development time in the parasitoid wasp Aphidius ervi in relation to the size of its host, Acyrthosiphum pisum. Evol Ecol 6:34–44CrossRefGoogle Scholar
  42. 42.
    Godfray HCJ (1994) Parasitoids behavioral and evolutionary ecology. Princeton University Press, Princeton, NJ, p 788Google Scholar
  43. 43.
    Jowyk EA, Smilowitz Z (1978) A comparison of growth and development rates of the parasite Hyposoter exiguae reared from two instars of its host, Trichoplusia ni. Ann Entomol Soc Am 71:467–472CrossRefGoogle Scholar
  44. 44.
    Beckage NE, Templeton TJ (1985) Temporal synchronization of emergence of Hyposoter exiguae and H. fugitivus (Hymenoptera: Ichneumonidae) with apolysis preceding larval molting in Manduca sexta (Lepidoptera: Sphingidae). Ann Entomol Soc Am 78:775–782CrossRefGoogle Scholar
  45. 45.
    Gunasena GH, Vinson SB, Williams HJ (1989) Interrelationships between growth of Heliothis virescens (Lepidoptera: Noctuidae) and that of its parasitoid, Campoletis sonorensis (Hymenoptera: Ichneumonidae). Ann Entomol Soc Am 82:187–191CrossRefGoogle Scholar
  46. 46.
    Pettit FL, Wietlisbach DO (1993) Effects of host instar and size on parasitization efficiency and life history parameters of Opius dissitus. Entomol Exp Appl 66:227–236CrossRefGoogle Scholar
  47. 47.
    Croft P, Copland MJW (1995) The effect of host instar on the size and sex ratio of the endoparasitoid Dacnusa sibrica. Entomol Exp Appl 74:121–124CrossRefGoogle Scholar
  48. 48.
    Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford University Press, New York, p 516Google Scholar
  49. 49.
    Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Systemat 11:41–65Google Scholar
  50. 50.
    Hare JD (1992) Effects of plant variation on herbivore-natural enemy interactions. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens—ecology, evolution and genetics. The University of Chicago Press, Chicago, Illinois, pp 278–325Google Scholar
  51. 51.
    Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185CrossRefPubMedGoogle Scholar
  52. 52.
    Kester KM, Barbosa P (1991) Behavioral and ecological constraints imposed by plants on insect parasitoids: implications for biological control. Biol Control 1:94–106CrossRefGoogle Scholar
  53. 53.
    Koch KG, Bradshaw JD, Heng-Moss TM, Sarath G (2014) Categories of resistance to green bug and yellow sugarcane aphid (Hemiptera: Aphididae) in three tetraploid switchgrass populations. Bioenerg Res. doi: 10.1007/s12155-014-9420-1 Google Scholar
  54. 54.
    Koch KG, Fithian R, Heng-Moss TM, Bradshaw JD, Sarath G, Spilker C (2014) Evaluation of tetraploid switchgrass (Poales: Poaceae) populations for host suitability and differential resistance to four cereal aphids. J Econ Entomol 107:424–431. doi: 10.1603/EC13315 CrossRefPubMedGoogle Scholar
  55. 55.
    Chacón JM, Asplen MK, Heimpel GE (2014) Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field. Biol Control 60:16–25. doi: 10.1016/j.biocontrol.2011.09.003 CrossRefGoogle Scholar
  56. 56.
    Ode PJ, Crompton DS (2013) Compatibility of aphid resistance in soybean and biological control by the parasitoid Aphidius colemani (Hymenoptera: Braconidae). Biol Control 64:255–262. doi: 10.1016/j.biocontrol.2012.12.001 CrossRefGoogle Scholar
  57. 57.
    Hopper KR, Diers BW (2014) Parasitism of soybean aphid by Aphelinus species on soybean susceptible versus resistant to the aphid. Biol Control 76:101–106. doi: 10.1016/j.biocontrol.2014.05.006 CrossRefGoogle Scholar
  58. 58.
    Starks KJ, Muniappan R, Eikenbary RD (1972) Interaction between plant resistance and parasitism against the greenbug on barley and sorghum. Ann Entomol Soc Am 65:650–655CrossRefGoogle Scholar
  59. 59.
    Cai QN, Ma XM, Zhao X, Cao YZ, Yang XQ (2009) Effects of host plant resistance on insect pests and its parasitoid: a case study of wheat-aphid-parasitoid system. Biol Control 49:134–138. doi: 10.1016/j.biocontrol.2008.12.009 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • G. Doury
    • 1
  • J. Pottier
    • 1
  • A. Ameline
    • 1
  • A. Mennerat
    • 1
    • 3
  • F. Dubois
    • 1
  • C. Rambaud
    • 2
  • A. Couty
    • 1
  1. 1.EDYSAN Ecologie et Dynamique des Systèmes Anthropisés FRE 3498CNRS-UPJVAmiens Cedex 1France
  2. 2.UMR INRA 1281, Stress Abiotiques et Différenciation des Végétaux cultivésUniversité Lille Nord de FranceVilleneuve d’Ascq CedexFrance
  3. 3.Department of BiologyUniversity of BergenBergenNorway

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