Eur. J. Entomol. 110 (2): 271-276, 2013 | 10.14411/eje.2013.040

Seasonal cues mediate host behaviour modification and cocoon polymorphism in Microplitis mediator (Hymenoptera: Braconidae)

Shu-Ping LUO1,4, J.P. MICHAUD2, Jian-Cheng LI3, Jing ZHANG1, Xiao-Xia LIU*,1, Qing-Wen ZHANG*,1
1 Department of Entomology, China Agricultural University, Beijing, 100193, China
2 Department of Entomology, Kansas State University, Agricultural Research Center - Hays, Hays, Kansas, 67601, USA; e-mail: jpmi@ksu.edu
3 Institute of Plant Protection, Hebei Academy of Agriculture and Forestry Sciences, Baoding 071001, China
4 State Key Laboratory for Biology of Plant Diseases and Insect Pest, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Laboratory experiments were conducted to examine the effects of photoperiod and temperature on the pupation behaviour of the parasitoid, Microplitis mediator (Haliday) (Hymenoptera: Braconidae), parasitizing larvae of Mythimna separata Walker (Lepidoptera: Noctuidae). A combination of long photoperiod (14 + h L) and warm temperatures (20-24C) caused parasitized caterpillars to climb to upper plant parts where the parasitoid produced a green, non-diapausing cocoon on a green leaf, initially retaining the dying caterpillar host as a protective covering. In contrast, short photoperiod (8-10 h L) and low temperature (16-18C) induced host caterpillars to descend the plant where the parasitoid produced a brown, diapausing cocoon either hanging by silk from a senescing leaf or simply lying on the soil, but without any continued association with the host. These findings illustrate the potential for seasonal environmental cues to simultaneously mediate diapause induction, cocoon polymorphism, and alternate forms of host behaviour modification in a hymenopterous parasitoid.

Keywords: Hymenoptera, Braconidae, Microplitis mediator, Lepidoptera, Noctuidae, Mythimna separata, photoperiod, host behaviour, pupation site selection, cocoon polymorphism, temperature

Received: October 15, 2012; Accepted: November 27, 2012; Published: April 11, 2013

Download citation

References

  1. ADAMO S.A. 2005: Parasitic suppression of feeding in the tobacco hornworm, Manduca sexta: Parallels with feeding depression after an immune challenge. - Arch. Insect Biochem. Physiol. 60: 185-197 Go to original source...
  2. ADAMO S.A. & SHOEMAKER K.L. 2000: Effects of parasitism on the octopamine content of the central nervous system of Manduca sexta: a possible mechanism underlying host behavioural change. - Can. J. Zool. 78: 1580-1587 Go to original source...
  3. BALDUF W.V. 1926: The bionomics of Dinocampus coccinellae Schrank. - Ann. Entomol. Soc. Am. 19: 465-498 Go to original source...
  4. BECKAGE N.E. 2002: Parasite- and pathogen-mediated manipulation of host behaviour. In Pfaff D., Arnold A., Etgen A., Fahr bach S. & Rubin R. (eds): Hormones, Brain and Behaviour. Academic Press, San Diego, pp. 281-315
  5. BECKAGE N.E. & GELMAN D.B. 2004: Wasp parasitoid disruption of host development: implications of new biologically based strategies for insect control. - Annu. Rev. Entomol. 49: 299-330 Go to original source...
  6. BECKERS O.M. & WAGNER W.E. JR. 2011: Male field crickets infested by parasitoid flies express phenotypes that may benefit the parasitoids. - Anim. Behav. 82: 1151-1157 Go to original source...
  7. BI F.C. 1981: A new artificial diet of Mythimna separata (Walker) (Lepidoptera: Noctuidae). - Acta Entomol. Sin. 124: 379-383
  8. BIRON D.G., JOLY C., GALEOTTI N., PONTON F. & MARCHE L. 2005: The proteomics: a new prospect for studying parasitic manipulation. - Behav. Process. 68: 249-253 Go to original source...
  9. BRODEUR J. & MCNEIL J.N. 1989: Seasonal microhabitat selection by an endoparasitoid through adaptive modification of host behaviour. - Science 244: 226-228 Go to original source...
  10. BRODEUR J. & MCNEIL J.N. 1992: Host behaviour modification by the endoparasitoid Aphidius nigripes: A strategy to reduce hyperparasitism. - Ecol. Entomol. 17: 97-104 Go to original source...
  11. BRODEUR J. & VET L.E.M. 1994: Usurpation of host behaviour by a parasitic wasp. - Anim. Behav. 48: 187-192 Go to original source...
  12. CEZILLY F. & PERROT-MINNOT M.J. 2005: Studying adaptive changes in the behaviour of infected hosts: a long and winding road. - Behav. Process. 68: 223-228 Go to original source...
  13. COLE T.J., BECKAGE N.E., TAN F.F., SRINIVASAN A. & RAMASWAMY S.B. 2002: Parasitoid-host endocrine relations: selfreliance or co-optation? - Insect Biochem. Mol. Biol. 32: 1673-1679 Go to original source...
  14. DANKS H.V. 1987: Insect Dormancy: An Ecological Perspective. Biological Survey of Canada (Terrestrial Arthropods), Ottawa, ix + 439 pp
  15. DENLINGER D.L. 2002: Regulation of diapause. - Annu. Rev. Entomol. 47: 93-122 Go to original source...
  16. EBERHARD W.G. 2000: Spider manipulation by a wasp larva. - Nature 406: 255-256 Go to original source...
  17. EBERHARD W.G. 2001: Under the influence: webs and building behaviour of Plesiometa argyra (Aranea, Tetragnathidae) when parasitized by Hymenoepimecis argyraphaga (Hymenoptera, Ichneumonidae). - J. Arachnol. 29: 354-366 Go to original source...
  18. FANG H.Y., ZHENG B.Z., WANG J.J., YANG X.Y. & TAN H.Y. 2000: Occurrence of Microplitis mediator in transgenic Bt cotton field. - China Cotton 37: 29
  19. FRANZ K. & KURTZ J. 2002: Altered host behaviour: manipulation or energy depletion in tapeworm-infected copepods? - Parasitology 125: 187-196 Go to original source...
  20. FRITZ R.S. 1982: Selection for host modification by insect parasitoids. - Evolution 36: 283-288 Go to original source...
  21. GODFRAY H.J.C. 1994: Parasitoids: Behavioural and Evolutionary Ecology. Princeton University Press, Princeton, NJ, 473 pp
  22. GROSMAN A.H., JANSSEN A., DE BRITO E.F., CORDEIRO E.G., COLARES F., FONSECA J.O., LIMA E.R., PALLINI A. & SABELIS M.W. 2008: Parasitoid increases survival of its pupae by inducing hosts to fight predators. - PLoS One 3: e2276 Go to original source...
  23. HENNE D.C. & JOHNSON S.J. 2007: Zombie fire ant workers: behavior controlled by decapitating fly parasitoids. - Insectes Soc. 54: 150-153 Go to original source...
  24. LAWRENCE P.O. 1986: Host-parasite hormonal interactions: An overview. - J. Insect Physiol. 32: 295-298 Go to original source...
  25. LI J.C., YAN F.M., COUDRON T.A., PAN W.L., ZHANG X.F., LIU X.X. & ZHANG Q.W. 2005: Field release of the parasitoid Microplitis mediator (Hymenoptera: Braconidae) for control of Helicoverpa armigera (Lepidoptera: Noctuidae) in cotton fields in Northwestern China's Xinjiang province. - Environ. Entomol. 35: 694-699 Go to original source...
  26. LI W.X., LI J.C., COUDRON T.A., LU Z.Y., PAN W.L., LIU X.X. & ZHANG Q.W. 2008: Role of photoperiod and temperature in diapause induction of the endoparasitoid wasp Microplitis mediator (Hymenoptera: Braconidae). - Ann. Entomol. Soc. Am. 101: 613-618 Go to original source...
  27. LIBERSAT F., DELAGO A. & GAL R. 2009: Manipulation of host behavior by parasitic insects and insect parasites. - Annu. Rev. Entomol. 54: 189-207 Go to original source...
  28. LIU X.X., ZHANG Q.W., ZHAO J.Z., LI J.C., XU B.L. & MA X.M. 2005: Effects of Bt transgenic cotton lines on the cotton bollworm parasitoid Microplitis mediator in the laboratory. - Biol. Contr. 35: 134-141 Go to original source...
  29. MASON P.G., ERLANDSON M.A. & YOUNGS B.J. 2001: Effects of parasitism by Banchus flavescens (Hymenoptera: Ichneumonidae) and Microplitis mediator (Hymenoptera: Braconidae) on the bertha armyworm, Mamestra configurata (Lepidoptera: Noctuidae). - J. Hymenopt. Res. 10: 81-90
  30. MCALLISTER M.K. & ROITBERG B.D. 1987: Adaptive suicidal behavior in pea aphids. - Nature 328: 797-799 Go to original source...
  31. MEHRNEJAD M.R. & COPLAND M.J.W. 2005: Diapause strategy in the parasitoid Psyllaephagus pistaciae. - Entomol. Exp. Appl. 116: 109-114 Go to original source...
  32. MOORE J. 1995: The behaviour of parasitized animals. - Bioscience 45: 89-96 Go to original source...
  33. MOORE J. 2002: Parasites and the Behavior of Animals. Oxford Series in Ecology and Evolution. Oxford University Press, Oxford, 338 pp
  34. PIVNICK K.A. 1993: Diapause initiation and pupation site selection of the Braconid parasitoid Microplitis mediator (Haliday) a case of manipulation of host behaviour. - Can. Entomol. 125: 825-830 Go to original source...
  35. PONTON F., LEBARBENCHON C., LEFEVRE T., BIRON D.G., DUNEAN D., HUGHES D.P. & THOMAS F. 2006: Parasitology: parasite survives predation on its host. - Nature 440: 756 Go to original source...
  36. POULIN R. 1995: "Adaptive" changes in the behaviour of parasitized animals: A critical review. - Int. J. Parasitol. 25: 1371-1383 Go to original source...
  37. POULIN R. 2010: Parasite manipulation of host behavior: An update and frequently asked questions. - Adv. Study Behav. 41: 151-186 Go to original source...
  38. RASEKH R., MICHAUD J.P., ALLAHYARI H. & SABAHU Q. 2010: The foraging behaviour of Lysiphlebus fabarum (Marshall), a thelytokous parasitoid of the black bean aphid in Iran. - J. Insect Behav. 23: 165-179 Go to original source...
  39. SAS INSTITUTE 2004: SAS(R) User's Guide: Statistics. SAS Institute, Cary, NC
  40. SEYAHOOEI M.A., KRAAIJEVELD-SMIT F.J.L., KRAAIJEVELD K., CROOIJMANS J.B.M., VAN DOOREN T.J.M. & VAN ALPHEN J.J.M. 2009: Closely related parasitoids induce different pupation and foraging responses in Drosophila larvae. - Oikos 118: 1148-1157 Go to original source...
  41. STAMP N.E. 1981: Behaviour of parasitized aposematic caterpillars - advantageous to the parasitoid or the host? - Am. Nat. 118: 715-725 Go to original source...
  42. TAUBER M.J. & TAUBER C.A. 1976: Insect seasonality: Diapause maintenance, termination and postdiapause development. - Annu. Rev. Entomol. 21: 81-107 Go to original source...
  43. THOMAS F., ADAMO S. & MOORE J. 2005: Parasitic manipulation: where are we and where should we go? Behav. Process. 68: 185-199 Go to original source...