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Duration of Plant Damage by Host Larvae Affects Attraction of Two Parasitoid Species (Microplitis croceipes and Cotesia marginiventris) to Cotton: Implications for Interspecific Competition

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Abstract

Volatile organic compounds (VOCs) released by herbivore-damaged plants can guide parasitoids to their hosts. The quantity and quality of VOC blends emitted by plants may be affected by the duration of plant damage by herbivores, which could have potential ramifications on the recruitment of competing parasitoids. We used two parasitoid species, Microplitis croceipes and Cotesia marginiventris (Hymenoptera: Braconidae), to address the question of whether duration of plant damage affects parasitoid use of plant VOCs for host location. Both wasp species are larval endoparasitoids of Heliothis virescens (Lepidoptera: Noctuidae), an important pest of cotton. Attraction of the two parasitoid species to odors emitted by undamaged (UD), fresh (6 h infestation) damage (FD), and old (24 h infestation) damage (OD) cotton plants infested by H. virescens larvae was investigated using a headspace volatile collection system coupled with four-choice olfactometer bioassay. Both sexes of M. croceipes showed a preference for FD- and OD-plant odors over UD-plants. On the other hand, more C. marginiventris females were attracted to UD- and FD-plants than to OD-plants. GC/MS analyses showed qualitative and quantitative differences in the VOC profiles of UD, FD, and OD-plants, which may explain the observed preferences of the parasitoids. These results suggest a temporal partitioning in the recruitment of M. croceipes and C. marginiventris to H. virescens-damaged cotton, and may have potential implications for interspecific competition between the two parasitoid species.

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References

  • Amarasekare P (2000) Coexistence of competing parasitoids on a patchily distributed host: local vs. spatial mechanisms. Ecology 81:1286–1296

    Article  Google Scholar 

  • Boland W, Hopke J, Piel J (1998) Induction of plant volatile biosynthesis by jasmonates. In Natural product analysis, chromatography, spectroscopy, biological testing. Schreier P, Herderich M, Humpf H.U, Schwab W. Braunschweig/Wiesbaden and Viehweg Verlag (eds) pp.255–269

  • Boland W, Koch T, Krumm T, Piel J, Jux A (1999) Induced biosynthesis of insect semiochemicals in plants. In: D. J. Chadwick & J. Goode (eds), Insect-plant interactions and induced plant defence. Wiley, Chicester (Novartis Foundation Symposium 223), pp. 110–126

  • Chen L, Fadamiro HY (2007) Differential electroantennogram response of females and males of two parasitoid species to host-related green leaf volatiles and inducible compounds. Bull Entomol Res 97:515–522

    Article  CAS  PubMed  Google Scholar 

  • Clausen CP, Clancey DW, Chock QC (1965) Biological control of the oriental fruit fly (Dacus dorsalis Hendel) and other fruit flies in Hawaii. US Dep Agric Tech Bull 1322:1–102

    Google Scholar 

  • Coley PD (1987) Interspecific variation in plant anti-herbivore properties: the role of habitat quality and rate of disturbance. New Phytol 106:251–263

    Article  Google Scholar 

  • Cortesero AM, De Moraes CM, Stapel JO, Tumlinson JH, Lewis WJ (1997) Comparisons and contrasts in host-foraging strategies of two larval parasitoids with different degrees of host specificity. J Chem Ecol 23:1589–1606

    Article  CAS  Google Scholar 

  • Cusumano A, Peri E, Vinson SB, Colazza S (2012) The ovipositing female of Ooencyrtus telenomicida relies on physiological mechanisms to mediate intrinsic competition with Trissolcus basalis. Entomol Ext Appl 143:155–163

    Article  Google Scholar 

  • D’Alessandro M, Turlings TCJ (2005) In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem Senses 30:739–753

    Article  PubMed  Google Scholar 

  • De Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897

    Article  CAS  PubMed  Google Scholar 

  • De Moraes CM, Lewis WJ (1999) Analyses of two parasitoids with convergent foraging strategies. J Insect Behav 12:571–583

    Article  Google Scholar 

  • De Moraes CM, Mescher MC (2005) Intrinsic competition between larval parasitoids with different degrees of host specificity. Ecol Entomol 30:564–570

    Article  Google Scholar 

  • De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • De Moraes CM, Cortesero AM, Stapel JO, Lewis WJ (1999) Intrinsic and extrinsic competitive interactions between two larval parasitoids of Heliothis virescens. Ecol Entomol 24:403–410

    Article  Google Scholar 

  • Dicke M, van Loon JA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324

    Article  CAS  PubMed  Google Scholar 

  • Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440

    Article  CAS  Google Scholar 

  • Dukas R, Duan JJ (2000) Potential fitness consequences of associative learning in a parasitoid wasp. Behav Ecol 11:536–543

    Article  Google Scholar 

  • Gershenzon J (1994) Metabolic costs of terpenoid accumulation in higher plants. J Chem Ecol 20:1281–1328

    Article  CAS  PubMed  Google Scholar 

  • Graham HM, Robertson OT (1970) Host plants of Heliothis virescens and H. zea (Lepidoptera: Noctuidae) in the Lower Rio Grande Valley, Texas. Ann Entomol Soc Am 63:1261–1265

    Google Scholar 

  • Harvey JA, Poelman EH, Tanaka T (2013) Intrinsic inter- and intraspecific competition in parasitoid wasps. Annu Rev Entomol 58:333–351

    Article  CAS  PubMed  Google Scholar 

  • Hoballah ME, Turlings TCJ (2005) The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J Chem Ecol 31:2003–2018

    Article  CAS  PubMed  Google Scholar 

  • Iwao K, Ohsaki N (1996) Inter- and intraspecific interactions among larvae of specialists and generalist parasitoids. Res Pop Ecol 38:265–273

    Article  Google Scholar 

  • Lewis WJ, Burton RL (1970) Rearing Microplitis croceipes in the laboratory with Heliothis zea as host. J Econ Entomol 63:656–658

    Google Scholar 

  • Lewis WJ, Snow WJ (1971) Fecundity, sex ratios, and egg distribution by Microplitis croceipes, a parasite of Heliothis. J Econ Entomol 64:6–8

    CAS  Google Scholar 

  • Lewis WJ, Takasu K (1990) Use of learned odors by a parasitic wasp in accordance with host and food needs. Nature 348:635–636

    Article  Google Scholar 

  • Loughrin JH, Manukian A, Heath RR, Turlings CJ, Tumlinson JH (1994) Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plants. Proc Natl Acad Sci U S A 91:11836–11840

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Magalhaes DM, Borges M, Laumann RA, Sujii ER, Mayor P et al (2012) Semiochemicals from herbivory induced cotton plants enhance the foraging behavior of the cotton boll weevil, Anthonomus grandis. J Chem Ecol 38:1528–1538

    Article  CAS  PubMed  Google Scholar 

  • Mainali BP, Lim UT (2012) Annual pattern of occurrence of Riptortus pedestris (Hemiptera: Alydidae) and its egg parasitoids Ooencyrtus nezarae Ishii and Gryon japonicum (Ashmead) in Andong. Korea Crop Prot 36:37–42

    Article  Google Scholar 

  • Mc Call PJ, Turlings CJ, Loughrin J, Proviouex AT, Tumlinson JH (1994) Herbivore-induced volatiles from cotton (Gossypium hirsutum L.) seedlings. J Chem Ecol 20:3039–3050

    Article  CAS  Google Scholar 

  • McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310

    Article  Google Scholar 

  • Mohamad R, Monge J, Goubault M (2011) Agonistic interactions and their implications for parasitoid species coexistence. Behav Ecol 22:1114–1122

    Article  Google Scholar 

  • Morawo T, Fadamiro H (2014) Attraction of two larval parasitoids with varying degree of host specificity to single components and a binary mixture of host-related plant volatiles. Chemoecology. doi:10.1007/s00049-014-0154-5

    Google Scholar 

  • Ngumbi E, Fadamiro H (2012) Species and sexual differences in behavioral responses of a specialist and generalist parasitoid species to host-related volatiles. Bull Entomol Res 102:710–718

    Article  CAS  PubMed  Google Scholar 

  • Ngumbi E, Chen L, Fadamiro HY (2009) Comparative GC-EAD responses of a specialist (Microplitis croceipes) and a generalist (Cotesia marginiventris) parasitoid to cotton volatiles induced by two caterpillar species. J Chem Ecol 35:1009–1020

    Article  CAS  PubMed  Google Scholar 

  • Ngumbi E, Chen L, Fadamiro H (2010) Electroantennogram (EAG) responses of Microplitis croceipes and Cotesia marginiventris and their lepidopteran hosts to a wide array of odor stimuli: correlation between EAG response and degree of host specificity? J Insect Physiol 56:1260–1268

    Article  CAS  PubMed  Google Scholar 

  • Ngumbi E, Jordan M, Fadamiro H (2012) Comparison of associative learning of host-related plant volatiles in two parasitoids with different degrees of host specificity, Cotesia marginiventris and Microplitis croceipes. Chemoecology 22:207–215

    Article  CAS  Google Scholar 

  • Pare PW, Tumlinson JH (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:1161–1167

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pare PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Poelman EH, Harvey JA, van Loon JJA, Vet LEM, Dicke M (2013) Variation in herbivore-induced plant volatiles corresponds with spatial heterogeneity in the level of parasitoid competition and parasitoid exposure to hyperparasitism. Funct Ecol 27:1107–1116

    Article  Google Scholar 

  • Rose USR, Tumlinson JH (2004) Volatiles released from cotton plants in response to Helicoverpa zea feeding damage on cotton flower buds. Planta 218:824–832

    Article  PubMed  Google Scholar 

  • Rose USR, Manukian A, Heath RR, Turlings CJ, Tumlinson JH (1996) Volatile semiochemicals released from undamaged cotton Leaves. A systemic response of living plants to caterpillar damage. Plant Physiol 111:487–495

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rose USR, Lewis WJ, Tumlinson JH (1998) Specificity of systemically released cotton volatiles as attractants for specialist and generalist parasitic wasps. J Chem Ecol 24:303–319

    Article  CAS  Google Scholar 

  • Shorey HH, Hale RL (1965) Mass rearing of the larvae of nine noctuid species on a simple artificial medium. J Econ Entomol 58:55–68

    Google Scholar 

  • Smith BH (1998) Analysis of interaction in binary mixtures. Physiol Behav 65:397–407

    Article  CAS  PubMed  Google Scholar 

  • Stadelbacher EA, Powell JE, King EG (1984) Parasitism of Heliothis zea and H. virescens (Lepidoptera: Noctuidae) larvae in wild and cultivated host plants in the delta of Mississippi. Environ Entomol 13:1167–1172

    Google Scholar 

  • Tillman PG (1996) Functional Response of Microplitis croceipes and Cardiochiles nigriceps (Hymenoptera: Braconidae) to variation in density of tobacco budworm (Lepidoptera: Noctuidae). Environ Entomol 25:524–528

    Google Scholar 

  • Tillman PG, Laster ML (1995) Parasitization of Heliothis virescens and H. virescens-H. subflexa backcross (Lepidoptera: Noctuidae) by Microplitis croceipes (Hymenoptera: Braconidae). Environ Entomol 24:409–411

    Google Scholar 

  • Tillman PG, Powell JE (1992) Intraspecific host discrimination and larval competition in Microplitis croceipes, Microplitis demolitor, Cotesia kazak (Hym.: Braconidae) and Hyposoter didymator (Hym.: Ichneumonidae), parasitoids of Heliothis virescens (Lep.: Noctuidae). BioControl 37:429–437

    Google Scholar 

  • Turlings TCJ, Loughrin PJ, Mc Call PJ, Rose USR, Lewis WJP, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci U S A 92:4169–4174

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Turlings TCJ, Davison AC, Tamo C (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiol Entomol 29:45–55

    Article  Google Scholar 

  • Turlings TCJ, Jeanbourquin PM, Held M, Degen T (2005) Evaluating the induced-odour emission of a Bt. maize and its attractiveness to parasitic wasps. Transgenic Res 14:807–816

    Article  CAS  PubMed  Google Scholar 

  • van Strien-van LWTFH (1983) The competition between Asobara tabida Nees Von Esenbeck, 1834 and Leptopilina heterotoma (Thonson, 1862) in multiparasitized hosts. Neth J Zool 33:125–163

    Article  Google Scholar 

  • van Wijk M, De Bruijn PJA, Sabelis MW (2011) Complex odor from plants under attack: herbivore’s enemies react to the whole, not its parts. PLoS ONE 6:e21742. doi:10.1371/journal.pone.0021742

    Article  PubMed Central  PubMed  Google Scholar 

  • Wajnberg É, Haccou P (2008) Statistical tools for analyzing data on behavioral ecology of insect parasitoids: From Theoretical approaches to field applications (eds É. Wajnberg, C. Bernstein and J. van Alphen), Blackwell Publishing Ltd, Oxford, UK

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Acknowledgments

We thank Matthew McTernan and Savannah Duke for rearing the insects. This study was supported by Auburn University and the Alabama Agricultural Experiment Station.

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Correspondence to Henry Fadamiro.

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Morawo, T., Fadamiro, H. Duration of Plant Damage by Host Larvae Affects Attraction of Two Parasitoid Species (Microplitis croceipes and Cotesia marginiventris) to Cotton: Implications for Interspecific Competition. J Chem Ecol 40, 1176–1185 (2014). https://doi.org/10.1007/s10886-014-0525-y

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