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Comparison of associative learning of host-related plant volatiles in two parasitoids with different degrees of host specificity, Cotesia marginiventris and Microplitis croceipes

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Abstract

The ability of parasitoids to learn a wide range of volatiles, including ecologically relevant and novel odors, and respond favorably to the learned stimuli has been documented for various species. Comparison of odor learning in closely related species can elucidate adaptive differences in species responses to infochemicals. The present study used a Y-tube olfactometer to compare odor learning and priming of behavioral responses of two parasitoids, Cotesia marginiventris (Cresson) and Microplitis croceipes (Cresson), to four selected host-related volatile compounds which have been previously shown to elicit behavioral response in both species; trans-2-hexanal, α-pinene, cis-3-hexenyl butyrate, and (E,E)-α-farnesene. The two parasitoid species differ in their degree of specialization at the host level with M. croceipes having a more specialized host range, but otherwise represent infochemical generalist parasitoid species at the plant level. Naïve females as well as females that had been trained to associate sugar water with the test compounds were tested. Compared to naïve females, trained females of C. marginiventris showed a significant increase in behavioral response to all four tested compounds. In contrast, trained females of M. croceipes showed a significant increase in behavioral response only to α-pinene, and (E,E)-α-farnesene. Overall, the species with a wider host range, C. marginiventris showed a greater learning-induced increase in response than the species with a relatively specialized host range, M. croceipes. The results imply that animals with different ecological constraints may show variations in learning. The adaptive significance of behavioral responses as related to dietary specializations of the parasitoids is discussed.

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References

  • Baker MB (2005) Experience influences settling behavior in desert isopods, Hemilepistus reaumuri. Animal Behav 69:1131–1138

    Article  Google Scholar 

  • Bleeker MAK, Smid HM, Steidle JLM, Kruidhof M, van Loon JJA, Vet LEM (2006) Differences in memory dynamics between two closely related parasitoid wasp species. Animal Behav 71:1343–1350

    Article  Google Scholar 

  • 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  PubMed  CAS  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 

  • Dalesman S, Rundle S, Coleman RA, Cotton PA (2006) Cue association and antipredator behavior in a pulmonate snail Lymnaea stagnalis. Animal Behav 71:789–797

    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 

  • Dukas R, Bernays EA (2000) Learning improves growth rate in grasshoppers. Proc Natl Acad Sci USA 97:2637–2640

    Article  PubMed  CAS  Google Scholar 

  • Eller FJ (1990) Foraging behavior of Microplitis croceipes, a parasitoid of Heliothis species. Dissertation, University of Florida, Gainesville

  • Farina WM, Grutter C, Diaz PC (2005) Social learning of floral odors inside the honeybee hive. Proc R Soc Lond B 272:1923–1928

    Article  Google Scholar 

  • Fukushima J, Kainoh Y, Honda H, Takabayashi J (2002) Learning of herbivore-induced and nonspecific plant volatiles by a parasitoid, Cotesia kariyai. J Chem Ecol 28:579–585

    Article  PubMed  CAS  Google Scholar 

  • Geervliet JBF, Vreugdenhil AI, Dicke M, Vet LEM (1998) Learning to discriminate between infochemicals from different plant–host complexes by the parasitoids Cotesia glomerata and Cotesia rubecula (Hymenoptera: Braconidae). Entomol Exp Appl 86:241–252

    Article  CAS  Google Scholar 

  • Hérard F, Keller MA, Lewis WJ, Tumlinson JH (1988) Beneficial arthropod behavior mediated by airborne semiochemicals. IV. Influence of host diet on host-oriented flight chamber responses of Microplitis demolitor Wilkinson. J Chem Ecol 14:1597–1606

    Article  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  PubMed  CAS  Google Scholar 

  • Hoedjes KM, Marjolein Kruidhof H, Huigens ME, Dicke M, Vet LEM, Smid H (2011) Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience. Proc R Soc Lond B 278:889–897

    Article  Google Scholar 

  • Jaenike J (1988) Effects of early adult experience on host selection in insects: some experimental and theoretical results. J Insect Behav 1:3–15

    Article  Google Scholar 

  • Jalali SK, Singh SK, Ballal CR (1987) Studies on host age preference and biology of exotic parasite, Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae). Entomon 12:59–62

    Google Scholar 

  • Johnston TD (1982) Selective costs and benefits in the evolution of learning. Adv Study Behav 12:65–106

    Article  Google Scholar 

  • Kamil AC (1994) A synthetic approach to the study of animal intelligence. In: Real LA (ed) Behavioural mechanisms in evolutionary ecology. The University of Chicago Press, USA, pp 11–45

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

    Article  Google Scholar 

  • Lewis WJ, Tumlinson JH (1988) Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331:257–259

    Article  Google Scholar 

  • Lewis WJ, Vet LEM, Tumlinson JH, van Lenteren JC, Papaj DR (1990) Variations in parasitoid foraging behavior: essential element of a sound biological control theory. Environ Entomol 19:1183–1193

    Google Scholar 

  • Li Y, Dickens JC, Steiner WWM (1992) Antennal olfactory responsiveness of Microplitis croceipes (Hymenoptera: Braconidae) to cotton plant volatiles. J Chem Ecol 18:1761–1773

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mahometa MJ, Domjan M (2005) Classical conditioning increases reproductive success in Japanese quail, Coturnix japonica. Anim Behav 69:983–989

    Article  Google Scholar 

  • McCall PJ, Turlings TCJ, Loughrin J, Proveaux AT, Tumlinson JH (1994) Herbivore-induced volatile emissions from cotton (Gossypium hirsutum L.) seedlings. J Chem Ecol 20:3039–3050

    Article  CAS  Google Scholar 

  • Meiners T, Wäckers F, Lewis JW (2002) The effect of molecular structure on olfactory discrimination by the parasitoid Microplitis croceipes. Chem Senses 27:811–816

    Article  PubMed  CAS  Google Scholar 

  • Meiners T, Wäckers F, Lewis JW (2003) Associative learning of complex odors in parasitoid host location. Chem Senses 28:231–236

    Article  PubMed  CAS  Google Scholar 

  • Müller C, Collatz J, Wieland R, Steidle JLM (2006) Associative learning and memory duration in the parasitic wasp Lariophagus distinguendus. Anim Biol 56:221–232

    Article  Google Scholar 

  • Nafziger TD, Fadamiro HY (2011) Suitability of some farmscaping plants as nectar sources for the parasitoid wasp, Microplitis croceipes (Hymenoptera: Braconidae): effects on longevity and body nutrients. Biol Control 56:225–229

    Article  Google Scholar 

  • Ngumbi EN, 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  PubMed  CAS  Google Scholar 

  • Ngumbi EN, Chen L, Fadamiro HY (2010) Electroantennogram (EAG) responses of Microplitis croceipes and Cotesia marginiventris and their lepidopteran hosts to a wide array of host-related and non host-related compounds: correlation between EAG response and degree of host specificity. J Insect Physiol 56:1260–1268

    Article  PubMed  CAS  Google Scholar 

  • Olson DM, Rains GC, Meiners T, Takasu K, Tertuliano M, Tumlinson JH, Wäckers FL, Lewis WJ (2003) Parasitic wasps learn and report diverse chemicals with unique conditional behaviors. Chem Senses 28:545–549

    Article  PubMed  CAS  Google Scholar 

  • Poolman Simons MTT, Suverkropp BP, Vet LEM, de Moed G (1992) Comparison of learning in related generalist and specialist eucoilid parasitoids. Entom Exp Appl 64:117–124

    Article  Google Scholar 

  • Potting RPJ, Otten H, Vet LEM (1997) Absence of learning in the stemborer parasitoid Cotesia flavipes. Anim Behav 53:1211–1223

    Article  PubMed  Google Scholar 

  • Rains GC, Tomberlin JK, D’Alessandro M, Lewis WJ (2004) Limits of volatile chemical detection of a parasitoid wasp Microplitis croceipes, and an electronic nose: a comparative study. Am Soc Agric Eng 47:2145–2152

    CAS  Google Scholar 

  • Röse USR, Alborn HT, Makranczy G, Lewis WJ, Tumlinson JH (1997) Host recognition by the specialist endoparasitoid Microplitis croeipes (Hymenoptera: Braconidae): role of host- and plant-related volatiles. J Insect Behav 10:313–330

    Article  Google Scholar 

  • Röse 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  Google Scholar 

  • SAS Institute (2007) JMP 7.0.1. Statistical discovery software. SAS Institute Statistical Analysis System, Cary

  • Segura DF, Viscarret MM, Carabajal Paladino LZ, Ovruski SM, Cladera JL (2007) Role of visual information and learning in habitat selection by a generalist parasitoid foraging for concealed hosts. Anim Behav 74:131–142

    Article  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 

  • Smid HM, Wang G, Bukovinszky T, Steidle JLM, Bleeker MAK, van Loon JA, Vet LEM (2007) Species-specific acquisition and consolidation of long-term memory in parasitic wasps. Proc R Soc Lond B 274:1539–1546

    Article  Google Scholar 

  • Steidle JLM, van Loon JJA (2003) Dietary specialization and infochemical use in carnivorous arthropods: testing a concept. Entomol Exp Appl 108:133–148

    Article  Google Scholar 

  • Takasu K, Lewis WJ (1996) The role of learning in adult food location by the larval parasitoid Microplitis croceipes. J Insect Behav 9:265–281

    Article  Google Scholar 

  • Takasu K, Lewis WJ (2003) Learning of host searching cues by the larval parasitoid Microplitis croceipes. Entomol Exp Appl 108:77–86

    Article  Google Scholar 

  • Tamò C, Ricard I, Held M, Davison AC, Turlings TCJ (2006) A comparison of naïve and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odors. Anim Biol 56:205–220

    Article  Google Scholar 

  • Tomberlin JK, Tertuliano M, Rains G, Lewis WJ (2005) Conditioned Microplitis croceipes Cresson (Hymenoptera: Braconidae) detect and respond to 2,4-DNT: development of a biological sensor. J Forensic Sci 50:1187–1190

    PubMed  CAS  Google Scholar 

  • Turlings TCJ, Wackers FL, Vet LEM, Lewis WJ, Tumlinson JH (1993) Learning of host-finding cues by hymenopterous parasitoids. In: Papaj DR, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives. Chapman and Hall, New York, pp 51–78

    Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol 37:141–172

    Article  Google Scholar 

  • Vet LEM, Groenewold AW (1990) Semiochemicals and learning in parasitoids. J Chem Ecol 16:3119–3135

    Article  CAS  Google Scholar 

  • Vet LEM, Lewis WJ, Papaj DR, van Lenteren JC (1990) A variable-response model for parasitoid foraging behavior. J Insect Behav 3:471–490

    Article  Google Scholar 

  • Vet LEM, Sokolowski MB, MacDonald DE, Snellen H (1993) Responses of a generalist and a specialist parasitoid (Hymenoptera: Eucoilidae) to drosophid larval kairomones. J Insect Behav 6:615–624

    Article  Google Scholar 

  • Vet LEM, Lewis WJ, Cardé RT (1995) Parasitoid foraging and learning. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects, 2nd edn. Chapman and Hall, London, pp 65–101

    Chapter  Google Scholar 

  • Wäckers FL, Bonifay C, Lewis JW (2002) Conditioning of appetitive behavior in the Hymenopteran parasitoid Microplitis croceipes. Entomol Exp Appl 103:135–138

    Article  Google Scholar 

  • Whitman DW, Eller FJ (1992) Orientation of Microplitis croceipes (Hymenoptera: Braconidae) to green leaf volatiles: dose–response curves. J Chem Ecol 18:1743–1753

    Article  CAS  Google Scholar 

  • Woody DR, Mathis A (1995) Acquired recognition of chemical stimuli from an unfamiliar predator: associative learning by adult newts, Nolophthalmus viridescens. Copeia 4:1027–1031

    Google Scholar 

  • Xue HJ, Egas M, Yang XK (2007) Development of a positive preference–performance relationship in an oligophagous beetle: adaptive learning? Entomol Exp Appl 125:119–124

    Article  Google Scholar 

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Acknowledgments

We thank Prithwiraj Das, and Jennea Ollie for help with parasitoid rearing. We thank Paul Conner for designing the Y-tube stand. This research was funded by a National Science Foundation (NSF) Grant (Award Number: 0641621) to HYF.

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  1. Esther Ngumbi

    Present address: School of Biology, Georgia Institute of Technology, Atlanta, GA, 30322, USA

  2. Maggie Jordan

    Present address: Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, 80523, USA

Authors and Affiliations

  1. Department of Entomology & Plant Pathology, Auburn University, Auburn, AL, 36849, USA

    Esther Ngumbi, Maggie Jordan & Henry Fadamiro

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  1. Esther Ngumbi
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Correspondence to Henry Fadamiro.

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Ngumbi, E., Jordan, M. & Fadamiro, H. 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 (2012). https://doi.org/10.1007/s00049-012-0106-x

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