Skip to main content
SpringerLink
Log in

Neonate Silkworm (Bombyx mori) Larvae Are Attracted to Mulberry (Morus alba) Leaves with Conspecific Feeding Damage

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The silkworm Bombyx mori is a molecular genetic model for the Lepidoptera. Its odorant receptor genes have been described, and preliminary studies suggest that several are expressed specifically in the larval caterpillar stage. This study was undertaken to identify olfactory behaviors specific to the larvae. A two-choice leaf disk bioassay with naive neonate larvae was used to evaluate the attractiveness of three types of mulberry leaf (Morus alba): newly flushed leaves from branch tips, mature leaves, and mature leaves with feeding damage caused by conspecific larvae. Mature leaves with feeding damage were the most attractive, newly flushed leaves were moderately favored, and undamaged mature leaves were the least attractive. Volatile odors collected from whole mulberry leaves by using solid-phase microextraction fibers were analyzed by gas chromatography-mass spectrometry. The volatile profile of newly flushed leaves and mature leaves damaged by conspecific larvae was more complex compared to undamaged mature leaves. By comparing the volatile makeup of each leaf type, a list of 22 candidate odors responsible for attracting the neonate larvae was generated; α-farnesene was particularly notable as a herbivore-induced volatile. These odors will be used in future in vitro studies to determine whether they activate larval-specific odorant receptors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Anderson, A Z. R., Wanner, K. W., Trowell, S. C., Warr, C. G., Jaquin-Joly, E., Zagatti, P., Robertson, H., and Newcomb, R. D. 2009. Molecular basis of female-specific odorant responses in Bombyx mori. Insect Biochem. Mol. Bio. 39:189-197.

    Article  CAS  Google Scholar 

  • Beale, M. H., Birkett, M. A., Bruce, T. J., Chamberlain, K., Field, L. M., Huttly, A. K., Martin, J. L., Parker, R., Phillips, A. L., Pickett, J. A., Prosser, I. M., Shewry, P. R., Smart, L. E., Wadhams, L. J., Woodcock, C. M., and Zhang, Y. 2006. Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc. Natl. Acad. Sci. U S A. 103:10509-10513.

    Article  PubMed  CAS  Google Scholar 

  • Carroll, M. J., Schmelz, E. A., Meagher, R. L., and Teal, P. E. A. 2006. Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J. Chem. Ecol. 32:1911-1924.

    Article  PubMed  CAS  Google Scholar 

  • Carroll, M. J., Schmelz, E. A., and Teal, P. E. A. 2008. The attraction of Spodoptera frugiperda neonates to cowpea seedlings is mediated by volatiles induced by conspecific herbivory and the elicitor inceptin. J. Chem. Ecol. 34: 291-300.

    Article  PubMed  CAS  Google Scholar 

  • De Moraes, C. M., Mescher, M. C., and Tumlinson, J. H. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature. 410:577-580.

    Article  PubMed  CAS  Google Scholar 

  • Dicke, M., Gols, R., Ludeking, D., and Posthumus, M. A. 1988. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. J. Chem. Ecol. 25:1907-1922.

    Article  Google Scholar 

  • Goldsmith, M. R., Shimada, T., and Abe, H. 2005. The genetics and genomics of the silkworm, Bombyx mori. Annu. Rev. Entomol. 50:71-100.

    Article  PubMed  CAS  Google Scholar 

  • Hamamura, Y. and Naito, K. 1961. Food selection by silkworm larvae, Bombyx mori. Nature. 190:879-880.

    Article  CAS  Google Scholar 

  • Hoballah, M. E. and Turlings, T. C. J. 2005. The role of fresh vs. 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 

  • Ishikawa, S., Hirao, T., and Ari, N. 1969. Chemosensory basis of host plant selection in the silkworm. Ent. Exp. Appl. 12:544-554.

    Article  Google Scholar 

  • James, D. G. and Price., T. S. 2004. Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J. Chem. Ecol. 30:1613-1628.

    Article  PubMed  CAS  Google Scholar 

  • Kessler, A. and Baldwin, I. T. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science. 291:2141-2144.

    Article  PubMed  CAS  Google Scholar 

  • Kreher, S. A., Kwon, J. Y., and Carlson J. R. 2005. The molecular basis of odor coding in the Drosophila larva. Neuron. 46:445-456.

    Article  PubMed  CAS  Google Scholar 

  • Krieger, J., Grosse-Wilde, E., Gohl, T., and Breer, H. 2005. Candidate pheromone receptors of the silkmoth Bombyx mori. Eur. J. Neurosci. 21:2167-2176.

    Article  PubMed  Google Scholar 

  • Landolt, P. J., Brumley, J. A., Smithhisler, C. L., Biddick, L. L., and Hofstetter, R. W. 2000. Apple fruit infested with coddling moth are more attractive to neonate codling moth larvae and possess increased amounts of (E,E)-α-farnesene. J. Chem. Ecol. 26:1685-1699.

    Article  CAS  Google Scholar 

  • Mita, K., Kasahara, M., Sasaki, S., Nagayasu, Y., Yamada, T., Kanamori, H., Namiki, N., Kitagawa, M., Yamashita, H., Yasukochi, Y., Kadono-Okuda, K., Yamamoto, K., Ajimura, M., Ravikumar, G., Shimomura, M., Nagamura, Y., Shin-I, T., Abe, H., Shimada, T., Morishita, S., and Sasaki, T. 2004. The genome sequence of silkworm, Bombyx mori. DNA Res. 11:27-35.

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa, T., Sakurai, T., Nishioka, T., and Touhara, K. 2005. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638-1642.

    Article  PubMed  CAS  Google Scholar 

  • Pare, P. W. and Tumlinson, J. H. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiol. 121:325-332.

    Article  PubMed  CAS  Google Scholar 

  • Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., and Klessig, D. F. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science. 318:31-32.

    Google Scholar 

  • Prokopy, R. J. and Roitberg, B. D. 2001. Joining and avoidance behavior in nonsocial insects. Annu. Rev. Entomol. 46:631-665.

    Article  PubMed  CAS  Google Scholar 

  • Renwick, J. A. A. and Chew, F. S. 1994. Oviposition behavior in Lepidoptera. Annu. Rev. Entomol. 39:377-400.

    Article  Google Scholar 

  • Sakurai, T., Nakagawa, T., Mitsuno, H., Mori, H., Endo, Y., Tanoue, S., Yasukochi, Y., Touhara, K., and Nishioka, T. 2004. Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc. Natl. Acad. Sci.U.S.A. 101:16653-16658.

    Article  PubMed  CAS  Google Scholar 

  • Schneider, D. 1992. 100 years of pheromone research, an essay on Lepidoptera. Naturwissenschaften. 79:241-250.

    Article  CAS  Google Scholar 

  • Schoonhoven, L. M. 1987. What makes a caterpillar eat? The sensory code underlying feeding behavior, pp. 69-97, in R.F. Champman, E.A. Bernays and J.G. Stoffolanoeds (eds.). Advances in Chemoreception and Behavior. Springer, New York, New York.

    Google Scholar 

  • Stamps, J. and Krishnan, V. V. 2005. Nonintuitive cue use in habitat selection. Ecology. 86:2860-2867.

    Article  Google Scholar 

  • Turlings, T. C., Loughrin, J. H., McCall, P. J., Rose, U. S., Lewis, W. J., and Tumlinson, J. H. 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl. Acad. Sci. USA. 92:4169-4174.

    Article  PubMed  CAS  Google Scholar 

  • Varela, L. G. and Bernays, E. A. 1987. Behavior of newly hatched potato tuber moth larvae, Phthorimaea operculella Zell. (Lepidoptera: Gelechiidae), in relation to their host plants. J. Insect. Behav. 1:261-275.

    Article  Google Scholar 

  • Wanner, K. W., Anderson, A. R., Trowell, S. C., Theilmann, D. A., Robertson, H. M., and Newcomb, R. D. 2007. Female biased expression of odourant receptor genes in the adult antennae of the silkworm. Bombyx mori. Insect Mol. Bio. 16:107-119.

    Article  CAS  Google Scholar 

  • Williams, L. 3rd, Rodriguez-Saona, C., Castle, S. C., and Zhu, S. 2008. EAG-active herbivore-induced plant volatiles modify behavioral responses and host attack by an egg parasitoid. J. Chem. Ecol. 34:1190-1201.

    Article  PubMed  CAS  Google Scholar 

  • Xia, Q., Zhou, Z., Lu, C., Cheng, D., Dai, F., Li, B., Zhao, P., Zha, X., Cheng, T., Chai, C., Pan, G., Xu, J., Liu, C., Lin, Y., Qian, J., Hou, Y., Wu, Z., Li, G., Pan, M., Li, C., Shen, Y., Lan, X., Yuan, L., Li, T., Xu, H., Yang, G., Wan, Y., Zhu, Y., Yu, M., Shen, W., Wu, D., Xiang, Z., Yu, J., Wang, J., Li, R., Shi, J., Li, H., Li, G., Su, J., Wang, X., Li, G., Zhang, Z., Wu, Q., Li, J., Zhang, Q., Wei, N., Xu, J., Sun, H., Dong, L., Liu, D., Zhao, S., Zhao, X., Meng, Q., Lan, F., Huang, X., Li, Y., Fang, L., Li, C., Li, D., Sun, Y., Zhang, Z., Yang, Z., Huang, Y., Xi, Y., Qi, Q., He, D., Huang, H., Zhang, X., Wang, Z., Li, W., Cao, Y., Yu, Y., Yu, H., Li, J., Ye, J., Chen, H., Zhou, Y., Liu, B., Wang, J., Ye, J., Ji, H., Li, S., Ni, P., Zhang, J., Zhang, Y., Zheng, H., Mao, B., Wang, W., Ye, C., Li, S., Wang, J., Wong, G. K., and Yang, H. 2004. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306:1937-1940.

    Article  PubMed  Google Scholar 

  • Zalucki, M. P., Clarke, A. R., and Malcom, S. B. 2002. Ecology and behavior of first instar larval Lepidoptera. Annu. Rev. Entomol. 47:361-393.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Hanks’ lab for the use of the GC-MS and technical advice, Annie Ray and Emerson Lacey for their help with designing experiments and running the GC/MS, and Art Zangerl for assisting with volatile identification. We also thank the two anonymous reviewers for helpful comments that improved the manuscript. This research was funded by USDA NRI grant #2006-03826.

Author information

Authors and Affiliations

  1. Department of Entomology, University of Illinois at Urbana-Champaign, 505 S. Goodwin Ave, Urbana, IL, 61801, USA

    Allison C. Mooney, Hugh M. Robertson & Kevin W. Wanner

  2. Entomology, Department of Plant Sciences and Plant Pathology, Montana State University, 119 Plant BioSciences, Bozeman, MT, 59717-3150, USA

    Kevin W. Wanner

Authors
  1. Allison C. Mooney
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hugh M. Robertson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kevin W. Wanner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kevin W. Wanner.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Volatile profile of filter paper exposed to mature mulberry leaves that were fed upon for 24 h by neonate silkworm larvae. One major peak (peak #C) representing α-farnesene was detected. Two minor peaks were identified as 6-methyl-5-hepten-2-one (peak A) and (Z)-3-hexenyl 2-methylbutanoate (peak B). Retention time (min) is labeled on the x-axis, relative abundance (×106) on the y-axis. (GIF 9 kb)

High resolution image (EPS 1192 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mooney, A.C., Robertson, H.M. & Wanner, K.W. Neonate Silkworm (Bombyx mori) Larvae Are Attracted to Mulberry (Morus alba) Leaves with Conspecific Feeding Damage. J Chem Ecol 35, 552–559 (2009). https://doi.org/10.1007/s10886-009-9639-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-009-9639-z

Keywords

Search

Navigation