Skip to main content
SpringerLink
Log in

Costly leaf shelters protect moth pupae from parasitoids

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Many caterpillars construct shelters by folding leaves and feeding from within. Many shelter-constructing species suffer high rates of parasitism as larvae or pupae. In spite of the likely significance, the effects of these shelters on the survival of pupae and the trade-off between feeding and constructing shelters have attracted little experimental attention. In both field and laboratory experiments, fern-feeding caterpillars [Herpetogramma theseusalis (Walker) (Lepidoptera: Crambidae)] invested heavily in shelters, losing weight and significantly delaying pupation rather than feeding or pupating in exposed locations. Experimentally thinning the walls of shelters in the field doubled the parasitism rate. Parasitism of pupae exceeded predation by an order of magnitude or more in both seasons of this study. Caterpillars constructed similarly sized shelters regardless of availability of fern fronds, resulting in incomplete shelters on especially small fronds, putting pupae at increased risk of parasitism. We suggest that similar interactions are common and merit more attention.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abarca M, Boege K (2011) Fitness costs and benefits of shelter building and leaf trenching behaviour in a pyralid caterpillar. Ecol Entomol 36:564–573

    Article  Google Scholar 

  • Brault S (1991) Host choice and offspring sex allocation in a solitary parasitic wasp. Behav Ecol Sociobiol 29:353–360

    Article  Google Scholar 

  • Cerda O, Hinojosa IA, Thiel M (2010) Shelter-building behavior by the amphipod Peramphithoe femorata (Kroyer) on the kelp Macrocystis pyrifera (Linnaeus) C. Agardh from northern-central Chile. Biol Bull 218:248–258

    PubMed  Google Scholar 

  • Danks HV (2002) Modification of adverse conditions by insects. Oikos 99:10–24

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Diniz IR, Hay JD, Rico-Gray V, Greeney HF, Morais HC (2012) Shelter-building caterpillars in the cerrado: seasonal variation in relative abundance, parasitism, and the influence of extra-floral nectaries. Arthropod Plant Interact 6:583–589

    Article  Google Scholar 

  • Fukui A (2001) Indirect interactions mediated by leaf-shelters in animal-plant communities. Popul Ecol 43:31–40

    Article  Google Scholar 

  • Gentry GL, Dyer LA (2002) On the conditional nature of neotropical caterpillar defenses against their natural enemies. Ecology 83:3108–3119

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids. Princeton University Press, New Jersey

    Google Scholar 

  • Greeney HF, Walla TR, Lynch RL (2010) Architectural changes in larval leaf shelters of Noctuana haematospila (Lepidoptera: Hesperiidae) between host plant species with different leaf thicknesses. Zoologia 27:65–69

    Article  Google Scholar 

  • Greeney HF, Dyer LA, Smilanich AM (2012) Feeding by lepidopteran larvae is dangerous: a review of caterpillars’ chemical, physiological, morphological, and behavioral defenses against natural enemies. Invert Surv J 9:7–34

    Google Scholar 

  • Hagen SB, Sorlibraten O, Ims RA, Yoccoz NG (2006) Density-dependent melanism in winter moth larvae (Lepidoptera: Geometridae): a countermeasure against parasitoids? Environ Entomol 35:1249–1253

    Article  Google Scholar 

  • Hawkins BA (1994) Pattern and process in host–parasitoid interactions. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152

    Article  Google Scholar 

  • Hochberg ME, Hawkins BA (1992) Refuges as a predictor of parasitoid diversity. Science 255:973–976

    Article  PubMed  CAS  Google Scholar 

  • Jervis MA, Kidd NAC (1986) Host-feeding strategies in hymenopterous parasitoids. Biol Rev 61:395–434

    Article  Google Scholar 

  • Jones MT, Castellanos I, Weiss MR (2002) Do leaf-shelters always protect caterpillars from invertebrate predators? Ecol Entomol 27:753–757

    Article  Google Scholar 

  • Lill JT, Marquis RJ (2003) Ecosystem engineering by caterpillars increases insect herbivore diversity on white oak. Ecology 84:682–690

    Article  Google Scholar 

  • Lill JT, Marquis RJ (2007) Microhabitat manipulation: ecosystem engineering by shelter-building insects. In: Cuddington K, Byers JE, Wilson WG, Hastings A (eds) Ecosystem engineers. Academic Press, London, pp 107–138

    Chapter  Google Scholar 

  • Lill JT, Marquis RJ, Walker MA, Peterson L (2007) Ecological consequences of shelter sharing by leaf-tying caterpillars. Entomol Exp Appl 124:45–53

    Article  Google Scholar 

  • Loeffler CC (1994) Natural history of leaf-folding caterpillars, Dichomeris spp. (Gelechiidae), on goldenrods and asters. J N Y Entomol Soc 102:405–428

    Google Scholar 

  • Loeffler CC (1996a) Caterpillar leaf folding as a defense against predation and dislodgement: staged encounters using Dichomeris (Gelechiidae) larvae on goldenrods. J Lepid Soc 50:245–260

    Google Scholar 

  • Loeffler CC (1996b) Adaptive trade-offs of leaf folding in Dichomeris caterpillars on goldenrods. Ecol Entomol 21:34–40

    Article  Google Scholar 

  • Martinsen GD, Floate KD, Waltz AM, Wimp GM, Whitham TG (2000) Positive interactions between leafrollers and other arthropods enhance biodiversity on hybrid cottonwoods. Oecologia 123:82–89

    Article  Google Scholar 

  • Morse DH (2009) Four-level interactions: herbivore use of ferns and subsequent parasitoid-hyperparasitoid performance. Ecol Entomol 34:246–253

    Article  Google Scholar 

  • Morse DH (2011) Size and development times of herbivorous host and parasitoid on distantly related foodplants. Am Midl Nat 166:252–265

    Article  Google Scholar 

  • Nakamura M, Ohgushi T (2003) Positive and negative effects of leaf shelters on herbivorous insects: linking multiple herbivore species on a willow. Oecologia 136:445–449

    Article  PubMed  Google Scholar 

  • Ruehlmann TE, Matthews RW, Matthews JR (1988) Roles for structural and temporal shelter-changing by fern-feeding lepidopteran larvae. Oecologia 75:228–232

    Article  Google Scholar 

  • Sagers CL (1992) Manipulation of host plant quality: herbivores keep leaves in the dark. Funct Ecol 6:741–743

    Article  Google Scholar 

  • Schott T, Hagen SB, Ims RA, Yoccoz NG (2010) Are population outbreaks in sub-arctic geometrids terminated by larval parasitoids? J Anim Ecol 79:701–708

    Article  PubMed  Google Scholar 

  • Smith HD (1932) Phaeogenes nigridens Wesmael, an important ichneumonid parasitoid of the European corn borer. Washington, DC, US Department of Agriculture, USDA Technical Bulletin 331, 46pp

  • Sokal RR, Rohlf FJ (1969) Biometry. W.H. Freeman & Co., San Francisco

    Google Scholar 

  • Wiklund C, Sillén-Tullberg B (1985) Why distasteful butterflies have aposematic larvae and adults, but cryptic pupae: evidence from predation experiments on the monarch and the European swallowtail. Evolution 39:1155–1158

    Article  Google Scholar 

Download references

Acknowledgments

We thank E.K. Morse, G.Chapman and N.H. Rose for assistance in the field; and K.J. Eckelbarger, T.E. Miller, L. Healy and other staff members of the Darling Marine Center of the University of Maine for facilitating work on the premises. B. Hawkins, R. Karban, N.H. Rose, J.K. Waage, J.D. Witman, I. Pearse and several anonymous reviewers read earlier drafts of the manuscript and contributed much helpful commentary. We thank D.L. Wagner, University of Connecticut, for identifying Herpetogramma theseusalis; M.J. Sharkey, University of Kentucky, for identifying Alabagrus texanus; and D. Wahl, American Entomological Institute, Gainesville, Florida, for determination of the ichneumonid wasps. R. Carlson, D. Bragg and E. Diller provided many useful references and much information on the parasitoids. E.F. LoPresti was supported by a Brown University undergraduate research award 2009–2010.

Author information

Authors and Affiliations

  1. Graduate Group in Ecology, Department of Entomology and Center for Population Biology, University of California, Davis, 1 Shields Ave., Davis, CA, USA

    E. F. LoPresti

  2. Department of Ecology and Evolutionary Biology, Brown University, 79 Waterman St., Providence, RI, USA

    E. F. LoPresti & D. H. Morse

Authors
  1. E. F. LoPresti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. H. Morse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. F. LoPresti.

Additional information

Handling Editor: Robert Glinwood.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (MPG 5958 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

LoPresti, E.F., Morse, D.H. Costly leaf shelters protect moth pupae from parasitoids. Arthropod-Plant Interactions 7, 445–453 (2013). https://doi.org/10.1007/s11829-013-9261-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-013-9261-4

Keywords

Search

Navigation