Advertisement

Oecologia

, Volume 173, Issue 2, pp 521–532 | Cite as

Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest

  • Jan Hrcek
  • Scott E. Miller
  • James B. Whitfield
  • Hiroshi Shima
  • Vojtech Novotny
Community ecology - Original research

Abstract

The processes maintaining the enormous diversity of herbivore—parasitoid food webs depend on parasitism rate and parasitoid host specificity. The two parameters have to be evaluated in concert to make conclusions about the importance of parasitoids as natural enemies and guide biological control. We document parasitism rate and host specificity in a highly diverse caterpillar-parasitoid food web encompassing 266 species of lepidopteran hosts and 172 species of hymenopteran or dipteran parasitoids from a lowland tropical forest in Papua New Guinea. We found that semi-concealed hosts (leaf rollers and leaf tiers) represented 84 % of all caterpillars, suffered a higher parasitism rate than exposed caterpillars (12 vs. 5 %) and their parasitoids were also more host specific. Semi-concealed hosts may therefore be generally more amenable to biological control by parasitoids than exposed ones. Parasitoid host specificity was highest in Braconidae, lower in Diptera: Tachinidae, and, unexpectedly, the lowest in Ichneumonidae. This result challenges the long-standing view of low host specificity in caterpillar-attacking Tachinidae and suggests higher suitability of Braconidae and lower suitability of Ichneumonidae for biological control of caterpillars. Semi-concealed hosts and their parasitoids are the largest, yet understudied component of caterpillar—parasitoid food webs. However, they still remain much closer in parasitism patterns to exposed hosts than to what literature reports on fully concealed leaf miners. Specifically, semi-concealed hosts keep an equally low share of idiobionts (2 %) as exposed caterpillars.

Keywords

Lepidoptera Specialization Community structure External feeding Malesia 

Notes

Acknowledgments

We thank the New Guinea Binatang Research Center parataxonomists, village assistants, Lauren Helgen, Karolyn Darrow and Kristyna Hrckova for technical assistance and general support. Host plants were identified by George D. Weiblen. Lepidopteran taxonomy was assisted by Jeremy Holloway, Jadranka Rota, Michael Shaffer, Tosio Kumata, Issei Ohshima, and others acknowledged in Craft et al. (2010). Parasitoids were identified by: Kees van Achterberg (Macrocentrinae), Celso Oliveira Azevedo (Bethylidae), Yves Braet (Orgilinae), Michael W. Gates (Chalcidoidea), Ian D. Gauld (Ichneumonidae), Donald L. J. Quicke (Rogadinae and Hormiinae), Michael J. Sharkey (Agathidinae), David Wahl (Ichneumonidae), and Dicky Yu (Cheloninae). This paper is based on work supported by the US National Science Foundation (DEB 0841885), the Czech Science Foundation (206/09/0115 and 13-10486S), the Academy of Sciences of the Czech Republic (IAA600960712), the Czech Ministry of Education (LH11008 and MSM6007665801), and the project CZ.1.07/2.3.00/20.0064 co-financed by the European Social Fund and the state budget of the Czech Republic. The Papua New Guinea caterpillar rearing campaign has been funded by NSF since 1995 in collaboration with George Weiblen and Yves Basset. We thank Paul Hebert, Alex Smith and the Biodiversity Institute of Ontario for the DNA barcodes. Laboratory reagents and BOLD infrastructure were funded by Genome Canada through the Ontario Genomics Institute. We also thank David Wahl, Tom Fayle, Kees van Achterberg, Becky Morris, Owen Lewis, David Storch and two anonymous reviewers for comments on the manuscript.

Supplementary material

442_2013_2619_MOESM1_ESM.doc (1.1 mb)
Supplementary material 1 (DOC 1163 kb)

References

  1. APG III (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121CrossRefGoogle Scholar
  2. Askew RR, Shaw MR (1979) Mortality factors affecting the leaf-mining stages of Phyllonorycter (Lepidoptera, Gracillariidae) on oak and birch. 2. Biology of the parasite species. Zool J Linn Soc 67:51–64CrossRefGoogle Scholar
  3. Askew RR, Shaw MR (1986) Parasitoid communities: their size, structure and development. In: Waage J, Greathead D (eds) Insect Parasitoids. 13th Symposium of the Royal Entomological Society of London. Academic Press, London, pp 225–263Google Scholar
  4. Barbosa P, Caldas A (2004) Patterns of parasitoid-host associations in differentially parasitized macrolepidopteran assemblages on black willow Salix nigra (Marsh) and box elder Acer negundo L. Basic Appl Ecol 5:75–85CrossRefGoogle Scholar
  5. Barbosa P, Tammaru T, Caldas A (2004) Is parasitism of numerically dominant species in macro lepidopteran assemblages independent of their abundance? Basic Appl Ecol 5:357–366CrossRefGoogle Scholar
  6. Belshaw R (1994) Life history characteristics of Tachinidae (Diptera) and their effects on polyphagy. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 145–162Google Scholar
  7. Belshaw R, Fitton M, Herniou E, Gimeno C, Quicke DLJ (1998) A phylogenetic reconstruction of the Ichneumonoidea (Hymenoptera) based on the D2 variable region of 28S ribosomal RNA. Syst Entomol 23:109–123CrossRefGoogle Scholar
  8. Connahs H, Aiello A, Van Bael S, Rodriguez-Castaneda G (2011) Caterpillar abundance and parasitism in a seasonally dry versus wet tropical forest of Panama. J Trop Ecol 27:51–58CrossRefGoogle Scholar
  9. Cornell HV, Hawkins BA (1995) Survival patterns and mortality sources of herbivorous insects—some demographic trends. Am Nat 145:563–593CrossRefGoogle Scholar
  10. Craft KJ, et al. (2010) Population genetics of ecological communities with DNA barcodes: An example from New Guinea Lepidoptera. Proc Natl Acad Sci USA 107:5041–5046CrossRefGoogle Scholar
  11. Diniz IR, Morais HC (1997) Lepidopteran ceterpillar fauna of cerrado host plants. Biodivers Conserv 6:817–836CrossRefGoogle Scholar
  12. Eggleton P, Gaston KJ (1990) Parasitoid species and assemblages—convenient definitions or misleading compromises. Oikos 59:417–421CrossRefGoogle Scholar
  13. Eggleton P, Gaston KJ (1992) Tachinid host ranges: a reappraisal (Diptera: Tachinidae). Entomol Gaz 43:139–143Google Scholar
  14. Gauld ID (1984) An introduction to the Ichneumonidae of Australia; with a contribution on Metopiinae by M.G. Fitton. BM(NH), LondonGoogle Scholar
  15. Gauld ID (1988) Evolutionary patterns of host utilization by ichneumonoid parasitoids (Hymenoptera, Ichneumonidae and Braconidae). Biol J Linn Soc 35:351–377CrossRefGoogle Scholar
  16. Gauld I, Bolton B (1996) The Hymenoptera. Oxford University Press, OxfordGoogle Scholar
  17. Gentry GL, Dyer LA (2002) On the conditional nature of Neotropical caterpillar defenses against their natural enemies. Ecology 83:3108–3119CrossRefGoogle Scholar
  18. Gibson GAP, Huber JT, Woolley JB (eds) (1997) Annotated keys to the genera of Nearctic Chalcidoidea (Hymenoptera). NRC, OttawaGoogle Scholar
  19. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, OxfordGoogle Scholar
  20. Godfray HCJ, Lewis OT, Memmott J (1999) Studying insect diversity in the tropics. Philos Trans R Soc B Biol Sci 354:1811–1824CrossRefGoogle Scholar
  21. Goulet H, Huber JT (eds) (1993) Hymenoptera of the world: an identification guide to families. Research branch, Agriculture CanadaGoogle Scholar
  22. Greathead DJ (1987) Parasitoids in classical biological control. In: Waage JK, Greathead D (eds) Insect parasitoids. Academic Press, London, pp 289–318Google Scholar
  23. Hamilton AJ, et al. (2010) Quantifying uncertainty in estimation of tropical arthropod species richness. Am Nat 176:90–95CrossRefGoogle Scholar
  24. Hanson PE, Gauld ID (eds) (1995) The Hymenoptera of Costa Rica. Oxford University Press, OxfordGoogle Scholar
  25. Hawkins BA (1994) Pattern and process in host-parasitoid interactions. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  26. Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152CrossRefGoogle Scholar
  27. Hespenheide HA (1991) Bionomics of leaf-mining insects. Annu Rev Entomol 36:535–560CrossRefGoogle Scholar
  28. Holloway JD, Kibby G, Peggie D (2001) The families of malesian moths and butterflies. Brill, LeidenGoogle Scholar
  29. Hrcek J, Miller SE, Quicke DLJ, Smith MA (2011) Molecular detection of trophic links in a complex insect host-parasitoid food web. Mol Ecol Resour 11:786–794CrossRefGoogle Scholar
  30. Janzen DH (1995) The caterpillars and their parasitoids of a tropical dry forest. Tachinid Time 8:1–3Google Scholar
  31. Janzen DH, Gauld ID (1997) Patterns of use of large moth caterpillars (Lepidoptera: Saturniidae and Sphingidae) by ichneumonid parasitoids (Hymenoptera) in Costa Rican dry forest. In: Watt AD, Stork NE, Hunter MD (eds) Forests and insects. Chapman & Hall, London, pp 251–271Google Scholar
  32. Kaartinen R, Stone GN, Hearn J, Lohse K, Roslin T (2010) Revealing secret liaisons: DNA barcoding changes our understanding of food webs. Ecol Entomol 35:623–638CrossRefGoogle Scholar
  33. Kidd NAC, Jervis MA (2005) Population dynamics. In: Jervis MA (ed) Insects as natural enemies: a practical perspective. Springer, Dordrecht, pp 435–523CrossRefGoogle Scholar
  34. Le Corff J, Marquis RJ (1999) Differences between understorey and canopy in herbivore community composition and leaf quality for two oak species in Missouri. Ecol Entomol 24:46–58CrossRefGoogle Scholar
  35. Le Corff J, Marquis RJ, Whitfield JB (2000) Temporal and spatial variation in a parasitoid community associated with the herbivores that feed on Missouri Quercus. Environ Entomol 29:181–194CrossRefGoogle Scholar
  36. Leps J, Novotny V, Basset Y (2001) Habitat and successional status of plants in relation to the communities of their leaf-chewing herbivores in Papua New Guinea. J Ecol 89:186–199CrossRefGoogle Scholar
  37. Lewis OT, Memmott J, Lasalle J, Lyal CHC, Whitefoord C, Godfray HCJ (2002) Structure of a diverse tropical forest insect-parasitoid community. J Anim Ecol 71:855–873CrossRefGoogle Scholar
  38. Lill JT, Marquis RJ, Ricklefs RE (2002) Host plants influence parasitism of forest caterpillars. Nature 417:170–173CrossRefGoogle Scholar
  39. McAlpine JR, Keig R, Falls R (1983) Climate of Papua New Guinea. CSIRO and Australian National University Press, CanberraGoogle Scholar
  40. Memmott J, Godfray HCJ, Gauld ID (1994) The structure of a tropical host parasitoid community. J Anim Ecol 63:521–540CrossRefGoogle Scholar
  41. Miller SE, Novotny V, Basset Y (2003) Studies on New Guinea moths. I. Introduction (Lepidoptera). Proc Entomol Soc Wash 105:1034–1042Google Scholar
  42. Mills NJ (1992) Parasitoid guilds, life-styles, and host ranges in the parasitoid complexes of tortricoid hosts (Lepidoptera, Tortricoidea). Environ Entomol 21:230–239Google Scholar
  43. Mills NJ (1993) Species richness and structure in the parasitoid complexes of tortricoid hosts. J Anim Ecol 62:45–58CrossRefGoogle Scholar
  44. Morris RJ, Lewis OT, Godfray HCJ (2004) Experimental evidence for apparent competition in a tropical forest food web. Nature 428:310–313CrossRefGoogle Scholar
  45. Murakami M, Yoshida K, Hara H, Toda MJ (2005) Spatio-temporal variation in Lepidopteran larval assemblages associated with oak, Quercus crispula: the importance of leaf quality. Ecol Entomol 30:521–531CrossRefGoogle Scholar
  46. Murakami M, Hirao T, Ichie T (2007) Comparison of lepidopteran larval communities among tree species in a temperate deciduous forest, Japan. Ecol Entomol 32:613–620CrossRefGoogle Scholar
  47. Novotny V, et al. (2002) Predictably simple: assemblages of caterpillars (Lepidoptera) feeding on rainforest trees in Papua New Guinea. Proc R Soc Lond Ser B Biol Sci 269:2337–2344CrossRefGoogle Scholar
  48. Novotny V, et al. (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–1118CrossRefGoogle Scholar
  49. Novotny V, et al. (2007) Low beta diversity of herbivorous insects in tropical forests. Nature 448:692–695CrossRefGoogle Scholar
  50. Novotny V, et al. (2010) Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. J Anim Ecol 79:1193–1203CrossRefGoogle Scholar
  51. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation - potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330CrossRefGoogle Scholar
  52. Price PW (2002) Resource-driven terrestrial interaction webs. Ecol Res 17:241–247CrossRefGoogle Scholar
  53. Quicke DLJ (1997) Parasitic Wasps. Chapman and Hall, LondonGoogle Scholar
  54. Quicke DLJ, Laurenne NM, Fitton MG, Broad GR (2009) A thousand and one wasps: a 28S rDNA and morphological phylogeny of the Ichneumonidae (Insecta: Hymenoptera) with an investigation into alignment parameter space and elision. J Nat Hist 43:1305–1421CrossRefGoogle Scholar
  55. Quicke DLJ, Smith MA, Miller SE, Hrcek J, Butcher B (2012) Colastomion Baker (Braconidae, Rogadinae): nine new species from Papua New Guinea reared from Crambidae. J Hymenoptera Res 28:85–121CrossRefGoogle Scholar
  56. Salvo A, Valladares GR, Cagnolo L (2011) Parasitic assemblages on leafminers: a comparison of structure and function among host orders. Stud Neotrop Fauna Environ 46:11–22CrossRefGoogle Scholar
  57. Shaw MR (1994) Parasitoid host ranges. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 111–144Google Scholar
  58. Sheehan W (1991) Host range patterns of hymenopteran parasitoids of exophytic lepidopteran folivores. In: Bernays EA (ed) Insect-plant interactions, vol 3. CRC, Boca Raton, pp 209–248Google Scholar
  59. Sheehan W (1994) Parasitoid community structure: effects of host abundance, phylogeny, and ecology. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 90–107Google Scholar
  60. Smith MA, Woodley NE, Janzen DH, Hallwachs W, Hebert PDN (2006) DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proc Natl Acad Sci USA 103:3657–3662CrossRefGoogle Scholar
  61. Smith MA, Wood DM, Janzen DH, Hallwachs W, Hebert PDN (2007) DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proc Natl Acad Sci USA 104:4967–4972CrossRefGoogle Scholar
  62. Smith MA, et al. (2008) Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology and collections. Proc Natl Acad Sci USA 105:12359–12364CrossRefGoogle Scholar
  63. Smith MA, Eveleigh ES, McCann KS, Merilo MT, McCarthy PC, Van Rooyen KI (2011) Barcoding a quantified food web: crypsis, concepts, ecology and hypotheses. PLoS ONE 6:e14424CrossRefGoogle Scholar
  64. Stireman JO, Singer MS (2003) Determinants of parasitoid-host associations: insights from a natural tachinid-lepidopteran community. Ecology 84:296–310CrossRefGoogle Scholar
  65. Stireman JO, et al. (2005) Climatic unpredictability and parasitism of caterpillars: implications of global warming. Proc Natl Acad Sci USA 102:17384–17387CrossRefGoogle Scholar
  66. Tachi T, Shima H (2010) Molecular phylogeny of the subfamily Exoristinae (Diptera, Tachinidae), with discussions on the evolutionary history of female oviposition strategy. Syst Entomol 35:148–163CrossRefGoogle Scholar
  67. Tvardikova K, Novotny V (2012) Predation on exposed and leaf-rolling artificial caterpillars in tropical forests of Papua New Guinea. J Trop Ecol 28:331–341. doi: 310.1017/S0266467412000235 CrossRefGoogle Scholar
  68. Van Driesche RG (1983) The meaning of percent parasitism in studies of insect parasitoids. Environ Entomol 12:1611–1622Google Scholar
  69. Whitfield JB (1994) Mutualistic viruses and the evolution of host ranges in endoparasitoid Hymenoptera. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 111–144Google Scholar
  70. Whitfield JB (2003) Phylogenetic insights into the evolution of parasitism in Hymenoptera. Adv Parasitol 54:69–100CrossRefGoogle Scholar
  71. Whitfield JB, O’Connor JM (2011) Molecular systematics of wasp and polydnavirus genomes and their coevolution. In: Beckage NE, Drezen J-M (eds) Parasitoid viruses. Academic Press, pp 89–97Google Scholar
  72. Whitfield JB, Wagner DL (1988) Patterns in host ranges within the Nearctic species of the parasitoid genus Pholetesor Mason (Hymenoptera, Braconidae). Environ Entomol 17:608–615Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2013

Authors and Affiliations

  • Jan Hrcek
    • 1
  • Scott E. Miller
    • 2
  • James B. Whitfield
    • 3
  • Hiroshi Shima
    • 4
  • Vojtech Novotny
    • 1
  1. 1.Faculty of ScienceUniversity of South Bohemia and Biology Center, Czech Academy of SciencesCeske BudejoviceCzech Republic
  2. 2.National Museum of Natural HistorySmithsonian InstitutionWashington, DCUSA
  3. 3.Department of EntomologyUniversity of IllinoisUrbanaUSA
  4. 4.Kyushu University MuseumKyushu UniversityFukuokaJapan

Personalised recommendations