, Volume 142, Issue 4, pp 529–540 | Cite as

Impacts of biological control and invasive species on a non-target native Hawaiian insect

  • M. Tracy JohnsonEmail author
  • Peter A. Follett
  • Andrew D. Taylor
  • Vincent P. Jones
Population Ecology


The potential for classical biological control to cause unintended harm to native species was evaluated in the case of the endemic Hawaiian koa bug, Coleotichus blackburniae White (Hemiptera: Scutelleridae), and parasitoids introduced to Hawaii for control of an agricultural pest, the southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae). Parasitism of C. blackburniae eggs, nymphs and adults by biocontrol agents was quantified across a wide range of habitats and compared to other sources of mortality. Egg mortality due to the biocontrol agent Trissolcus basalis Wollaston (Hymenoptera: Scelionidae) was low (maximum 26%) and confined to elevations below 500 m on a single host plant. Predation, mainly by alien spiders and ants, was the greatest source of egg mortality (maximum 87%). Parasitism of adult C. blackburniae by the biocontrol agent Trichopoda pilipes (F.) (Diptera: Tachinidae) was near zero at 21 of 24 sites surveyed. Three sites with high bug density had higher levels of T. pilipes parasitism, reaching maxima of 70% among adult female bugs, 100% among males and 50% among fifth instars. Male-biased parasitism indicated that T. pilipes is adapted to using male aggregation pheromone for finding C. blackburniae hosts. The relative impacts of biocontrol agents and other sources of mortality were compared using life tables. Invasive species, particularly generalist egg predators, had the greatest impacts on C. blackburniae populations. Effects of intentionally introduced parasitoids were relatively minor, although the tachinid T. pilipes showed potential for large impacts at individual sites. In retrospect, non-target attacks by biological control agents on C. blackburniae were predictable, but the environmental range and magnitude of impacts would have been difficult to foresee.


Coleotichus blackburniae Life table Nezara viridula Trichopoda pilipes Trissolcus basalis 



For technical assistance we thank Jan Wolff, Jing Zhang, Michelle Hanano, Kelly Funes, Annie Tran, Marcus Hayden, Wendy Kunimitsu, Vanessa Johnson, Garett Chang, Jeremy Kaneshiro, Denis Krot, Marisa Heath, Maria Aihara-Sasaki and Donna Ohora. Gary Gibson of Agriculture Canada identified our egg parasitoids. Jim Baldwin assisted with statistical analyses. Julie Denslow, Roger Vargas and anonymous reviewers helped improve the manuscript. The Hawaii Department of Land and Natural Resources and Hawaii Volcanoes National Park granted us collecting permits. This work was supported with funding from the USDA National Research Initiative and the University of Hawaii Research Council.


  1. Aldrich JR, Lusby WR, Marron BE, Nicolaou KC, Hoffmann MP, Wilson LT (1989) Pheromone blends of green stink bugs and possible parasitoid selection. Naturwissenschaften 76:173–175Google Scholar
  2. Beardsley JW (1965) Notes and exhibitions. Proc Hawaiian Entomol Soc 19:25–26Google Scholar
  3. Beardsley JW (1966) Insects and other terrestrial arthropods from the leeward Hawaiian Islands. Proc Hawaiian Entomol Soc 19:157–185Google Scholar
  4. Bellows TS, Van Driesche RG, Elkinton JS (1992) Life-table construction and analysis in the evaluation of natural enemies. Annu Rev Entomol 37:587–614CrossRefGoogle Scholar
  5. Bin F, Vinson SB, Strand MR, Colazza S, Jones WA (1993) Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula . Physiol Entomol 18:7–15Google Scholar
  6. Clarke AR, Seymour JE (1992) Two species of Acroclisoides Girault & Dodd (Hymenoptera: Pteromalidae) parasitic on Trissolcus basalis Wollaston (Hymenoptera: Scelionidae), a parasitoid of Nezara viridula L. (Hemiptera: Pentatomidae). J Aust Entomol Soc 31:299–300Google Scholar
  7. Colazza S, Salerno G, Wajnberg E (1999) Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol Control 16:310–317CrossRefGoogle Scholar
  8. Davis CJ (1964) The introduction, propagation, liberation, and establishment of parasites to control Nezara viridula variety smaragdula (Fabricius) in Hawaii (Heteroptera: Pentatomidae). Proc Hawaiian Entomol Soc 18:369–375Google Scholar
  9. Davis CJ (1967) Progress in the biological control of the southern green stink bug, Nezara viridula variety smaragdula (Fabricius) in Hawaii (Heteroptera: Pentatomidae). Mushi 39(Suppl):9–16Google Scholar
  10. Duan JJ, Messing RH (1999) Evaluating nontarget effects of classical biological control: fruit fly parasitoids in Hawaii as a case study. In: Follett PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer, Boston, pp 95–109Google Scholar
  11. Follett PA, Duan JJ (1999) Nontarget effects of biological control. Kluwer, Boston, p 316Google Scholar
  12. Follett PA, Duan J, Messing RH, Jones VP (2000) Parasitoid drift after biological control introductions: re-examining Pandora’s box. Am Entomol 46:82–94Google Scholar
  13. Funasaki GY, Lai P-Y, Nakahara LM, Beardsley JW, Ota AK (1988) A review of biological control introductions in Hawaii: 1890–1985. Proc Hawaiian Entomol Soc 28:105–160Google Scholar
  14. Gambino P (1992) Yellowjacket (Vespula pensylvanica) predation at Hawaii Volcanoes and Haleakala National Parks: identity of prey items. Proc Hawaiian Entomol Soc 31:157–164Google Scholar
  15. Hardy DE (1950) Notes and exhibitions. Proc Hawaiian Entomol Soc 14:19–20Google Scholar
  16. Hardy DE (1952) Notes and exhibitions. Proc Hawaiian Entomol Soc 14:352Google Scholar
  17. Harris VE, Todd JW (1980) Male-mediated aggregation of male, female, and 5th instar southern green stink bugs and concomitant attraction of a tachinid parasite, Trichopoda pennipes. Entomol Exp Appl 27:117–126Google Scholar
  18. Harris VE, Todd JW (1981) Validity of estimating percentage parasitization of Nezara viridula populations by Trichopoda pennipes using parasite-egg presence on the host cuticle as the indicator. J Ga Entomol Soc 16:505–510Google Scholar
  19. Harris VE, Todd JW (1982) Longevity and reproduction of the southern green stink bug, Nezara viridula, as affected by parasitization by Trichopoda pennipes. Entomol Exp Appl 31:409–412Google Scholar
  20. Hawaii Audubon Society (1989) Hawaii’s birds. Hawaii Audubon Society, HonoluluGoogle Scholar
  21. Hawkins BA (1994) Pattern and process in host-parasitoid interactions. Cambridge University Press, Cambridge, p 190Google Scholar
  22. Henneman ML, Memmott J (2001) Infiltration of a Hawaiian community by introduced biological control agents. Science 293:1314–1316CrossRefPubMedGoogle Scholar
  23. Howarth FG (1983) Classical biocontrol: panacea or Pandora’s box? Proc Hawaiian Entomol Soc 24:239–244Google Scholar
  24. Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509CrossRefGoogle Scholar
  25. Jones WA (1988) World review of the parasitoids of the southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae). Ann Entomol Soc Am 81:262–273Google Scholar
  26. Jones VP (1995) Reassessment of the role of predators and Trissolcus basalis in biological control of southern green stink bug (Hemiptera: Pentatomidae) in Hawaii. Biol Control 5:566–572CrossRefGoogle Scholar
  27. Jones VP, Westcot D (2002) The effect of seasonal changes on Nezara viridula (L.) (Hemiptera: Pentatomidae) and Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) in Hawaii. Biol Control 23:115–120CrossRefGoogle Scholar
  28. Jones VP, Westcott DM, Finson NN, Nishimoto RK (2001) Relationship between community structure and southern green stink bug (Hemiptera: Pentatomidae) damage in macadamia nuts. Environ Entomol 30:1028–1035Google Scholar
  29. Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Non-target effects—the Achilles’ heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu Rev Entomol 48:365–96CrossRefPubMedGoogle Scholar
  30. Lynch LD, Thomas MB (2000) Nontarget effects in the biological control of insects with insects, nematodes and microbial agents: the evidence. Biocontrol News Inf 21:117–130Google Scholar
  31. Mitchell WC, Mau RFL (1971) Response of the female southern green stink bug and its parasite, Trichopoda pennipes, to male stink bug pheromones. J Econ Entomol 64:856–859Google Scholar
  32. Nishida T (1966) Behavior and mortality of the southern green stink bug Nezara viridula in Hawaii. Res Popul Ecol 8:78–88Google Scholar
  33. Nishida GM (2002) Hawaiian terrestrial arthropod checklist. Bishop Museum Technical Report No. 24. Bishop Museum, HonoluluGoogle Scholar
  34. Noyes JS (2003) Universal Chalcidoidea database. World Wide Web electronic publication [accessed 2 July 2004]
  35. Onstad DW, McManus ML (1996) Risks of host range expansion by parasites of insects. Bioscience 46:430–35Google Scholar
  36. Reimer NJ (1994) Distribution and impact of alien ants in vulnerable Hawaiian ecosystems. In: Williams DF (ed) Exotic ants: biology, impact, and control of introduced species. Westview Press, Boulder, Col., pp 11–22Google Scholar
  37. SAS (2000) SAS/STAT user’s guide. Version 8. SAS Institute, Cary, N.C.Google Scholar
  38. Shahjahan M (1968) Superparasitization of the southern green stink bug by the tachinid parasite Trichopoda pennipes pilipes and its effect on the host and parasite survival. J Econ Entomol 61:1088–1091Google Scholar
  39. Van Driesche RG, Hoddle M (1997) Should arthropod parasitoids and predators be subject to host range testing when used as biological control agents? Agric Hum Values 14:211–226CrossRefGoogle Scholar
  40. Van Zwaluwenburg RH (1954) Notes and exhibitions. Proc Hawaiian Entomol Soc 15:281Google Scholar
  41. Wagner WL, Herbst DR, Sohmer SH (1990) Manual of the flowering plants of Hawai’i. Bishop Museum Press, HonoluluGoogle Scholar
  42. Wajnberg E, Scott JK, Quimby PC (2001) Evaluating indirect ecological effects of biological control. CAB International, WallingfordGoogle Scholar
  43. Zimmerman EC (1948a) Insects of Hawaii, vol 3. Heteroptera. University of Hawaii Press, HonoluluGoogle Scholar
  44. Zimmerman EC (1948b) Insects of Hawaii, vol 4. Homoptera: Auchenorryncha. University of Hawaii Press, HonoluluGoogle Scholar
  45. Zimmerman EC (1978) Insects of Hawaii, vol 9. Microlepidoptera, part I. University of Hawaii Press, HonoluluGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • M. Tracy Johnson
    • 1
    • 5
    Email author
  • Peter A. Follett
    • 2
  • Andrew D. Taylor
    • 3
  • Vincent P. Jones
    • 4
    • 5
  1. 1.Institute of Pacific Islands ForestryPacific Southwest Research Station, USDA Forest ServiceVolcanoUSA
  2. 2.Pacific Basin Agricultural Research CenterUSDA-ARSHiloUSA
  3. 3.Department of ZoologyUniversity of Hawaii at ManoaHonoluluUSA
  4. 4.Tree Fruit Research and Extension CenterWashington State UniversityWenatcheeUSA
  5. 5.Department of EntomologyUniversity of Hawaii at ManoaHonoluluUSA

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