Biological Invasions

, Volume 16, Issue 12, pp 2713–2724 | Cite as

Persistence in Massachusetts of the veined white butterfly due to use of the invasive form of cuckoo flower

  • M. V. Herlihy
  • R. G. Van Driesche
  • D. L. Wagner
Original Paper


The native pierid butterfly Pieris oleracea underwent a large range reduction in New England in the twentieth century, likely due to the introduction the invasive butterfly Pieris rapae (Lep.: Pieridae) to North America in 1860, and later the oligophagous parasitoid Cotesia glomerata (Hymenoptera: Braconidae) in 1884. Thought extirpated from the state by the 1970s, one large dense population of the butterfly was found in the mid 1980s in a flood plain meadow along the Housatonic River in Lenox, Berkshire Co., Massachusetts. We examined how this native pierid was able to maintain a relatively dense local population by feeding on a novel, invasive host plant, Cardamine pratensis (cuckoo flower), in a meadow habitat despite known parasitoid presence. We approached this question in three ways. First, we deployed trap host plants (cuckoo flower and collards) stocked host larvae (first and second instars of either P. rapae or P. oleracea) at the Lenox site and other locations to determine current rates of C. glomerata attack, for comparison with historical information. Second, we used olfactometer experiments to determine if C. glomerata females could detect the cuckoo flower volatiles released during P. oleracea larval feeding. Third, we used field-cage experiments to determine if the plant architecture found in the flood plain meadow inhibited the ability of C. glomerata females to locate and parasitize hosts. Specifically, we asked if overtopping vegetation prevented or reduced parasitism of P. oleracea larvae feeding on the covered basal rosettes of C. pratensis, which is the physical form of host plant for three of the four butterfly generations at the site.


Biological control Non-target impact Enemy-free space Parasitoid displacement Pieris oleracea Pieris rapae Pieris napi Cotesia glomerata Cotesia rubecula Cardamine pratensis 



The authors thank Richard Casagrande of the University of Rhode Island, George Boettner and Stephen Donahue of the University of Massachusetts Amherst, Patrick DeFlorio of Yankee Glassblower, Jian Duan and Craig Oppel of USDA ARS Newark, DE, Lisa Dachinger of River Valley Farm, Lenox, Massachusetts, and Emmet Van Driesche. For help with the rearing of insects and conduct of sentinel larval studies at Lenox in 2008 and 2009, we thank Alex Meleg, Sabina Perkins, April Rodd, and Ryan Wagner. This material is based upon work supported by the National Institute of food and Agriculture, U.S. Department of Agriculture, the Massachusetts Agricultural Experiment Station and the Department of Plant, Soil and Insect Sciences under Project number MAS00957.


  1. Agerbirk N, Olsen CE, Chew FS, Orgaard M (2010) Variable glucosinolate profiles of Cardamine pratensis (Brassicaceae) with equal chromosome numbers. J Agric Food Chem 58:4693–4700PubMedCrossRefGoogle Scholar
  2. Asher J, Warren M, Fox R, Harding P, Jeffcoate G, Jeffcoate S (2001) Millennium atlas of butterflies in Britain and Ireland. Oxford University Press, New YorkGoogle Scholar
  3. Benson J, van Driesche RG, Pasquale A, Elkinton J (2003) Introduced braconid parasitoids and range reduction of a native butterfly in New England. Biol Cont 28:197–213CrossRefGoogle Scholar
  4. Biever KD (1992) Distribution and occurrence of Cotesia rubecula (Hymenoptera: Braconidae), a parasite of Artogeia rapae in Washington and Oregon. J Econ Entomol 85:739–742Google Scholar
  5. Brodeur J, Geervliet JBF, VET, LEM (1998) Effects of Pieris host species on life history parameters in a solitary specialist and gregarious generalist parasitoid (Cotesia species). Entomol Exp Appl 86:145–152CrossRefGoogle Scholar
  6. Chew FS, van Driesche RG, Casagrande RA (2012) A native butterfly confronts exotic plants and parasitoids. Mass Butterflies 39:2–6Google Scholar
  7. Clausen CP (1978) Introduced parasites and predators of arthropod pests and weeds: a world review. USDA Agriculture Handbook 480, WashingtonGoogle Scholar
  8. Corrigan JE (1982) Cotesia (Apanteles) rubecula [Hymenoptera: Braconidae] recovered in Ottawa, Ontario ten years after its release. Proc Entomol Soc Ontario 113:71Google Scholar
  9. Courant AV, Holbrook AE, van der Reijden ED, Chew FS (1994) Native pierine butterfly (Pieridae) adapting to naturalized crucifer? J Lepid Soc 48:168–170Google Scholar
  10. Geervliet JBF, Ariens S, Dicke M, Vet LEM (1998) Long-distance assessment of patch profitability through volatile infochemicals by the parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae). Biol Cont 11:113–121CrossRefGoogle Scholar
  11. Graves SD, Shapiro AM (2003) Exotics as hosts of the California butterfly fauna. Biol Conserv 110:413–433CrossRefGoogle Scholar
  12. Herlihy MV, van Driesche RG (2013) Effect of Cotesia rubecula (Hymenoptera: Braconidae) on survival of larval cohorts of Pieris rapae (Lepidoptera: Pieridae) on collards: evaluation of an introduced biological control sgent. Fla Entomol 96:360–369CrossRefGoogle Scholar
  13. Herlihy MV, van Driesche RG, Abney MR, Brodeur J, Bryant AB, Casagrande RA, Delaney DA, Elkner TE, Fleischer SL, Groves RL, Gruner DS, Harmon JP, Heimpel GE, Hemady K, Kuhar TP, Maund CM, Olmstead RD, Seaman AM, Skinner M, Weinzierl R, Yeargan KV, Szendrei Z (2012) Occurrence of Cotesia rubecula (Hymenoptera: Braconidae) and its displacement of Cotesia glomerata (Hymenoptera: Braconidae) in eastern North America. Fla Entomol 95:458–464CrossRefGoogle Scholar
  14. Herrera Gonzalez J (1982) La vida silvestre: ¿Se extinguen las mariposas en Chile? Santiago. Academia Superior de Ciencias Pedagogicas de Santiago, ChileGoogle Scholar
  15. Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286CrossRefGoogle Scholar
  16. Karimzadeh J, Hardie J, Wright DJ (2012) Plant resistance affects the olfactory response and parasitism success of Cotesia vestalis. J Insect Behav 25, doi  10.1007/s10905-012-9331-y
  17. Keeler MS, Chew FS (2008) Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oceologia 156:559–568CrossRefGoogle Scholar
  18. Keeler MS, Chew FS, Goodale BC, Reed JM (2006) Modeling the impacts of two exotic invasive species on a native butterfly: top-down vs. bottom-up effects. J Animal Ecol 75:777–788CrossRefGoogle Scholar
  19. Lee JC, Heimpel GE (2005) Impact of flowering buckwheat on lepidopteran cabbage pests and their parasitoids at two spatial scales. Biol Control 34:290–301CrossRefGoogle Scholar
  20. Mattiacci L, Dicke M (1995) Host-age discrimination during host location by Cotesia glomerata, a larval parasitoid of Pieris brassicae. Entomol Exp Appl 76:37–48CrossRefGoogle Scholar
  21. McDonald RC, Kok LT (1992) Colonization and hyperparasitism of Cotesia rubecula (Hymenoptera: Braconidae), a newly introduced parasite of Pieris rapae, in Virginia. Entomophaga 37:223–228CrossRefGoogle Scholar
  22. Meiners T, Obermaier E (2004) Hide and seek on two spatial scales—vegetation structure affects herbivore oviposition and egg parasitism. Basic Appl Ecol 5:87–94CrossRefGoogle Scholar
  23. Obermaier E, Heisswolf A, Poethke HJ, Randlkofer B, Meiners T (2008) Plant architecture and vegetation structure: two ways for insect herbivores to escape parasitism. Eur J Entomol 105:233–240CrossRefGoogle Scholar
  24. Ohsaki N, Sato Y (1990) Avoidance mechanisms of three Pieris butterfly species against the parasitoid wasp Apantales glomeratus. Ecol Entomol 15:169–176CrossRefGoogle Scholar
  25. Parker FD, Pinnell RE (1972) Further studies of the biological control of Pieris rapae using supplemental host and parasite releases. Environ Entomol 1:150–157Google Scholar
  26. Puttler B, Parker FD, Pinnell RE, Thewke SE (1970) Introduction of Apanteles rubecula Marshall and other parasites of Pieris rapae in British Columbia. J Econ Entomol 63:304–305Google Scholar
  27. Sato Y, Ohsaki N (1987) Host-habitat location by Apanteles glomeratus and effect of food-plant exposure on host-parasitism. Ecol Entomol 12:291–297CrossRefGoogle Scholar
  28. Scudder SH (1889) The butterflies of the Eastern United States and Canada. Vol. 1. Pub. by author, CambridgeGoogle Scholar
  29. Shapiro AM (2002) The California urban butterfly fauna is dependent on alien plants. Divers Distrib 8:31–40CrossRefGoogle Scholar
  30. Steinberg S, Dicke M, Vet LEM (1993) Relative Importance of infochemicals from first and second trophic level in long-range host location by the larval parasitoid Cotesia glomerata. J Chem Ecol 19:47–59PubMedCrossRefGoogle Scholar
  31. van Driesche RG (1988) Survivorship patterns of larvae of Pieris rapae (L.) (Lepidoptera: Pieridae) in Massachusetts kale, with special reference to mortality due to Apanteles glomeratus L. (Hymenoptera: Braconidae). Bull Entomol Res 78:397–405CrossRefGoogle Scholar
  32. van Driesche RG (2008) Biological control of Pieris rapae in New England: Host suppression and displacement of Cotesia glomerata by Cotesia rubecula (Hymenoptera: Braconidae). Fla Entomol 91:22–25CrossRefGoogle Scholar
  33. van Driesche RG, Bellows TS (1988) Host and parasitoid recruitment for quantifying losses from parasitism, with reference to Pieris rapae and Cotesia glomerata. Ecol Entomol 13:215–222CrossRefGoogle Scholar
  34. van Driesche RG, Nunn C (2002) Establishment of a Chinese strain of Cotesia rubecula (Hymenoptera: Braconidae) in the northeastern United States. Fla Entomol 85:386–388CrossRefGoogle Scholar
  35. van Driesche RG, Nunn C, Kreke N, Goldstein B, Benson J (2003) Laboratory and field host preferences of introduced Cotesia spp. parasitoids (Hymenoptera: Braconidae) between native and invasive Pieris butterflies. Biol Control 28:214–221CrossRefGoogle Scholar
  36. van Driesche RG, Nunn C, Pasqual A (2004) Life history pattern, host plants, and habitat determinants of population survival of Pieris napi oleracea interacting with an introduced braconid parasitoid. Biol Control 29:278–287CrossRefGoogle Scholar
  37. Williamson GD (1971) Insect liberation in Canada. Parasites and predators 1970. Ag Canada (Liberation Bulletin) No. 34Google Scholar
  38. Williamson GD (1972) Insect liberation in Canada. Parasites and predators 1971. Ag Canada (Liberation Bulletin) No. 35Google Scholar
  39. Wold-Burkness SJ, Hutchison WD, Lee JC, Hines RL, Bolin PC, Heimpel GE (2005) A long-term survey of parasitoid species composition and parasitism of Trichoplusia ni (Lepidoptera: Noctuidae), Plutella xylostella (Lepidoptera : Plutellidae), and Pieris rapae (Lepidoptera: Pieridae) in Minnesota cabbage. J Entomol Sci 40:211–221Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • M. V. Herlihy
    • 1
  • R. G. Van Driesche
    • 1
  • D. L. Wagner
    • 2
  1. 1.Department of Environmental ConservationUniversity of MassachusettsAmherstUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA

Personalised recommendations