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Modeling the decline and potential recovery of a native butterfly following serial invasions by exotic species

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Abstract

Population sizes and range of the native butterfly Pieris oleracea declined after habitat loss and parasitism by an exotic braconid wasp (Cotesia glomerata) introduced to control the exotic invasive butterfly Pieris rapae. Further declines are attributed to the invasive exotic weed garlic mustard (Alliaria petiolata), an oviposition sensory trap on which P. oleracea larval survival and growth are very poor. But a population of P. oleracea has adapted to garlic mustard over the past several decades, coincident with the introduction of a second parasitoid, C. rubecula, a specialist on P. rapae that is competitively dominant to C. glomerata. We used stochastic simulation models to assess the plausibility of a hypothesis that reduced parasitoid pressure over this time period enabled P. oleracea to adapt to A. petiolata. We simulated scenarios of trait proliferation via spontaneous mutation or immigration of the trait, and residual variation in the trait following the butterfly’s isolation in North America. Results indicate that the most likely scenario for the population that has adapted to garlic mustard includes (1) a change in selection following garlic mustard invasion to favor previously neutral residual variation in the population, (2) release from parasitism, and (3) evolution of improved larval survival on garlic mustard, which allowed an increased host range, and potentially, population size.

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References

  • Benson J, Van Driesche R, Pasquale A, Elkinton J (2003) Introduced braconid parasitoids and range reduction of a native butterfly in New England. Biol Control 28:197–213

    Article  Google Scholar 

  • Bigger DS, Fox LR (1997) High-density populations of diamond back moth have broader host-plant diets. Oecologia 112:179–186

    Article  Google Scholar 

  • Bowden S (1971) American white butterflies (Pieridae) and English food-plants. J Lepid Soc 25:6–12

    Google Scholar 

  • Bowden S (1979) Subspecific variation in butterflies: adaptation and dissected polymorphism in Pieris (Artogeia) (Pieridae). J Lepid Soc 33:77–111

    Google Scholar 

  • Bowers M, Stamp N, Collinge S (1992) Early stage of host range expansion by a specialist herbivore, Euphydryas phaeton (Nymphalidae). Ecology 73:526–536

    Article  Google Scholar 

  • Brodeur J, Geervliet J, Vet L (1996) The role of host species, age and defensive behavior on ovipositional decisions in a solitary specialist and gregarious generalist parasitoid (Cotesia species). Entomol Exp Appl 81:125–132

    Article  Google Scholar 

  • Camara MD (1997) A recent host range expansion in Junonia coenia Hubner (Nymphalidae): oviposition preference, survival, growth, and chemical defense. Evolution 51:873–884

    Article  Google Scholar 

  • Casagrande R, Dacey J (2007) Monarch butterfly oviposition on swallow-worts (Vincetoxicum spp.). Environ Entomol 36:631–636

    Article  CAS  PubMed  Google Scholar 

  • Chew FS (1975) Coevolution of pierid butterflies and their cruciferous food plants. I. The relative quality of available resources. Oecologia 20:117–127

    Article  Google Scholar 

  • Chew FS (1981) Coexistence and local extinction in two pierid butterflies. Am Nat 118:655–672

    Article  Google Scholar 

  • Chew FS, Renwick JAA (1995) Host plant choice in Pieris butterflies. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects 2. Chapman & Hall, New York, pp 214–238

    Chapter  Google Scholar 

  • Chew FS, Watt WB (2006) The green-veined white (Pieris napi L.), its Pierine relatives, and the systematics dilemmas of divergent character sets (Lepidoptera, Pieridae). Biol J Linn Soc 88:413–435

    Article  Google Scholar 

  • Chew FS, Van Driesche RG, Casagrande RA (2012) A native butterfly confronts exotic plants and parasitoids. Mass Butterflies 39:1–6

  • Clausen C (1978) Introduced parasites and predators of arthropod pests and weeds: a world review. United States Department of Agriculture, Washington

    Google Scholar 

  • Courant A (1996) The effect of a naturalized crucifer on the feeding ecology of Pieris napi oleracea and Pieris virginiensis (Lepidoptera: Pieridae). M.S. thesis, Tufts University, Medford

  • Courant A, Holbrook A, Van der Reijden E, Chew F (1994) Native pierine butterfly (Pieridae) adapting to naturalized crucifer? J Lepid Soc 48:168–170

    Google Scholar 

  • Cox G (2004) Alien species and evolution: the evolutionary ecology of exotic plants, animals, microbes, and interacting native species. Island Press, Washington

    Google Scholar 

  • Davis SL, Cipollini D (2014) The oviposition preference and larval performance of Pieris virginiensis on the novel, invasive host Alliaria petiolata. Biol Invasions 16:1941–1950

  • Dyer LA, Floyd T (1993) Determinants of predation on phytophagous insects: the importance of diet breadth. Oecologia 96:575–582

    Article  Google Scholar 

  • Feeny P, Rosenberry L (1982) Seasonal variation in the glucosinolate content of North American Brassica nigra and Dentaria species. Biochem Syst Ecol 10:23–32

    Article  CAS  Google Scholar 

  • Forister ML, Scholl CF (2012) Use of an exotic host plant affects mate choice in an insect herbivore. Am Nat 179:805–810

    Article  PubMed  Google Scholar 

  • Forister ML, Wilson JS (2013) The population ecologyof novel plant-herbivore interactions. Oikos 122:657–666

    Article  Google Scholar 

  • Fox L, Eisenbach J (1992) Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers. Oecologia 89:574–579

    Article  Google Scholar 

  • Gratton C (2006) Interactions between a native silkmoth Hemileuca sp. and an invasive wetland plant, Lythrum salicaria. Ann Entomol Soc Am 99:1182–1190

    Article  Google Scholar 

  • Harcourt DG (1961) Spatial pattern of the imported cabbage-worm Pieris rapae (L.) (Lepidoptera: Pieridae) on cultivated Cruciferae. Can Entomol 93:945–952

    Article  Google Scholar 

  • Hardy PB, Dennis RLH (2008) Resources for British butterflies (Lepidoptera: Hesperioidea, Papilionoidea). The alien consumer component and its significance for butterfly habitats. Eur J Entomol 105:649–657

    Article  Google Scholar 

  • Harvey JA, Biere A, Fortuna T, Vet LEM, Engelkes T, Morrien E, Gols R, Verhoeven K, Vogel H, Macel M, Heidel-Fischer HM, Schramm K, van der Putten WH (2010a) Ecological fits, mis-fits and lotteries involving insect herbivores on the invasive plant, Bunias orientalis. Biol Invasions 12:3045–3059

    Article  Google Scholar 

  • Harvey JA, Bukovinsk T, van der Putten WH (2010b) Interactions between invasive plants and insect herbivores: a plea for a multitrophic perspective. Biol Conserv 143:2251–2259

    Article  Google Scholar 

  • Hedrick PW (2013) Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol 22:4606–4618

    Article  PubMed  Google Scholar 

  • Herlihy MV (2012) Interactions between Pieris oleracea and Pieris rapae (Lepidoptera: Pieridae) butterflies and biological control agents Cotesia glomerata and Cotesia rubecula (Hymenoptera: Braconidae). M.S. Thesis, University of Massachusetts, Amherst

  • Herlihy MV, Van Driesche RG, Abney MR, Brodeur J, Bryant AB, Casagrande RA, Delaney DA, Elkner TE, Fleischer SJ, Groves RL, Gruner DS, Harmon JP, Heimpel GE, Hemady K, Kuhar TP, Maund CM, Shelton AM, Seaman AJ, Skinner M, Weinzierl P, Yeargan KV, Szendrei Z (2012) Distribution of Cotesia rubecula (Hymenoptera: Braconidae) and its displacement of Cotesia glomerata in eastern North America. Fla Entomol 95:461–467

    Article  Google Scholar 

  • Huang X, Renwick J, Chew F (1995) Oviposition stimulants and deterrents control acceptance of Alliaria petiolata by Pieris rapae and P. napi oleracea. Chemoecology 5:79–87

    CAS  Google Scholar 

  • Jahner JP, Bonilla MM, Badik KJ, Shapiro AM, Forister ML (2011) Use of exotic hosts by Lepidoptera: widespread species colonize more novel hosts. Evolution 65:2719–2724

    Article  PubMed  Google Scholar 

  • Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286

    Article  Google Scholar 

  • Keeler M, Chew F (2008) Escaping an evolutionary trap: preference and performance of a native insect on an exotic invasive host. Oecologia 156:559–568

    Article  PubMed  Google Scholar 

  • Keeler M, Chew F, Goodale BC, Reed JM (2006) Modelling the impacts of two exotic invasive species on a native butterfly: top-down vs. bottom-up effects. J Anim Ecol 75:777–788

    Article  PubMed  Google Scholar 

  • Klots A (1951) A field guide to the butterflies of North America east of the Great Plains. Houghton Mifflin, Boston

    Google Scholar 

  • Knerl A, Bowers MD (2013) Incorporation of an introduced weed into the diet of a native butterfly: consequences for preference, performance and chemical defense. J Chem Ecol 39:1313–1321

    Article  CAS  PubMed  Google Scholar 

  • Laing J, Corrigan J (1987) Intrinsic competition between the gregarious parasite, Cotesia glomeratus and the solitary parasite, Cotesia rubecula (Hymenpotera: Braconidae) for their host, Artogeia rapae (Lepidoptera: Pieridae). Entomophaga 32:493–501

    Article  Google Scholar 

  • Lau JA (2006) Evolutionary responses of native plants to novel community members. Evolution 60:56–63

    Article  PubMed  Google Scholar 

  • Longstaff G (1912) Butterfly-hunting in many lands. Longmans and Green, New York

    Google Scholar 

  • Massachusetts Natural Heritage and Endangered Species Program (2010) http://www.mass.gov/eea/agencies/dfg/dfw/natural-heritage/species-information-and-conservation/mesa-list/list-of-rare-species-in-massachusetts.html

  • Mooney KA, Pratt RT, Singer MS (2012) The tri-tropohic interactions hypothesis: interactive effects of host plant quality, diet breadth and natural enemies on herbivores. PLoS ONE 7:e34403

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Murphy S (2004) Enemy-free space maintains swallowtail butterfly host shift. Proc Natl Acad Sci USA 101:18048–18052

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakajima M, Boggs CL, Chew FS, Cummings A, Bowsher J (2014) Dynamics and structure of a native Pieris population in the presence of a non-native, toxic larval host plant. J Lepid Soc 68:175–184

  • Nuzzo V (1993) Distribution and spread of the invasive biennial Alliaria petiolata (garlic mustard) in North America. Biology pollution, the control and impact of invasive exotic species. In: McNight BN (ed) Biological pollution: the control and impact of invasive exotic species. Indiana Academy of Sciences, Indianapolis, pp 137–145

  • Ohsaki N, Sato Y (1994) Food plant choice of Pieris butterflies as a trade-off between parasitoid avoidance and quality of plants. Ecology 75:59–68

    Article  Google Scholar 

  • Ohsaki N, Sato Y (1999) The role of parasitoids in evolution of habitat and larval food plant preference by three Pieris butterflies. Res Popul Ecol 41:107–119

    Article  Google Scholar 

  • Opler P, Krizek G (1984) Butterflies east of the Great Plains. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Pearse IS, Altermatt F (2013) Predicting novel trophic interactions in a non-native world. Ecol Lett 16:1088–1094

    Article  PubMed  Google Scholar 

  • Porter A (1994) Implications of introduced garlic mustard (Alliaria petiolata) in the habitat of Pieris virginiensis (Pieridae). J Lepid Soc 48:171–172

    Google Scholar 

  • Reznick D, Ghalambor C (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112–113:183–198

    Article  PubMed  Google Scholar 

  • Schlaepfer M, Runge M, Sherman P (2002) Ecological and evolutionary traps. Trends Ecol Evol 17:474–480

    Article  Google Scholar 

  • Scudder S (1889) The Butterflies of the Eastern United States. Houghton Mifflin, Boston

    Google Scholar 

  • Strauss S, Lau J, Carroll S (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374

    Article  PubMed  Google Scholar 

  • Thompson JN (ed) (1999) Coevolution. Am Nat Suppl 153: S1–S93

  • Van Driesche RG (1988) Field measurement of population recruitment of Apanteles glomeratus (L.) (Hymenoptera: Braconidae), a parasitoid of Pieris rapae (L.) (Lepidoptera: Pieridae), and factors influencing adult parasitoid foraging success in kale. Bull Entomol Res 78:199–208

    Article  Google Scholar 

  • 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 91:22–25

    Article  Google Scholar 

  • Van Driesche RG, Nunn C (2002) Establishment of a Chinese strain of Cotesia rubecula (Hymenoptera: Braconidae) in the Northeastern United States. Fla Entomol 85:386–388

    Article  Google Scholar 

  • 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 28:214–221

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Acknowledgments

We thank Tufts University, Department of Biology for resources and support, and M. Keeler for her advice and use of her original model. We thank C. Boggs and S. Davis for sharing their unpublished results. We also thank anonymous reviewers for comments leading to revision and strengthening of the manuscript.

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Authors and Affiliations

  1. Department of Biology, Tufts University, Medford, MA, 02155, USA

    Tegan A. L. Morton, Alexandra Thorn, J. Michael Reed & Frances S. Chew

  2. Department of Entomology, Plant, Soil and Insect Sciences, University of Massachusetts, Amherst, MA, 01002, USA

    Roy G. Van Driesche

  3. Department of Plant Science and Entomology, University of Rhode Island, Kingston, RI, 02881, USA

    Richard A. Casagrande

  4. Institute for the Study of Earth, Oceans, and Space, University of New Hampshire, Durham, NH, 03824, USA

    Alexandra Thorn

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  1. Tegan A. L. Morton
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  2. Alexandra Thorn
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  4. Roy G. Van Driesche
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  5. Richard A. Casagrande
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  6. Frances S. Chew
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Correspondence to Frances S. Chew.

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Morton, T.A.L., Thorn, A., Reed, J.M. et al. Modeling the decline and potential recovery of a native butterfly following serial invasions by exotic species. Biol Invasions 17, 1683–1695 (2015). https://doi.org/10.1007/s10530-014-0826-7

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  • DOI: https://doi.org/10.1007/s10530-014-0826-7

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