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European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America

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Abstract

We consider the possibility of an extensive invasional meltdown occurring in central North America involving eleven Eurasian species. The scenario begins with the potential co-facilitation between the European earthworm Lumbricus terrestris and European buckthorn, Rhamnus cathartica. Once introduced, European buckthorn has served as the overwintering host for two important invasive crop pests, oat crown rust, Puccinea coronata and the soybean aphid, Aphis glycines. The spread of R. cathartica itself may have been aided by seed dispersal by the European starling, Sturnus vulgaris, and the presence of L. terrestris has likely facilitated the invasion of Bipalium adventitium, an Asian predatory flatworm that specializes on earthworms. Beyond this, the soybean aphid is consumed by a number of introduced species, including the lady beetle Harmonia axyridis, the ground beetle Agonum muelleri and the parasitoid Aphelinus certus. We hypothesize that the presence of soybean aphid increases regional abundances of these species. We discuss both the evidence for this multi-species invasional meltdown scenario and potential implications of meltdown dynamics for invasive species management. The particular management issues that we discuss are: (1) opportunities for managing multiple invasive species simultaneously by targeting facilitator species, and (2) implications of meltdown dynamics for biological control introductions against the soybean aphid.

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References

  • Abrams PA (1987) On classifying interactions between populations. Oecologia 73:272–281

    Google Scholar 

  • Aplet GH, Anderson SJ, Stone CP (1991) Association between feral pig disturbance and the composition of some alien plant assemblages in Hawaii Volcanoes National Park. Plant Ecol 95:55–62

    Google Scholar 

  • Bahlai CA, Welsman JA, Schaafsma AW, Sears MK (2007) Development of soybean aphid (Homoptera: Aphididae) on its primary overwintering host, Rhamnus cathartica. Environ Entomol 36:998–1006

    PubMed  CAS  Google Scholar 

  • Bahlai CA, Sikkema S, Hallett RH, Newman JA, Schaafsma AW (2008) Modeling distribution and abundance of soybean aphid in soybean fields using measurements from the surrounding landscapes. Abstract; Entomological Society of America Annual Meeting; Nov. 16–19, Reno

  • Belaoussoff S, Kevan PG, Murphy S, Swanton C (2003) Assessing tillage disturbance on assemblages of ground beetles (Coleoptera: Carabidae) by using a range of ecological indices. Biodivers Conserv 12:851–882

    Google Scholar 

  • Bianchi FJJA, van der Werf W (2004) Model evaluation of the function of prey in non-crop habitats for biological control by ladybeetles in agricultural landscapes. Ecol Modell 171:177–193

    Google Scholar 

  • Bousquet Y, Larochelle A (1993) Catalogue of the Geadephaga (Coleoptera: Trachypachidae, Rhysodidae, Carabidae including Cicindelini) of American north of Mexico. Mem Entomol Soc Can 167:1–397

    Google Scholar 

  • Bowles ML, Jacobs KA, Mengler JL (2007) Long-term changes in an oak forest’s woody understory and herb layer with repeated burning. J Torrey Bot Soc 134:223–237

    Google Scholar 

  • Butt KR, Shipitalo MJ, Bohlen PJ, Edwards WM, Parmelee RW (1999) Long-term trends in earthworm populations of cropped experimental watersheds in Ohio, USA. Pedobiologia 43:713–719

    Google Scholar 

  • Byers RA, Barker GM, Davidson RL, Hoebeke ER, Sanderson MA (2000) Richness and abundance of Carabidae and Staphylinidae (Coleoptera), in northeastern dairy pastures under intensive grazing. Gt Lakes Entomol 33:81–105

    Google Scholar 

  • Cardenas AM, Buddle CM (2007) Distribution and potential range expansion of seven introduced ground beetle species (Coleoptera : Carabidae) in Quebec, Canada. Coleopt Bull 61:135–142

    Google Scholar 

  • Catling PM, Porebski ZS (1994) The history of invasion and current status of glossy buckthorn, Rhamnus frangula, in southern Ontario. Can Field-Nat 108:305–310

    Google Scholar 

  • Chacon J, Heimpel GE (in press) Density-dependent intraguild predation of an aphid parasitoid. Oecologia

  • Chacon JM, Landis DA, Heimpel GE (2008) Potential for biotic interference of a classical biological control agent of the soybean aphid. Biol Control 46:216–225

    CAS  Google Scholar 

  • Chapin JB, Brou VA (1991) Harmonia Axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proc Entomol Soc Wash 93:630–635

    Google Scholar 

  • Chong J, Kolmer JA (1993) Virulence dynamics and phenotypic diversity of Puccinia coronata f. sp. avenae in Canada from 1974 to 1990. Can J Bot 71:248–255

    Google Scholar 

  • Chong J, Zegeye T (2004) Physiologic specialization of Puccinia coronata f. sp avenae, the cause of oat crown rust, in Canada from 1999 to 2001. Can J Plant Pathol-Revue Canadienne De Phytopathologie 26:97–108

    Google Scholar 

  • Chong J, Gruenke J, Dueck R, Mayert W, Woods S (2008) Virulence of oat crown rust [Puccinia coronata f. sp avenae] in Canada during 2002-2006. Can J Plant Pathol 30:115–123

    CAS  Google Scholar 

  • Clark TL, Puttler B, Bailey WC (2006) Is horsenettle, Solanum carolinense L. (Solanaceae), an alternate host for soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae)? J Kans Entomol Soc 79:380–383

    Google Scholar 

  • Colunga-Garcia M, Gage SH (1998) Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera : Coccinellidae) in a Michigan landscape. Environ Entomol 27:1574–1580

    Google Scholar 

  • Converse CK (1984) Element Stewardship Abstract for Rhamnus cathartica, Rhamnus frangula (Syn. Frangula alnus). The Nature Conservancy, Arlington, p 14

    Google Scholar 

  • Costamagna AC, Landis DA (2006) Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecol Appl 16:1619–1628

    PubMed  Google Scholar 

  • Costamagna AC, Landis DA, Difonzo CD (2007) Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans. Ecol Appl 17:441–451

    PubMed  Google Scholar 

  • Costamagna AC, Landis DA, Brewer MJ (2008) The role of natural enemy guilds in Aphis glycines suppression. Biol Control 45:368–379

    Google Scholar 

  • Day WH, Prokrym DR, Ellis DR, Chianese RJ (1994) The known distribution of the predator Propylea quattuordecimpunctata (Coleoptera, Coccinellidae) in the United-States, and thoughts on the origin of this species and 5 other exotic lady beetles in eastern North America. Entomol News 105:244–256

    Google Scholar 

  • Delanoy L, Archibold OW (2007) Efficacy of control measures for European buckthorn (Rhamnus cathartica l.) in Saskatchewan. Environ Manag 40:709–718

    Google Scholar 

  • Desneux N, Barta RJ, Delebeque CJ, Heimpel GE (2009a) Transient host paralysis as a means of reducing self-superparasitism in koinobiont endoparasitoids. J Insect Physiol 55:321–327

    PubMed  CAS  Google Scholar 

  • Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE (2009b) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160:387–398

    PubMed  Google Scholar 

  • Desneux N, Stary P, Delebeque CJ, Gariepy TD, Barta RJ, Hoelmer KA, Heimpel GE (2009c) Cryptic species of parasitoids attacking the soybean aphid (Hemiptera: Aphididae) in Asia: Binodoxys communis and Binodoxys koreanus (Hymenoptera: Braconidae: Aphidiinae). Ann Entomol Soc Am 102:925–936

    Google Scholar 

  • Donaldson JR, Myers SW, Gratton C (2007) Density-dependent responses of soybean aphid (Aphis glycines Matsumura) populations to generalist predators in mid to late season soybean fields. Biol Control 43:111–118

    Google Scholar 

  • Fan YQ, Liebman M, Groden E, Alford AR (1993) Abundance of carabid beetles and other ground-dwelling arthropods in conventional versus low-input bean cropping systems. Agri Ecosyst Environ 43:127–139

    Google Scholar 

  • Feng M, Chen C, Shang S, Ying S, Shen Z, Chen X (2007) Aphid dispersal flight disseminates fungal pathogens and parasitoids as natural control agents of aphids. Ecol Entomol 32:97–104

    Google Scholar 

  • Fox TB, Landis DA, Cardoso FF, Difonzo CD (2004) Predators suppress Aphis glycines Matsumura population growth in soybean. Environ Entomol 33:608–618

    Google Scholar 

  • Frelich LE, Hale CM, Scheu S, Holdsworth AR, Heneghan L, Bohlen PJ, Reich PB (2006) Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol Invasions 8:1235–1245

    Google Scholar 

  • Gao J-F (1994) Biological characteristics and control effect of Lysiphlebia japonica [Hym.: Braconidae] on Aphis glycines [Hom.: Aphididae]. Chin J Biol Control 10:91–92 in Chinese

    Google Scholar 

  • Gardiner MM, Landis DA, Gratton C, Difonzo CD, O’Neal ME, Chacon J, Wayo M, Schmidt N, Mueller EE, Heimpel GE (2009a) Landscape diversity enhances biological control of an introduced crop pest in the North-Central USA. Ecol Appl 19:143–154

    PubMed  CAS  Google Scholar 

  • Gardiner MM, Landis DA, Gratton C, Schmidt N, O’Neal M, Mueller E, Chacon J, Heimpel GE, DiFonzo CD (2009b) Landscape composition mediates coccinellid community structure. Divers Distrib 15:554–564

    Google Scholar 

  • Gassmann A, Tosevski I, Skinner L (2008) Use of native range surveys to determine the potential host range of arthropod herbivores for biological control of two related weed species, Rhamnus cathartica and Frangula alnus. Biol Control 45:11–20

    Google Scholar 

  • Godwin H (1936) Studies in the ecology of wicken fen III. The establishment and development of fen scrub (Carr). J Ecol 24:82–116

    Google Scholar 

  • Godwin H (1943) Rhamnaceae. J Ecol 31:66–92

    Google Scholar 

  • Goetz DW (2008) Harmonia axyridis ladybug invasion and allergy. Allergy Asthma Proc 29:123–129

    PubMed  Google Scholar 

  • Gordon RD (1985) North American Coccinellidae. J N Y Entomol Soc 93:696–703

    Google Scholar 

  • Groth JV, Roelfs AP (1982) Effect of sexual and asexual reproduction on race abundance in cereal rust fungus populations. Phytopathology 72:1503–1507

    Google Scholar 

  • Hajek AE, Hannam JJ, Nielsen C, Bell AJ, Liebherr JK (2007) Distribution and abundance of Carabidae (Coleoptera) associated with soybean aphid (Hemiptera: Aphididae) populations in central New York. Ann Entomol Soc Am 100:876–886

    Google Scholar 

  • Hale CM, Frelich LE, Reich PB (2005) Exotic European earthworm invasion dynamics in northern hardwood forests of Minnesota, USA. Ecol Appl 15:848–860

    Google Scholar 

  • Hale CM, Frelich LE, Reich PB (2006) Changes in hardwood forest understory plant communities in response to European earthworm invasions. Ecology 87:1637–1649

    PubMed  Google Scholar 

  • Hannam JJ, Liebherr JK, Hajek AE (2008) Climbing behaviour and aphid predation by Agonum muelleri (Coleoptera: Carabidae). Can Entomol 140:203–207

    Google Scholar 

  • Harmon JP, Stephens E, Losey J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. J Insect Conserv 11:85–94

    Google Scholar 

  • Heimpel GE, Lee JC, Wu Z, Weiser L, Wackers F, Jervis MA (2004a) Gut sugar analysis in field-caught parasitoids: adapting methods originally developed for biting flies. Int J Pest Manag 50:193–198

    CAS  Google Scholar 

  • Heimpel GE, Ragsdale DW, Venette R, Hopper KR, O’Neil RJ, Rutledge CE, Wu Z (2004b) Prospects for importation biological control of the soybean aphid: anticipating potential costs and benefits. Ann Entomol Soc Am 97:249–258

    Google Scholar 

  • Hendrix PF (ed) (1995) Earthworm ecology and biogeography in North America. Lewis Publishers, Boca Raton

    Google Scholar 

  • Heneghen L, Steffen J, Fagen K (2007) Interactions of an introduced shrub and introduced earthworms in an Illinois urban woodland: Impact on leaf litter decomposition. Pedobiologia 50:543–551

    Google Scholar 

  • Heraty JM, Woolley JB, Hopper KR, Hawks DL, Kim JW, Buffington M (2007) Molecular phylogenetics and reproductive incompatibility in a complex of cryptic species of aphid parasitoids. Mol Phylogenet Evol 45:480–493

    PubMed  CAS  Google Scholar 

  • Hoelmer KA, Kirk AA (2005) Selecting arthropod biological control agents against arthropod pests: can the science be improved to decrease the risk of releasing ineffective agents? Biol Control 34:255–264

    Google Scholar 

  • Holdsworth AR, Frelich LE, Reich PB (2007) Effects of earthworm invasion on plant species richness in northern hardwood forests. Conserv Biol 21:997–1008

    PubMed  Google Scholar 

  • Holdsworth AR, Frelich LE, Reich PB (2008) Litter decomposition in earthworm-invaded northern hardwood forests: role of invasion degree and litter chemistry. Ecoscience 15:536–544

    Google Scholar 

  • Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Ann Rev Ecol Syst 25:495–520

    Google Scholar 

  • Hopper KR, Coutinot D, Chen K, Mercadier G, Halbert SE, Kazmer DJ, Miller RH, Pike KS, Tanigoshi LK (1998) Exploration for natural enemies to control Diuraphis noxia in the United States. In: Quissenbery SS, Peairs FB (eds) A response model for an introduced pest—The Russian wheat aphid. Entomological Society of America, Lanham, pp 166–182

    Google Scholar 

  • Hougen-Eitzman D, Karban R (1995) Mechanisms of interspecific competition that result in successful control of Pacific mites following inoculations of Willamette mites on grapevines. Oecologia 103:157–161

    Google Scholar 

  • Howell JA, Blackwell WH (1977) The history of Rhamnus frangula (glossy buckthorn) in the Ohio flora. Castanea 42:111–115

    Google Scholar 

  • Huebner CD (2006) Fire and invasive exotic plant species in eastern oak communities: an assessment of current knowledge. General Technical Report - NRS-P-1. USDA Forest Service, Newtown Square, pp 218–232

  • James SW, Hendrix PF (2004) Invasion of exotic earthworms into North America and other regions. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton, p 441

    Google Scholar 

  • Kaiser ME, Noma T, Brewer MJ, Pike KS, Vockeroth JR, Gaimari SD (2007) Hymenopteran parasitoids and dipteran predators found using soybean aphid after its midwestern United States invasion. Ann Entomol Soc Am 100:196–205

    Google Scholar 

  • Kladivko EJ, Akhouri NM, Weesies G (1997) Earthworm populations and species distributions under no-till and conventional tillage in Indiana and Illinois. Soil Biol Biochem 29:613–615

    CAS  Google Scholar 

  • Knight GS, Kurylo JS, Endress AG, Stewart JR, Reich PB (2007) Ecology and ecosystem impacts of common buckthorn (Rhamnus cathartica): a review. Biol Invasions 9:925–937

    Google Scholar 

  • Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:1–16

    Google Scholar 

  • Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. Biocontrol 53:23–35

    Google Scholar 

  • Koch RL, Hutchison WD, Venette RC, Heimpel GE (2003) Susceptibiligy of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae) to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biol Control 28:265–270

    Google Scholar 

  • Kourtev PS, Huang WZ, Ehrenfeld JG (1999) Differences in earthworm densities and nitrogen dynamics in soil under exotic and native plant species. Biol Invasions 1:237–245

    Google Scholar 

  • Lawrence B, Fisk MC, Fahey TJ, Suarez ER (2003) Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytol 157:145–153

    Google Scholar 

  • Leonard KJ (2003) Regional frequencies of virulence in oat crown rust in the United States from 1990 through 2000. Plant Dis 87:1301–1310

    Google Scholar 

  • Levesque C, Levesque GY (1994) Abundance and seasonal activity of ground beetles (Coleoptera, Carabidae) in a raspberry plantation and adjacent sites in southern Quebec (Canada). J Kans Entomol Soc 67:73–101

    Google Scholar 

  • Lin LA, Ives AR (2003) The effect of parasitoid host-size preference on host population growth rates: an example of Aphidius colemani and Aphis glycines. Ecol Entomol 28:542–550

    Google Scholar 

  • Lindsey AA (1939) Food of the starling in central New York state. Wilson Bull 51:176–182

    Google Scholar 

  • Liu J, Wu K, Hopper KR, Zhao K (2004) Population dynamics of Aphis glycines (Homoptera: Aphididae) and its natural enemies in soybean in Northern China. Ann Entomol Soc Am 97:235–239

    Google Scholar 

  • Madritch MD, Lindroth RL (2009) Removal of invasive shrubs reduces exotic earthworm populations. Biol Invasions 11:663–671

    Google Scholar 

  • Magalhaes LC, Hunt TE, Siegfried BD (2009) Efficacy of neonicotinoid seed treatments to reduce soybean aphid populations under field and controlled conditions in Nebraska. J Econ Entomol 102:187–195

    PubMed  CAS  Google Scholar 

  • McAvoy WA, Bennett KA (2001) The Flora of Delaware: an annotated checklist. Delaware Department of Natural Resources & Environmental Council

  • McCallum BD, Fetch T, Chong J (2007) Cereal rust control in Canada. Aust J Agric Res 58:639–647

    Google Scholar 

  • Miao J, Wu K, Hopper KR, Li G (2007) Population dynamics of Aphis glycines (Homoptera: Aphididae) and impact of natural enemies in northern China. Environ Entomol 36:840–848

    PubMed  Google Scholar 

  • Michel AP, Zhang W, Jung JK, Kang ST, Mian MAR (2009) Population genetic study of Aphis glycines. Environ Entomol 38:1301–1311

    PubMed  Google Scholar 

  • Mignault MP, Roy M, Brodeur J (2006) Soybean aphid predators in Quebec and the suitability of Aphis glycines as prey for three Coccinellidae. Biocontrol 51:89–106

    Google Scholar 

  • Moon RD (1980) Biological control through interspecific competition. Environ Entomol 9:723–728dpf

    Google Scholar 

  • Myers SW, Hogg DB, Wedberg JL (2005) Determining the optimal timing of foliar insecticide applications for control of soybean aphid (Hemiptera : Aphididae) on soybean. J Econ Entomol 98:2006–2012

    PubMed  Google Scholar 

  • Nichols E, Spector S, Louzada J, Larsen T, Amequita S, Favila ME (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474

    Google Scholar 

  • Nielsen C, Hajek AE (2005) Control of invasive soybean aphid, Aphis glycines (Hemiptera: Aphididae), populations by existing natural enemies in New York state, with emphasis on entomopathogenic fungi. Environ Entomol 34:1036–1047

    Google Scholar 

  • Noma T, Brewer MJ (2008) Seasonal abundance of resident parasitoids and predatory flies and corresponding soybean aphid densities, with comments on classical biological control of soybean aphid in the Midwest. J Econ Entomol 101:278–287

    PubMed  Google Scholar 

  • Noma T, Gratton C, Colunga-Garcia M, Brewer MJ, Mueller EE, Wyckhuys KAG, Heimpel GE, O’Neal ME (2010) Relationship of soybean aphid (Hemiptera: Aphididae) to soybean plant nutrients, landscape structure, and natural enemies. Environ Entomol 39:31–41

    PubMed  Google Scholar 

  • Pearce J, Schuurman D, Venier L, McKee J (2002) Carabid assemblage of an urban woodlot in Sault Ste Marie, Canada. Gt Lakes Entomol 35:161–170

    Google Scholar 

  • Pergams ORW, Norton JE (2006) Treating a single stem can kill the whole shrub: a scientific assessment of buckthorn control methods. Nat Areas J 26:300–309

    Google Scholar 

  • Polgár LA, Hardie J (2000) Diapause induction in aphid parasitoids. Entomologia Experimentalis et Applicata 97:21–27

    Google Scholar 

  • Ragsdale DW, Voegtlin DJ, O’Neil RJ (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97:204–208

    Google Scholar 

  • Ragsdale DW, McCornack BP, Venette RC, Potter BD, Macrae IV, Hodgson EW, O’Neal ME, Johnson KD, O’Neil RJ, Difonzo CD, Hunt TE, Glogoza PA, Cullen EM (2007) Economic threshold for soybean aphid (Hemiptera : Aphididae). J Econ Entomol 100:1258–1267

    PubMed  CAS  Google Scholar 

  • Rauwald KS, Ives AR (2001) Biological control in disturbed agricultural systems and the rapid re-establishment of parasitoids. Ecol Appl 11:1224–1234

    Google Scholar 

  • Reinartz JA (1997) Controlling glossy buckthorn (Rhamnus frangula L) with winter herbicide treatments of cut stumps. Nat Areas J 17:38–41

    Google Scholar 

  • Reynolds JW, Linden DR, Hale CM (2002) The earthworms of Minnesota (Oligochaeta: Acanthodrilidae, Lumbricidae and Megascolocidae). Megadrilogica 8:85–100

    Google Scholar 

  • Rhainds M, Yoo HJS, Kindlmann P, Voegtlin D, Castillo D, Rutledge C, Sadof C, Yaninek S, O'Neil RJ (2010) Two-year oscillation cycle in abundance of soybean aphid (Hemiptera: Aphididae) in Indiana. Agric For Entomol (in press)

  • Ricciardi A (2001) Facilitative interactions among aquatic invaders: is an “invasional meltdown” occurring in the Great Lakes? Can J Fish Aquat Sci 58:2513–2525

    Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93

    PubMed  CAS  Google Scholar 

  • Ridley HN (1930) The Dispersal of plants throughout the world. L. Reeve & Co, Ashford

    Google Scholar 

  • Roelfs AP (1989) Epidemiology of the cereal rusts in North America. Can J Plant Pathol 11:86–90

    Google Scholar 

  • Rutledge CE, O’Neil RJ, Fox TB, Landis DA (2004) Soybean aphid predators and their use in integrated pest management. Ann Entomol Soc Am 97:240–248

    Google Scholar 

  • Shearin AF, Reberg-Horton SC, Gallandt ER (2007) Direct effects of tillage on the activity density of ground beetle (Coleoptera : Carabidae) weed seed predators. Environ Entomol 36:1140–1146

    PubMed  CAS  Google Scholar 

  • Shelton AM, Andaloro JT, Hoy CW (1983) Survey of ground-dwelling predaceous and parasitic arthropods in cabbage fields in upstate New York. Environ Entomol 12:1026–1030

    Google Scholar 

  • Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919

    PubMed  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32

    Google Scholar 

  • Simons MD (1985) Crown rust. In: Roelfs AP, Bushnell WR (eds) The cereal rusts, Vol II. Academic Press, Orlando, pp 131–172

    Google Scholar 

  • Simpson SR, Gross CL, Siberbauer LX (2005) Broom and honeybees in Australia: an alien invasion. Plant Biol 7:541–548

    PubMed  CAS  Google Scholar 

  • Stary P, Rakhshani E, Tomanovic Z, Hoelmer K, Kavallieratos NG, Yu J, Wang M, Heimpel GE (2010) A new species of Lysiphlebus Forster 1862 (Hymenoptera: Braconidae: Aphidiinae) attacking soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) from China. J Hymenopt Res 19:184–191

    Google Scholar 

  • Tecco PA, Diaz S, Gurvich DE, Perez-Harguindeguy N, Cabido M, Bertone GA (2007) Facilitation and interference underlying the association between the woody invaders Pyracantha angustifolia and Ligustrum lucidum. Appl Veg Sci 10:211–218

    Google Scholar 

  • USDA (2008) Plants database. http://plants.usda.gov/

  • van den Berg H, Ankasah D, Muhammad A, Rusli R, Widayanto A, Wirasto HB, Yully I (1997) Evaluating the role of predation in population fluctuations of the soybean aphid Aphis glycines in farmer’s fields in Indonesia. J Appl Ecol 34:971–984

    Google Scholar 

  • Venette RC, Ragsdale DW (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Ann Entomol Soc Am 97:219–228

    Google Scholar 

  • Voegtlin DJ, O’Neil RJ, Graves WR, Lagos D, Yoo HJS (2005) Potential winter hosts of soybean aphid. Ann Entomol Soc Am 98:690–693

    Google Scholar 

  • Watermolen DJ, Fojut P (2008) An introduced flatworm, Bipalium adventitium (Tricladida: Terricola), in Wisconsin and its potential impacts. Wisconsin Department of Natural Resources, Madison. Miscellaneous Publication PUB-SS-1041 2008, p 20

  • Welsman JA, Bahlai CA, Sears MK, Schaafsma AW (2007) Decline of soybean aphid (Homoptera: Aphididae) egg populations from autumn to spring on the primary host, Rhamnus cathartica. Environ Entomol 36:541–548

    PubMed  CAS  Google Scholar 

  • Woodruffe-Peackock EA (1918) A fox-covert study. J Ecol 6:110–125

    Google Scholar 

  • Wu Z, Hopper KR, O’Neil RJ, Voegtlin DJ, Prokrym DR, Heimpel GE (2004a) Reproductive compatibility and genetic variation between two strains of Aphelinus albipodus (Hymenoptera: Aphelinidae), a parasitoid of the soybean aphid, Aphis glycines (Homoptera: Aphididae). Biol Control 31:311–319

    CAS  Google Scholar 

  • Wu Z, Schenk-Hamlin D, Zhan W, Ragsdale DW, Heimpel GE (2004b) The soybean aphid in China: a historical perspective. Ann Entomol Soc Am 97:209–218

    Google Scholar 

  • Wyckhuys KAG, Hopper KR, Wu K-M, Straub C, Gratton C, Heimpel GE (2007a) Predicting potential ecological impact of soybean aphid biological control introductions. Biocontrol News Inf 28:30N–34N

    Google Scholar 

  • Wyckhuys KAG, Koch RL, Heimpel GE (2007b) Physical and ant-mediated refuges from parasitism: implications for non-target effects in biological control. Biol Control 40:306–313

    Google Scholar 

  • Wyckhuys KAG, Stone L, Desneux N, Hoelmer KA, Hopper KR, Heimpel GE (2008a) Parasitism of the soybean aphid, Aphis glycines, by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance. Bull Entomol Res 98:361–370

    PubMed  CAS  Google Scholar 

  • Wyckhuys KAG, Strange-George JE, Kulhanek CA, Wackers FL, Heimpel GE (2008b) Sugar feeding by the aphid parasitoid Binodoxys communis: how does honeydew compare to other sugar sources? J Insect Physiol 54:481–491

    PubMed  CAS  Google Scholar 

  • Wyckhuys KAG, Koch RL, Kula RR, Heimpel GE (2009) Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America. Biol Invasions 11:857–871

    Google Scholar 

  • Yoo HJS, O’Neil RJ, Voegtlin DJ, Graves WR (2005) Plant suitability of Rhamnaceae for soybean aphid (Homoptera : Aphididae). Ann Entomol Soc Am 98:926–930

    Google Scholar 

  • Zhang Y, Wang L, Wu K, Wyckhuys KAG, Heimpel GE (2008) Flight performance of the soybean aphid, Aphis glycines (Hemiptera: Aphididae) under different temperature and humidity regimens. Environ Entomol 37:301–306

    PubMed  Google Scholar 

  • Zhang Y, Wu K, Wyckhuys KAG, Heimpel GE (2009) Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines. Biol Control 51:475–479

    Google Scholar 

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Acknowledgments

We thank Sarah Gunderson, Simon Lueth and Yanhui Li for help with field experiments, Stuart Gage for sharing his long-term data set on coccinellids at the Kellogg Biological Station LTER site, Mary Gardiner and Jonathan Lundgren for sharing unpublished information, and two anonymous reviewers for suggestions on the manuscript. GEH and SZ were supported in part by a grant from the North Central Soybean Research Council, the Minnesota Soybean Research and Promotion Council and the University of Minnesota Agricultural Experiment Station. LEF was supported in part by the Jonathan and Lois Bishop fund of the Minneapolis Foundation. DAL was supported in part by the USDA National Research Initiative, NSF Long Term Ecological Research Program, MSU Environmental Research Initiative, and the Michigan Agricultural Experiment station. MKA was supported in part by a grant from the USDA North Central Regional IPM Program. The sketches in Fig. 1 were drawn by Julie Martinez with support from the Minnesota Futures program at the University of Minnesota.

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Authors and Affiliations

  1. Department of Entomology, University of Minnesota, 1980 Folwell Ave., St. Paul, MN, 55108, USA

    George E. Heimpel, Zeynep Sezen & Mark K. Asplen

  2. Department of Forest Resources, University of Minnesota, 1530 Cleveland Ave. N., St. Paul, MN, 55108, USA

    Lee E. Frelich

  3. Department of Entomology, Michigan State University, 204 CIPS, East Lansing, MI, 48824, USA

    Douglas A. Landis

  4. United States Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Unit, 501 South Chapel Street, Newark, DE, 19713, USA

    Keith R. Hopper & Kim A. Hoelmer

  5. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, 100094, Beijing, People’s Republic of China

    Kongming Wu

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  1. George E. Heimpel
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Correspondence to George E. Heimpel.

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Heimpel, G.E., Frelich, L.E., Landis, D.A. et al. European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12, 2913–2931 (2010). https://doi.org/10.1007/s10530-010-9736-5

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