European buckthorn and Asian soybean aphid as components ...

1 ORIGINAL PAPERE uropean buckthorn and Asian soybean aphid ascomponents of an extensive invasional meltdownin north AmericaGeorge E. Heimpel Lee E. Frelich Douglas A. Landis Keith R. Hopper Kim A. Hoelmer Zeynep Sezen Mark K. Asplen Kongming WuReceived: 12 June 2009 / Accepted: 25 September 2009 Springer Science+Business Media 2010 AbstractWe consider the possibility of an extensiveinvasional meltdown occurring in central NorthAmerica involving eleven Eurasian species. Thescenario begins with the potential co-facilitationbetween the European earthwormLumbricus terrestrisand European buckthorn ,Rhamnus cathartica.

2 Onceintroduced, European buckthorn has served as theoverwintering host for two important invasive croppests, oat crown rust,Puccinea coronataand thesoybean aphid ,Aphis glycines. The spread ofR. catharticaitself may have been aided by seeddispersal by the European starling,Sturnus vulgaris,and the presence ofL. terrestrishas likely facilitated theinvasion ofBipalium adventitium, an Asian predatoryflatworm that specializes on earthworms. Beyond this,the soybean aphid is consumed by a number ofintroduced species, including the lady beetleHarmoniaaxyridis, the ground beetleAgonum muelleriand theparasitoidAphelinus certus.

3 We hypothesize that thepresence of soybean aphid increases regional abun-dances of these species. We discuss both the evidencefor this multi-species invasional meltdown scenario andpotential implications of meltdown dynamics for inva-sive species management. The particular managementissues that we discuss are: (1) opportunities formanaging multiple invasive species simultaneously bytargeting facilitator species, and (2) implications ofmeltdown dynamics for biological control introduc-tions against the soybean meltdown Lumbricusterrestris Rhamnus cathartica Aphis glycines Puccinia coronata Harmonia axyridis Sturnusvulgaris Bipalium adventitium Agonum muelleri Aphelinus certus Binodoxys communisIntroductionSimberloff and von Holle (1999) introduced the term invasional meltdown to describe situations in whichG.

4 E. Heimpel (&) Z. Sezen M. K. AsplenDepartment of Entomology, University of Minnesota,1980 Folwell Ave., St. Paul, MN 55108, USAe-mail: E. FrelichDepartment of Forest Resources, University of Minnesota,1530 Cleveland Ave. N., St. Paul, MN 55108, USAD. A. LandisDepartment of Entomology, Michigan State University,204 CIPS, East Lansing, MI 48824, USAK. R. Hopper K. A. HoelmerUnited States Department of Agriculture, AgriculturalResearch Service, Beneficial Insects IntroductionResearch Unit, 501 South Chapel Street, Newark,DE 19713, USAK. WuState Key Laboratory for Biology of Plant Diseasesand Insect Pests, Institute of Plant Protection, ChineseAcademy of Agricultural Sciences, 100094 Beijing,People s Republic of China123 Biol InvasionsDOI a group of nonindigenous species facilitate oneanother s invasion in various ways, increasing thelikelihood of survival and/or of ecological impact.

5 They classified interactions among nonindigenousspecies gleaned from 254 articles published in theecological literature between 1993 and 1997 as either?/?,?/0,?/-or-/-, in which the two interactiondirections apply reciprocally to two species (Abrams1987). Out of 190 interactions between pairs ofintroduced species, 10 were interpreted by Simberloff& von Holle as being reciprocally facilitative (?/?).One-way facilitation (?/-or?/0 interactions) wasfound in 178 of the 190 interactions, with most ofthese being herbivory (?/-), in which an introducedplant facilitated an introduced herbivore.

6 Richardsonet al. (2000) have discussed plant invasions involvingmutualistic interactions with introduced pollinators,seed dispersers, mycorrhizae, or nitrogen-fixing bac-teria, although quantifying the importance of mutu-alisms between alien species was beyond the scope oftheir the initial focus on pairwise speciesinteractions, Simberloff (2006) added that meltdownshould be considered a community-level phenome-non in which the net effect of facilitations would leadto an increasing rate of establishment of introducedspecies and/or an accelerating impact . In this vein,Ricciardi (2001) argued that a series of interrelatedinvasional meltdowns were occurring among intro-duced species in the Great Lakes of north as we will discuss in more detail for our studysystem below, it has been suggested that introducedearthworms facilitate the establishment of introducedplants and other invaders, and in turn that introducedplants facilitate earthworm invasions, leading to thepotential for positive feedback among invaders(Aplet et ; Kourtev et ; Frelichet ).

7 In this contribution we consider a series ofinteractions among invasive species in the north -Central United States that appear to fit the invasionalmeltdown model. The web of interactions that weconsider is pictured in it is centered on theEuropean shrubRhamnus cathartica(common buck-thorn) and the Asian soybean aphid (Aphis glycines)in the sense that these species are involved in themost direct interactions with other species in the interactions that make up the putative extensiveinvasional meltdown can be summarized as follows:(1) The growth and spread ofR. catharticaisfacilitated by the actions of invasive earthworms, inparticular the EuropeanLumbricus terrestris, turn creates favorable conditions forgrowth and reproduction ofL.

8 Terrestris.(2) Native earthworms are not present in thenorthern portion of the central United States, so thatintroduced earthworms such asL. terrestrisfacilitatethe spread of the introduced Asian flatworm,Bipa-lium adventitium, a specialist predator of earthworms.(3)R. catharticais an important overwinteringhost of oat crown rust,Puccinia coronata, and hasenabled the invasion of this plant pathogen. Culti-vated oats,Avena sativa, also facilitated this invasionbecause they are a major host of oat crown rustduring the summer growing season.(4)R. catharticais also an obligate overwinteringhost for the Asian soybean aphid ,Aphis glycines,inthe north -Central United States and thus enabled itsinvasion, as did widespread planting of soybean , theobligate summer host ofA.

9 Glycines.(5) The seeds ofR. catharticaare dispersed by anumber of bird species, including the Europeanstarling,Sturnus vulgaris, so starlings may havecontributed to the spread ofR. catharticawithinNorth America. It is not clear whether feeding improves or decreases starlingfitness.(6) A number of introduced predatory insects feedupon the soybean aphid in north America. Inparticular, populations of the invasive lady beetle,Harmonia axyridis, appear to be benefiting from theintroduction of the soybean aphid . The introducedground beetleAgonum muellerihas also been docu-mented feeding on soybean aphids in the eastern , an Asian parasitoid of soybean aphid ,Aphelinus certus, appears to have been introducedeither at the same time as the aphid or the eleven species involved in this web ofinteractions, two are introduced crop plants (soybeansand oats), three are intentionally introduced speciesthat have become invasive (R.)

10 Cathartica,S. vulgaris,andL. terrestris) and five are accidentally-introducedinvaders (B. adventitium,Aphis glycines,P. coronata,Agonum muelleriandAphelinus certus). The eleventhspecies,H. axyridis, was both intentionally andaccidentally introduced, and it is not clear whichclass of introduction has led to establishment andspread (see below).G. E. Heimpel et begin by considering each interaction in turnto evaluate the evidence for or against meltdowndynamics, focusing in particular on evidence forfacilitation at the population level. Where appropri-ate, we suggest critical tests that could be done tovalidate or disprove the hypothesis of facilitation.