Understanding the socioeconomic drivers of biological invasion informs policy development for curtailing future invasions. While early 20th-century plant trade expansions preceded increased establishments of plant pests in Northern America, increased establishments did not follow accelerating imports later that century. To explore this puzzle, we estimate the historical establishment of plant-feeding Hemiptera in Northern America as a function of historical U.S. imports of live plants from seven world regions. Delays between establishment and discovery are modeled using a previously unused proxy for dynamic discovery effort. By recovering the timing of pest arrivals from their historical discoveries, we disentangle the joint establishment-discovery process. We estimate long delays to discovery, which are partially attributable to the low detectability of less economically important insect species. We estimate that many introduced species remain undiscovered, ranging from around one-fifth for Eurasian regions to two-fifths for Central and South America.

Environmental Science and Policy University of California Davis Davis CA 95616 USA

Forestry and Wood Sciences Czech University of Life Sciences Prague Praha 6 Suchdol Czech Republic

Institute for Agro Environmental Sciences NARO Tsukuba Japan

U S Department of Agriculture Economic Research Service Washington DC 20024 USA

U S Department of Agriculture Forest Service Northern Research Station Morgantown WV 26505 USA

Zobrazit více v PubMed

Hulme P. E., Bacher S., Kenis M., Klotz S., Kühn I., Minchin D., Nentwig W., Olenin S., Panov V., Pergl J., Pyšek P., Roques A., Sol D., Solarz W., Vilà M., Grasping at the routes of biological invasions: A framework for integrating pathways into policy. J. Appl. Ecol. 45, 403–414 (2008).

Perrings C., Dehnen-Schmutz K., Touza J., Williamson M., How to manage biological invasions under globalization. Trends Ecol. Evol. 20, 212–215 (2005). PubMed

Arkolakis C., Costinot A., Rodríguez-Clare A., New trade models, same old gains? Am. Econ. Rev. 102, 94–130 (2012).

Melitz M. J., Redding S. J., Missing gains from trade? Am. Econ. Rev. 104, 317–321 (2014).

Bradshaw C. J., Leroy B., Bellard C., Roiz D., Albert C., Fournier A., Barbet-Massin M., Salles J.-M., Simard F., Courchamp F., Massive yet grossly underestimated global costs of invasive insects. Nat. Commun. 7, 12986 (2016). PubMed PMC

U.S. Fish and Wildlife Service, The cost of invasive species (2012); www.fws.gov/verobeach/PythonPDF/CostofInvasivesFactSheet.pdf.

Liebhold A. M., Brockerhoff E. G., Garrett L. J., Parke J. L., Britton K. O., Live plant imports: The major pathway for forest insect and pathogen invasions of the US. Front. Ecol. Environ. 10, 135–143 (2012).

K. Kiritani, K. Yamamura, Exotic insects and their pathways for invasion, in Invasive Species: Vectors and Management Strategies, G. M. Ruiz, J. T. Carlton, Eds. (Island Press, 2003), pp. 44–67.

A. Roques, W. Rabitsch, J.-Y. Rasplus, C. Lopez-Vaamonde, W. Nentwig, M. Kenis, Handbook of Alien Species in Europe (Springer, 2009), pp. 63–79.

Smith R. M., Baker R. H., Malumphy C. P., Hockland S., Hammon R. P., Ostojá-Starzewski J. C., Collins D. W., Recent non-native invertebrate plant pest establishments in Great Britain: Origins, pathways, and trends. Agric. For. Entomol. 9, 307–326 (2007).

Yamanaka T., Morimoto N., Nishida G. M., Kiritani K., Moriya S., Liebhold A. M., Comparison of insect invasions in North America, Japan and their Islands. Biol. Invasions 17, 3049–3061 (2015).

Levine J. M., D’Antonio C. M., Forecasting biological invasions with increasing international trade. Conserv. Biol. 17, 322–326 (2003).

Meyerson L. A., Mooney H. A., Invasive alien species in an era of globalization. Front. Ecol. Environ. 5, 199–208 (2007).

Lodge D. M., Simonin P. W., Burgiel S. W., Keller R. P., Bossenbroek J. M., Jerde C. L., Kramer A. M., Rutherford E. S., Barnes M. A., Wittmann M. E., Chadderton W. L., Apriesnig J. L., Beletsky D., Cooke R. M., Drake J. M., Egan S. P., Finnoff D. C., Gantz C. A., Grey E. K., Hoff M. H., Howeth J. G., Jensen R. A., Larson E. R., Mandrak N. E., Mason D. M., Martinez F. A., Newcomb T. J., Rothlisberger J. D., Tucker A. J., Warziniack T. W., Zhang H., Risk analysis and bioeconomics of invasive species to inform policy and management. Annu. Rev. Environ. Resour. 41, 453–488 (2016).

Costello C., Springborn M., McAusland C., Solow A., Unintended biological invasions: Does risk vary by trading partner? J. Environ. Econ. Manage. 54, 262–276 (2007).

Liebhold A. M., Brockerhoff E. G., Kimberley M., Depletion of heterogeneous source species pools predicts future invasion rates. J. Appl. Ecol. 54, 1968–1977 (2017).

Leung B., Springborn M. R., Turner J. A., Brockerhoff E. G., Pathway-level risk analysis: The net present value of an invasive species policy in the US. Front. Ecol. Environ. 12, 273–279 (2014).

P. E. Hulme, Biosecurity: The changing face of invasion biology, in Fifty Years of Invasion Ecology, D. M. Richardson, Ed. (Wiley-Blackwell, 2012), pp. 301–314.

P. E. Hulme, The Handbook of Plant Biosecurity (Springer, 2014), pp. 1–25.

Mérel P. R., Carter C. A., A second look at managing import risk from invasive species. J. Environ. Econ. Manage. 56, 286–290 (2008).

Essl F., Dullinger S., Rabitsch W., Hulme P. E., Hülber K., Jarošík V., Kleinbauer I., Krausmann F., Kühn I., Nentwig W., Vilà M., Genovesi P., Gherardi F., Desprez-Loustau M. L., Roques A., Pyšek P., Socioeconomic legacy yields an invasion debt. Proc. Natl. Acad. Sci. U.S.A. 108, 203–207 (2011). PubMed PMC

Springborn M. R., Lindsay A. R., Epanchin-Niell R. S., Harnessing enforcement leverage at the border to minimize biological risk from international live species trade. J. Econ. Behav. Organ. 132, 98–112 (2016).

Waage J., Mumford J. D., Agricultural biosecurity. Philos. Trans. R. Soc. B. Biol. Sci. 363, 863–876 (2008). PubMed PMC

Kawatsu K., Yamanaka T., Patoèka J., Liebhold A. M., Nonlinear time series analysis unravels underlying mechanisms of interspecific synchrony among foliage-feeding forest Lepidoptera species. Popul. Ecol. 62, 5–14 (2020).

Skvarla M. J., Halbert S. E., Foottit R. G., Jensen A. S., Maw E., Miller G. L., An update to the adventive aphids (Hemiptera: Aphidoidea) of America north of Mexico, with notes on intercepted species. Proc. Entomol. Soc. Wash. 119, 90–111 (2017).

Seebens H., Blackburn T. M., Dyer E. E., Genovesi P., Hulme P. E., Jeschke J. M., Pagad S., Pyšek P., van Kleunen M., Winter M., Ansong M., Arianoutsou M., Bacher S., Blasius B., Brockerhoff E. G., Brundu G., Capinha C., Causton C. E., Celesti-Grapow L., Dawson W., Dullinger S., Economo E. P., Fuentes N., Guénard B., Jäger H., Kartesz J., Kenis M., Kühn I., Lenzner B., Liebhold A. M., Mosena A., Moser D., Nentwig W., Nishino M., Pearman D., Pergl J., Rabitsch W., Rojas-Sandoval J., Roques A., Rorke S., Rossinelli S., Roy H. E., Scalera R., Schindler S., Štajerová K., Tokarska-Guzik B., Walker K., Ward D. F., Yamanaka T., Essl F., Global rise in emerging alien species results from increased accessibility of new source pools. Proc. Natl. Acad. Sci. U.S.A. 115, E2264–E2273 (2018). PubMed PMC

G. A. Weber, The Plant Quarantine and Control Administration; Its History, Activities and Organization (The Brookings Institution, 1930).

Liebhold A. M., Griffin R. L., The legacy of Charles Marlatt and efforts to limit plant pest invasions. Bull. Entomol. Soc. Am. 62, 218–227 (2016).

Magarey R. D., Colunga-Garcia M., Fieselmann D. A., Plant biosecurity in the United States: Roles, responsibilities, and information needs. Bioscience 59, 875–884 (2009).

USDA-APHIS, Importation of plants for planting: Establishment of category of plants for planting not authorized for importation pending pest risk analysis (2011); www.regulations.gov/document?D=APHIS-2006-0011-0267.

Lovett G. M., Weiss M., Liebhold A. M., Holmes T. P., Leung B., Lambert K. F., Orwig D. A., Campbell F. T., Rosenthal J., McCullough D. G., Wildova R., Ayres M. P., Canham C. D., Foster D. R., LaDeau S. L., Weldy T., Nonnative forest insects and pathogens in the United States: Impacts and policy options. Ecol. Appl. 26, 1437–1455 (2016). PubMed PMC

Morimoto N., Kiritani K., Yamamura K., Yamanaka T., Finding indications of lag time, saturation and trading inflow in the emergence record of exotic agricultural insect pests in Japan. Appl. Entomol. Zool. 54, 437–450 (2019).

Branco M., Nunes P., Roques A., Fernandes M. R., Orazio C., Jactel H., Urban trees facilitate the establishment of non-native forest insects. NeoBiota 52, 25–46 (2019).

Liebhold A. M., Yamanaka T., Roques A., Augustin S., Chown S. L., Brockerhoff E. G., Pyšek P., Plant diversity drives global patterns of insect invasions. Sci. Rep. 8, 12095 (2018). PubMed PMC

Solow A. R., Costello C. J., Estimating the rate of species introductions from the discovery record. Ecology 85, 1822–1825 (2004).

N. Shigesada, K. Kawasaki, Biological Invasions: Theory and Practice (Oxford Univ. Press, 1997).

Huang C.-Y., Qin J., Follmann D. A., A maximum pseudo-profile likelihood estimator for the Cox model under length-biased sampling. Biometrika 99, 199–210 (2012). PubMed PMC

Foottit R., Maw H., Pike K., Messing R., Aphids (Hemiptera: Aphididae and Adelgidae) of Hawai‘i: Annotated list and key to species of an adventive fauna. Pac. Sci. 66, 1–30 (2012).

Tanaka H., Redescription of Takahashia citricola Kuwana, 1909, and its transfer to the genus Pulvinaria Targioni Tozzetti (Coccoidea, Coccidae). Zookeys , 1–10 (2012). PubMed PMC

Percy D. M., Rung A., Hoddle M. S., An annotated checklist of the psyllids of California (Hemiptera: Psylloidea). Zootaxa 3193, 1 (2012).

S. E. Halbert, Y. Wu, S. D. Eigenbrode, Metopolophium festucae cerealium (Hemiptera: Aphididae), a new addition to the aphid fauna of North America (Center for Systematic Entomology, 2013).

J. H. Frank, M. C. Thomas, Invasive insects (adventive pest insects) in Florida, EDIS 2004 (2004).

Acheampong S., Strong W. B., Schwartz M. D., Higgins R. J., Thurston M. A., Walker E. J., Roberts J., First Canadian records of two invasive seed-feeding bugs, Arocatus melanocephalus (Fabricius, 1798) and Raglius alboacuminatus. J. Entomol. Soc. Br. Columbia 113, 74–78 (2016).

M. Ahmed, D. Miller, First US continental record of Fiorinia phantasma Cockerell & Robinson (Hemiptera: Diaspididae), phantasma scale, potential pest of palms and ornamentals plants. Pest Alert. FDACS-P-01880 (2018).

BEA, Gross domestic product, 4th quarter and year 2020 (advance estimate) (2020); https://bugguide.net/node/view/32329?from=200&comments_per_page=50.

Dowell R. V., Gill R. J., Jeske D. R., Hoddle M. S., Exotic terrestrial macro-invertebrate invaders in California from 1700 to 2015: An analysis of records. Proc. Calif. Acad. Sci. 63, 63–157 (2016).

USDA—FAS, Global agricultural trade system (2017); https://apps.fas.usda.gov/gats/default.aspx.

Goverment of Canada, Statistical overview of the canadian ornamental industry (2018); www.agr.gc.ca/eng/horticulture/horticulture-sector-reports/statistical-overview-of-the-canadian-ornamental-industry-2018/?id=1575470259743#a6.3.

U.S. Secretary of the Treasury, Foreign Commerce and Navigation of the United States (U.S. Government Printing Office, 1854–1966).

Integrated Taxonomic Information System, Database (2015); www.itis.gov/.

Hlasny V., Livingston M., Economic determinants of invasion and discovery of nonindigenous insects. J. Agric. Appl. Econ. 40, 37–52 (2007).

Crooks J. A., Lag times and exotic species: The ecology and management of biological invasions in slow-motion1. Ecosci. 12, 316–329 (2005).

Kotinsky J., The European fir trunk louse, Chermes (Dreyfusia) piceae Ratz. Proc. Entomol. Soc. Wash. 18, 14–16 (1916).

Witter J. A., Amman G. D., Field identification and sex determination of Aphidecta obliterata, an introduced predator of Adelges piceae. Ann. Entomol. Soc. Am. 62, 718–721 (1969).

Balch R. E., Studies on the balsam woolly aphid (Adelges piceae Ratz.) and its effects on balsam fir, Abies balsamea (L.) Mill. Publ. Dep. Agric. Canada 867, 1–76 (1952).

M. B. Stoetzel, B. Onken, R. Reardon, J. Lashomb, in Proceedings: Hemlock Woolly Adelgid in the Eastern United States Symposium (InB, 2002), vol. 12.

Havill N. P., Montgomery M. E., Yu G., Shiyake S., Caccone A., Mitochondrial DNA from hemlock woolly adelgid (Hemiptera: Adelgidae) suggests cryptic speciation and pinpoints the source of the introduction to eastern North America. Ann. Entomol. Soc. Am. 99, 195–203 (2006).

L. P. Newton, F. P. Hain, in Proceedings of the Third Symposium on Hemlock Woolly Adelgid in the Eastern United States (USDA Forest Service, 2005), pp. 1–3.

Ehrlich J., The beech bark disease: A Nectria disease of Fagus, following Cryptococcus fagi(Baer.). Can. J. Res. 10, 593–692 (1934).

Howard L. O., Marlatt G., The San Jose scale. US Dept. Agric. Div. Entomol. Bull. 3, 80 (1896).

L. O. Howard, A History of Applied Entomology (Somewhat Anecdotal), Smithsonian Miscellaneous Collections (Smithsonian Institution, 1930), vol. 84.

A. Hamon, T. Fasulo, Cottony Cushion Scale, Icerya Purchasi Maskell, DPI Entomology (University of Florida, 2005), vol. 352.

W. Ebeling, Subtropical fruit pests, in Subtropical Fruit Pests (University of California, 1959).

McClure M. S., Population dynamics of a pernicious parasite: Density-dependent vitality of red pine scale. Ecology 64, 710–718 (1983).

Berger J. O., Liseo B., Wolpert R. L., Integrated likelihood methods for eliminating nuisance parameters. Stat. Sci. 14, 1 (1999).

Montoya J. A., Díaz-Francés E., Sprott D. A., On a criticism of the profile likelihood function. Stat. Papers 50, 195–202 (2009).

Pathways for accidental biocontrol: The human-mediated dispersal of insect predators and parasitoids

Global proliferation of nonnative plants is a major driver of insect invasions

Historical plant introductions predict current insect invasions