Biological Invasions

, Volume 18, Issue 4, pp 1057–1075 | Cite as

Methods and approaches for the management of arthropod border incursions

  • Davina L. Saccaggi
  • Minette Karsten
  • Mark P. Robertson
  • Sabrina Kumschick
  • Michael J. Somers
  • John R. U. Wilson
  • John S. Terblanche
Insect Invasions

Abstract

Biological invasions are increasing and are strongly associated with negative agricultural, economic and ecological impacts. It is increasingly recognized that the primary focus in minimizing biological invasions should be to prevent initial entry of alien species. However, exclusion of terrestrial arthropods such as insects and mites is difficult, in part because of their relatively small size, cryptic habits, broad physiological tolerances and close association with various internationally traded goods. Here we discuss methods, approaches, management and intervention systems used by border biosecurity agencies to prevent entry of inadvertently transported arthropods. We examine the at-border systems that exist for the detection and identification of and response to alien arthropods, and discuss the constraints and challenges present in these systems. We critically review current border biosecurity systems and discuss their relative efficacy. We then discuss additional measures and key areas that could be addressed that may further improve these systems. These include: (1) the application of appropriate sampling strategies; (2) employment of suitable inspection methods adequate to detect small and hidden arthropods; and (3) thorough recording of methods, organisms detected and both negative and positive results of inspections. We emphasize that more research is needed on taxonomy, biology, genetics, distribution, host and disease associations, impacts and pathways of introductions for invasive arthropods. Of critical importance is the compilation of complete and accurate invasive species lists and high-risk species watch-lists. The adoption of these recommendations will contribute to improved biosecurity systems for the exclusion of alien, invasive and pest arthropods.

Keywords

Biosecurity Insects Invasive species Mites Sanitary and phytosanitary (SPS) measures 

References

  1. Arimoto M, Satoh M, Uesugi R, Osakabe M (2013) PCR-RFLP analysis for identification of Tetranychus spider mite species (Acari: Tetranychidae). J Econ Entomol 106:661–668CrossRefPubMedGoogle Scholar
  2. Armstrong KF, Ball SL (2005) DNA barcodes for biosecurity: invasive species identification. Philos Trans R Soc B Biol Sci 360(1462):813–1823CrossRefGoogle Scholar
  3. Bacon SJ, Bacher S, Aebi A (2012) Gaps in border controls are related to quarantine alien insect invasions in Europe. PLoS One 7:e47689CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barr NB, Copeland RS, De Meyer M, Masiga D, Kibogo HG, Billah MK, Osir E, Wharton RA, McPheron BA (2006) Molecular diagnostics of economically important Ceratitis fruit fly species (Diptera: Tephritidae) in Africa using PCR and RFLP analyses. Bull Entomol Res 96:505–521PubMedGoogle Scholar
  5. Beard JJ, Ochoa R, Bauchan GR, Trice MD, Redford AJ, Walters TW, Mitter C (2012) Flat mites of the world edition 2. Identification Technology Program, CPHST, PPQ, APHIS, USDA; Fort Collins, CO. http://idtools.org/id/mites/flatmites/. Accessed 30 Sept 2015
  6. Beard JJ, Ochoa R, Braswell WE, Bauchan GR (2015) Brevipalpus phoenicis (Geijskes) species complex (Acari: Tenuipalpidae)—a closer look. Zootaxa 3944:1–67CrossRefPubMedGoogle Scholar
  7. Boykin LM, Armstrong KF, Kubatko L, De Barro P (2012) Species delimitation and global biosecurity. Evolut Bioinform 8:1–37CrossRefGoogle Scholar
  8. Caley P, Ingram R, De Barro P (2015) Entry of exotic insects into Australia: does border interception count match incursion risk? Biol Invasions 17:1087–1094CrossRefGoogle Scholar
  9. CBD (1992) Convention on Biological Diversity. https://www.cbd.int/. Accessed 10 Sept 2015
  10. CBD (2002) Alien species that threaten ecosystems, habitats or species. In Sixth Conference of the Parties (COP 6), Decision VI/23. The Hague, Netherlands. http://www.cbd.int/decisions/. Accessed 30 Sept 2015
  11. Craemer C, Saccaggi DL (2013) Frequent quarantine interception in South Africa of grapevine Colomerus species (Trombidiformes: Prostigmata: Eriophyidae): taxonomic and distributional ambiguities. Int J Acarol 39:239–243CrossRefGoogle Scholar
  12. Eschen R, Rigaux L, Sukovata L, Vettraino AM, Marzano M, Grégoire J-C (2015a) Phytosanitary inspection of woody plants for planning at European Union entry points: a practical enquiry. Biol Invasions 17:2403–2413CrossRefGoogle Scholar
  13. Eschen R, Roques A, Santini A (2015b) Taxonomic dissimilarity in patterns of interception and establishment of alien arthropods, nematodes and pathogens affecting woody plants in Europe. Divers Distrib 21:36–45CrossRefGoogle Scholar
  14. Essl F, Bacher S, Blackburn TM, Booy O, Brundu G, Brunel S, Cardoso A-C, Eschen R, Gallardo B, Galil B, García-Berthou E, Genovesi P, Groom Q, Harrower C, Hulme PE, Katsanevakis S, Kenis M, Kühn I, Kumschick S, Martinou AF, Nentwig W, O’Flynn C, Pagad S, Pergl J, Pyšek P, Rabitsch W, Richardson DM, Roques A, Roy HE, Scalera R, Schindler S, Seebens H, Vanderhoeven S, Vilà M, Wilson JRU, Zenetos A, Jeschke JM (2015) Crossing frontiers in tackling pathways of biological invasions. Bioscience 65:769–782. doi:10.1093/biosci/biv082 CrossRefGoogle Scholar
  15. FAO (2001) Guidelines for the notification of non-compliance and emergency action. International Standard for Phytosanitary Measures Publication No. 13. FAO, Rome, ItalyGoogle Scholar
  16. FAO (2004) Guidelines for a phytosanitary import regulatory system. International Standard for Phytosanitary Measures Publication No. 20. FAO, Rome, ItalyGoogle Scholar
  17. FAO (2008) Methodologies for sampling of consignments. International Standard for Phytosanitary Measures Publication No. 31. FAO, Rome, ItalyGoogle Scholar
  18. FAO (2011a) Phytosanitary certificates. International Standard for Phytosanitary Measures Publication No. 12. FAO, Rome, ItalyGoogle Scholar
  19. FAO (2011b) International Standards for Phytosanitary Measures. https://www.ippc.int/en/core-activities/standards-setting/ispms/. Accessed 30 Sept 2015
  20. FAO (2013) Glossary of phytosanitary terms. International Standard for Phytosanitary Measures Publication No. 05. FAO, Rome, ItalyGoogle Scholar
  21. Faulkner KT, Robertson MP, Rouget M, Wilson JRU (2014) A simple, rapid methodology for developing invasive species watch lists. Biol Conserv 179:25–32CrossRefGoogle Scholar
  22. Faulkner KT, Spear D, Robertson MP, Rouget M, Wilson JRU (2015) An assessment of the information content of South African alien species databases. Bothalia 45(1):Art. #1103, 11 pagesGoogle Scholar
  23. Flechtmann CHW (2007) Eriophyoid mites and quarantine, pp 291–292. In: Morales-Malacara JB, Behan-Pelletier V, Ueckermann E, Péres TM, Estrada-Venegas EG, Badii M (eds) Acarology XI: proceedings of the international congress, MexicoGoogle Scholar
  24. Fortune AL (2006) Biosecurity at the extreme: pathways and vectors between New Zealand and Scott Base, Antarctica. M.Sc. thesis, pp 90, University of Canterbury, Canterbury, NZGoogle Scholar
  25. Garnas J, Auger-Rozenberg M-A, Roques A, Bertelsmeier C, Wingfield MJ, Saccaggi DL, Roy HE, Slippers B (2016) Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences. Biol Invasions. doi:10.1007/s10530-016-1082-9
  26. Goka K, Okabe K, Takano A (2013) Recent cases of invasive alien mites and ticks in Japan: Why is a regulatory framework needed? Exp Appl Acarol 59:245–261CrossRefPubMedGoogle Scholar
  27. Hauser M (2011) A historic account of the invasion of Drosophila suzukii (Matsumara) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag Sci 67:1352–1357CrossRefPubMedGoogle Scholar
  28. Hong X-Y, Wang D-S, Zhang Z-Q (2006) Distribution and damage of recent invasive eriophyoid mites (Acari: Eriophyoidea) in mainland China. Int J Acarol 32:227–240CrossRefGoogle Scholar
  29. Huang CG, Hsu JC, Haymer DS, Lin GC, Wu WJ (2009) Rapid identification of the Mediterranean fruit fly (Diptera: Tephritidae) by loop-mediated isothermal amplification. J Econ Entomol 102:1239–1246CrossRefPubMedGoogle Scholar
  30. Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18CrossRefGoogle Scholar
  31. Hulme PE, 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 (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414CrossRefGoogle Scholar
  32. IPPC (1997) International Plant Protection Convention. https://www.ippc.int/. Accessed 30 Sept 2015
  33. Jeschke JM, Aparicio LG, Haider S, Heger T, Lortie CJ, Pyšek P, Strayer DL (2012) Taxonomic bias and lack of cross-taxonomic studies in invasion biology. Front Ecol Environ 10:349–350CrossRefGoogle Scholar
  34. Jinbo U, Kato T, Ito M (2011) Current progress in DNA barcoding and future implications for entomology. Entomol Sci 14:107–124CrossRefGoogle Scholar
  35. Kane EC, Ochoa R, Mathurin G, Erbe EF (2005) Raoiella indica Hirst (Acari: Tenuipalpidae): an island-hopping mite pest in the Caribbean. In: Abstracts, ESA meeting, Fort Lauderdale, USAGoogle Scholar
  36. Karsten M, Jansen van Vuuren B, Addison P, Terblanche JS (2015) Deconstructing intercontinental invasion pathway hypotheses of the Mediterranean fruit fly (Ceratitis capitata) using a Bayesian inference approach: are port interceptions and quarantine protocols successfully preventing new invasions? Divers Distrib 21:813–825CrossRefGoogle Scholar
  37. Kenis M, Rabitsch W, Auger-Rozenberg MA, Roques A (2007) How can alien species inventories and interception data help us prevent insect invasions? Bull Entomol Res 97:489–502PubMedGoogle Scholar
  38. Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Péré C, Cock MJ, Settele J, Augustin S, Lopez-Vaamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45CrossRefGoogle Scholar
  39. Kiritani K (2001) Invasive insect pests and plant quarantine in Japan. Ext Bull Food Fertil Center Taipei 498:1–12Google Scholar
  40. Kobelt M, Nentwig W (2008) Alien spider introductions to Europe supported by global trade. Divers Distrib 14:273–280CrossRefGoogle Scholar
  41. Lee JC, Bruck DJ, Curry H, Edwards D, Haviland DR, Van Steenwyk RA, Yorgey BM (2011) The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii. Pest Manag Sci 67:1358–1367CrossRefPubMedGoogle Scholar
  42. Lichtenberg E, Olson LJ, Lawley C (2008) Cataloging life on earth: implications for international trade. University of Maryland, College Park, USAGoogle Scholar
  43. Liebhold AM, Work TT, McCullough DG, Cavey JF (2006) Airline baggage as a pathway for alien insect species invading the United States. Am Entomol 52:48–54CrossRefGoogle Scholar
  44. Liebhold AM, Brockerhoff EG, Garrett JL, Parke JL, Britton KO (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Front Ecol Environ 10:135–143CrossRefGoogle Scholar
  45. Lockwood JL, Cassey P, Blackburn TM (2009) The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Divers Distrib 15:904–910CrossRefGoogle Scholar
  46. Mack RN, Simberloff D, Mark Lonsdale W, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  47. Masaki M (1991) A list of Acarina intercepted in plant quarantine. Res Bull Plant Prot Jpn 27:87–92 (in Japanese) Google Scholar
  48. Masaki M, Kitamura H (2004) A list of intercepted tetranychoid mites (Acari: Tetranychoidea) on imported plants at the plant quarantine of Narita Airport. Res Bull Plant Prot Jpn 40:119–125 (in Japanese) Google Scholar
  49. Maynard GV, Hamilton JG, Grimshaw JF (2004) Quarantine–phytosanitary, sanitary and incursion management: an Australian entomological perspective. Aust J Entomol 43:318–328CrossRefGoogle Scholar
  50. McCullough DG, Work TT, Cavey JF, Liebhold AM, Marshall D (2006) Interceptions of nonindigenous plant pests at US ports of entry and border crossings over a 17-year period. Biol Invasions 8:611–630CrossRefGoogle Scholar
  51. McGeoch MA, Spear D, Kleynhans EJ, Marais E (2012) Uncertainty in invasive alien species listing. Ecol Appl 22:959–971CrossRefPubMedGoogle Scholar
  52. Meyer MKP, Dippenaar-Schoeman AS, Ueckermann EA (1996) Mite pests and their predators on cultivated plants in Southern Africa. Plant Protection Research Institute Handbook No. 6. Department of Agriculture and Fisheries, Pretoria, South AfricaGoogle Scholar
  53. Miller DR, Miller GL, Hodges GS, Davidson JA (2005) Introduced scale insects (Hemiptera: Coccoidea) of the United States and their impact on US Agriculture. Proc Entomol Soc Wash 107:123–158Google Scholar
  54. Miller DR, Rung A, Parikh G, Venable G, Redford AJ, Evans GA, Gill RJ (2014) Scale Insects, Edition 2. USDA APHIS Identification Technology Program (ITP). Fort Collins, CO. http://www.idtools.org/id/scales/. Accessed 30 Sept 2015
  55. Navajas M, Ochoa R (2013) Integrating ecology and genetics to address Acari invasions. Exp Appl Acarol 59:1–10CrossRefPubMedGoogle Scholar
  56. Navia D, Fletchmann CHW (2008) Eriophyoid mites intercepted from plant germplasm in Brazil—addressing questions on new introduction pathways, pp 58. In: Sixth European congress of acarology, abstracts, Montpellier, France. European Association of Acarologists (EURAAC)Google Scholar
  57. Navia D, De Moraes GJ, Flechtmann CHW (2007) Phytophagous mites as invasive alien species: quarantine procedures, pp 307–316. In: Morales-Malacara JB, Behan-Pelletier V, Ueckermann E, Péres TM, Estrada-Venegas EG, Badii M (eds) Acarology XI: proceedings of the international Congress, MexicoGoogle Scholar
  58. Navia D, Ochoa R, Welbourn C, Ferragut F (2010) Adventive eriophyoid mites: a global review of their impact, pathways, prevention and challenges. Exp Appl Acarol 51:225–255CrossRefPubMedGoogle Scholar
  59. Ochoa R, Aguilar H, Vargas C (1994) Phytophagous mites of Central America: An illustrated guide. CATIE, Serie Tecnica, Manual Tecnico No. 6, English edition. CATIEGoogle Scholar
  60. OIE 1924: World Organisation for Animal Health. https;//www.oie.int/. Accessed 30 Sept 2015
  61. Perrings C, Williamson M, Barbier EB, Delfino D, Dalmazzone S, Shogren J, Simmons P, Watkinson A (2002) Biological invasion risks and the public good: an economic perspective. Conserv Ecol 6(1):1, 7Google Scholar
  62. Pieterse W, Muller DL, van Vuuren Jansen (2010) A molecular identification approach for five species of mealybug (Hemiptera: Pseudococcidae) on citrus fruit exported from South Africa. Afr Entomol 18:23–28CrossRefGoogle Scholar
  63. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  64. Pyšek P, Richardson DM, Pergl J, Jarošík V, Sixtová Z, Weber E (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23:237–244CrossRefPubMedGoogle Scholar
  65. Roques A, Auger-Rozenberg MA (2006) Tentative analysis of the interceptions of non-indigenous organisms in Europe during 1995–20041. EPPO Bull 36:490–496CrossRefGoogle Scholar
  66. Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, De Clercq P, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez A, Guillemaud T, Haelewaters D, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Lawson Handley L, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, San Martin G, Martinkova Z, Minnaar I, Nedved O, Orlova-Bienkowskaja MJ, Rabitsch W, Peter Ravn H, Rondoni G, Rorke SL, Ryndevich SK, Saethre M-G, Onofre Soares A, Stals R, Tinsley MC, Vandereycken A, van Wielink P, Viglášová S, Zach P, Zaviezo T, Zhao Z (2016) The harlequin ladybird, Harmonia axyridis: an inspiration for global collaborations on invasion biology. Biol Invasions. doi:10.1007/s10530-016-1077-6
  67. Saccaggi DL, Pieterse W (2013) Intercepting aliens: insects and mites on budwood imported to South Africa. J Econ Entomol 106:1179–1189CrossRefPubMedGoogle Scholar
  68. Saccaggi DL, Krüger K, Pietersen G (2008) A multiplex PCR assay for the simultaneous identification of three mealybug species (Hemiptera: Pseudococcidae). Bull Entomol Res 98:27–33PubMedGoogle Scholar
  69. Simberloff D (2006) Risk assessments, blacklists, and white lists for introduced species: are predictions good enough to be useful? Agric Res Econ Rev 35:1–10CrossRefGoogle Scholar
  70. Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66CrossRefPubMedGoogle Scholar
  71. Sujay YH, Sattagi HN, Patil RK (2010) Invasive alien insects and their impact on agroecosystem. Karnataka J Agric Sci 23:26–34Google Scholar
  72. Surkov IV, Oude Lansink AGJM, Van Kooten O, Van Der Werf W (2008a) A model of optimal import phytosanitary inspection under capacity constraint. Agric Econ 38:363–373CrossRefGoogle Scholar
  73. Surkov IV, Van der Werf W, Van Kooten O, Oude Lansink AGJM (2008b) Modeling the rejection probability in plant imports. Phytopathology 98:728–735CrossRefPubMedGoogle Scholar
  74. USDA (2012) The 2012 prioritized offshore pest list. United States Department of Agriculture, WashingtonGoogle Scholar
  75. Venette RC, Moon RD, Hutchison WD (2002) Strategies and statistics of sampling for rare individuals. Annu Rev Entomol 4:143–174CrossRefGoogle Scholar
  76. Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee J, Bruck DJ, Walton VM, O’Neal SD, Zalom FG (2011) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:G1–G7CrossRefGoogle Scholar
  77. Walter DE (2006) Invasive mite identification: tools for quarantine and plant protection, Lucid v. 3.3, Colorado State University, Ft. Collins, CO and USDA/APHIS/PPQ Center for Plant Health Science and Technology, Raleigh, NC. http://www.lucidcentral.org/keys/v3/mites/. Accessed 30 Sept 2015
  78. Wingfield MJ, Garnas, JR, Hajek A, Slippers B, Hurley BP, De Beer, Z, Taerum, SJ (2016) Tree pathogens as drivers of insect invasions. Biol Invasions. doi:10.1007/s10530-016-1084-7
  79. Work TT, McCullough DG, Cavey JF, Komsa R (2005) Arrival rate of nonindigenous insect species into the United States through foreign trade. Biol Invasions 7:323–332CrossRefGoogle Scholar
  80. WTO (1994) The WTO Agreement on the application of sanitary and phytosanitary measures. https://www.wto.org/english/tratop_e/sps_e/spsagr_e.htm. Accessed 30 Sept 2015

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Davina L. Saccaggi
    • 1
    • 2
  • Minette Karsten
    • 2
  • Mark P. Robertson
    • 3
  • Sabrina Kumschick
    • 4
    • 5
  • Michael J. Somers
    • 6
  • John R. U. Wilson
    • 4
    • 5
  • John S. Terblanche
    • 2
  1. 1.Plant Health Diagnostic ServicesDepartment of Agriculture, Forestry and Fisheries (DAFF)StellenboschSouth Africa
  2. 2.Centre for Invasion Biology, Department of Conservation Ecology and Entomology, Faculty of AgriSciencesStellenbosch UniversityStellenboschSouth Africa
  3. 3.Centre for Invasion Biology, Department of Zoology and EntomologyUniversity of PretoriaPretoriaSouth Africa
  4. 4.Centre for Invasion Biology, Department of Botany and ZoologyStellenbosch UniversityStellenboschSouth Africa
  5. 5.Invasive Species ProgrammeSouth African National Biodiversity Institute, Kirstenbosch Research CentreClaremontSouth Africa
  6. 6.Centre for Invasion Biology, Centre for Wildlife ManagementUniversity of PretoriaPretoriaSouth Africa

Personalised recommendations