Biological Invasions

, Volume 18, Issue 4, pp 1077–1088 | Cite as

Intentionally introduced terrestrial invertebrates: patterns, risks, and options for management

  • Sabrina Kumschick
  • Adam Devenish
  • Marc Kenis
  • Wolfgang Rabitsch
  • David M. Richardson
  • John R. U. Wilson
Insect Invasions


Our understanding and management of pathways of alien species introductions has improved significantly in the past few years. However, little attention has been paid in most parts of the world to the risks posed by the intentional introduction of alien terrestrial invertebrates which are not intended for use in biological control. We review the species and pathways involved in this intentional trade, and discuss key factors that mediate different aspects of risk. A total of 20 different intentions for the introduction of terrestrial invertebrates were identified. Uses and trade patterns have changed over time and further changes are likely in the future. In particular, invertebrates used in the pet trade, and as human food and animal feed are likely to increase in relevance. We assess priorities for future research and regulation based on the perceived “risk” of the uses including propagule pressure, security of captivity and ease of regulation. Regarding risk assessment, we examine three options: (a) using an existing generic protocol developed for a broad range of taxa; (b) developing a new protocol, possibly by adapting a protocol developed for other taxa; and (c) adopting the approach applied for biological control, i.e. structured experiments and observations. This review highlights the diversity of uses and associated threats of intentional terrestrial invertebrate introductions. It provides recommendations on how to tackle and prevent related issues and can therefore serve as a guideline for future work. We argue that the most suitable option for risk assessment might depend on the type or organism and the level of knowledge of the organism, as well as the intended use.


Biological invasions Risk assessment Insects Arthropods Prediction Pathways 



The November 2014 workshop on “Drivers, impacts, mechanisms and adaptation in insect invasions” was hosted and co-funded by the DST-NRF Centre of Excellence for Invasion Biology at Stellenbosch University, South Africa. Additional financial support was provided by HortGro, the National Research Foundation of South Africa, Stellenbosch University, and SubTrop. We thank many people for providing helpful insights on pathways, especially David Burg, Marcus Byrne, Antoinette Malan, Margaret Palmer, Sheila Storey, Stefan Foord, Mark Robertson, Cavin Shivambu, Theresa Wossler and Ulrike Bauer. The work was supported by the South African National Department of Environment Affairs through its funding of the South African National Biodiversity Institute’s Invasive Species Programme, the DST-NRF Centre of Excellence for Invasion Biology, the Swiss National Science Foundation, and the National Research Foundation (Grant 85417 to DMR). MK was also supported by the EU FP7 PROTEINSECT project (Grant 312084).


  1. Aguiar AMF, Pombo DA, Gonçalves YM (2014) Identification, rearing, and distribution of stick insects of Madeira Island: an example of raising biodiversity awareness. J Insect Sci 14:1–13CrossRefGoogle Scholar
  2. Australian Government Department of Agriculture, Fisheries and Forestry (2011) Import Risk Analysis Handbook 2011, CanberraGoogle Scholar
  3. Baker GH, Brown G, Butt K, Curry JP, Scullion J (2006) Introduced earthworms in agricultural and reclaimed land: their ecology and influences on soil properties, plant production and other soil biota. Biol Invasions 8:1301–1316CrossRefGoogle Scholar
  4. Belluco S, Losasso C, Maggioletti M, Alonzi C, Ricci A, Paoletti MG (2015) Edible insects: a food security solution or a food safety concern? Anim Front 5(2):25–30Google Scholar
  5. Biosecurity New Zealand (2006) Risk Analysis Procedures Version 1Google Scholar
  6. Blakemore R (1999) Diversity of exotic earthworms in Australia—a status report. In: Ponder W, Lunney D (eds) The other 99%. The conservation and biodiversity of invertebrates. Trans. R. Zool. Soc., New South Wales, pp 182–187Google Scholar
  7. Boppré M, Vane-Wright RI (2012) The butterfly house industry: conservation risks and education opportunities. Conserv Soc 10:285–303CrossRefGoogle Scholar
  8. Capinera JL (1992) Insects in art and religion: The American Southwest. Am Entomol 39:221–230CrossRefGoogle Scholar
  9. Carroll MJ, Anderson BJ, Brereton TM, Knight SJ, Kudrna O, Thomas CD (2009) Climate change and translocations: the potential to re-establish two regionally-extinct butterfly species in Britain. Biol Conserv 142:2114–2121CrossRefGoogle Scholar
  10. Charabidze D, Colard T, Becart A, Hedouin V (2014) Use of larder beetles (Coleoptera: Dermestidae) to deflesh human jaws. Forensic Sci Int 234:162–164CrossRefPubMedGoogle Scholar
  11. Charlton AJ, Dickinson M, Wakefield ME, Fitches E, Kenis M, Han R, Zhu F, Kone N, Grant M, Devic E, Bruggeman G, Prior R, Smith R (2015) Exploring the chemical safety of fly larvae as a source of protein for animal feed. J Insects Food Feed 1:7–16CrossRefGoogle Scholar
  12. Cherniack EP (2010) Bugs as drugs, Part 1: insects. The “new” alternative medicine for the 21st century? Altern Med Rev 15(2):124–135PubMedGoogle Scholar
  13. Cowie RH (2011) Snails and slugs. In: Simberloff D, Rejmanek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley, pp 634–642Google Scholar
  14. Cowie RH, Robinson DG (2003) Pathways of introduction of nonindigenous land and freshwater snails and slugs. In: Ruiz GM, Carlton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington, pp 93–122Google Scholar
  15. Cowie RH, Dillon RT Jr, Robinson DG, Smith JW (2009) Alien non-marine snails and slugs of priority quarantine importance in the United States: a preliminary risk assessment. Am Malacol Bull 27:113–132CrossRefGoogle Scholar
  16. Crosby AW (1986) Ecological imperialism. The biological expansion of Europe, 900-1900. Cambridge University Press, CambridgeGoogle Scholar
  17. D’hondt B, Vanderhoeven S, Roelandt S, Mayer F, Versteirt V, Adriaens T, Ducheyne E, San Martin G, Grégoire JC, Stiers I, Quoilin S, Cigar J, Heughebaert A, Branquart E (2015) Harmonia+ and Pandora+: risk screening tools for potentially invasive plants, animals and their pathogens. Biol Invasions 17:1869–1883Google Scholar
  18. Daehler CC, Virtue JG (2010) Likelihood and consequences: reframing the Australian weed risk assessment to reflect a standard model of risk. Plant Prot Q 25:52–55Google Scholar
  19. Dafni A, Kevan P, Gross CL, Goka K (2010) Bombus terrestris, pollinator, invasive and pest: an assessment of problems associated with its widespread introductions for commercial purposes. J Appl Entomol Zool 45:101–113CrossRefGoogle Scholar
  20. Davis CJ, Buttler GD Jr (1964) Introduced enemies of the Giant African Snail, Achatina fulica Bodwich, in Hawaii (Pulmonata: Achatinidae). Proc Hawaiian Entomol Soc 153:377–390Google Scholar
  21. Denmark HA, Porter JE (1973) Regulation of importation of arthropods into and of their movement within Florida. Fla Entomol 56:347–358CrossRefGoogle Scholar
  22. Dutton LM (1992) Cochineal: a bright red animal dye. Master’s Thesis for Baylor UniversityGoogle Scholar
  23. Edwards CA, Bater JE (1992) The use of earthworms in environmental management. Soil Biol Biochem 24(12):1683–1689CrossRefGoogle Scholar
  24. Edwards GB, Hibbard KL (1999) The Mexican redrump, Brachypelma vagans (Araneae: Theraphosidae), an exotic tarantula established in Florida. Entomol Circular 394:1–2Google Scholar
  25. EPPO (2011) Guidelines on pest risk analysis: decision-support scheme for quarantine pests. EPPOGoogle Scholar
  26. 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 65:769–782CrossRefGoogle Scholar
  27. European Commission (2014) Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Off J European Union 57:35–55Google Scholar
  28. FAO (1996) Code of conduct for the import and release of exotic biological control agents. International Standard of Phytosanitary Measures, 3, 23 pp. Accessed 09 April 2015
  29. FAO (2013) Edible insects: future prospects for food and feed security. Food and Agriculture Organization of the United Nations, Rome Accessed 12 May 2015
  30. Faulkner KT, Robertson MP, Rouget M, Wilson JRU (2015) Understanding and managing the introduction pathways of alien taxa: South Africa as a case study. Biol Invasions. doi: 10.1007/s10530-015-0990-4
  31. GB Non-native species Secretariat (2011) Great Britain non-native species rapid risk assessment (NRRA). GB Non-native species Secretariat. York, UK
  32. Goulson D (2010) Impacts of non-native bumblebees in Western Europe and North America. Appl Entomol Zool 45:7–12CrossRefGoogle Scholar
  33. Haggett D (2013) Breeding insects as feeder food. Mantis Press, East SussexGoogle Scholar
  34. Hajek AE, Hurley BP, Kenis M, Garnas JR, Bush SJ, Wingfield MJ, van Lenteren JC, Cock MJ (2016) Exotic biological control agents: a solution or contribution to arthropod invasions? Biol Invasions. doi: 10.1007/s10530-016-1075-8 Google Scholar
  35. Halloran A, Muenke C, Vantomme P, van Huis A (2014) Insects in the human food chain: global status and opportunities. Food Chain 4:103–118CrossRefGoogle Scholar
  36. Hendrix PF (2006) Biological invasions belowground—earthworms as invasive species. Biol Invasions 8:1201–1204CrossRefGoogle Scholar
  37. 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 the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414CrossRefGoogle Scholar
  38. Hunt EJ, Kuhlmann U, Sheppard A, Qin TK, Barratt BIP, Harrison L, Mason PG, Parker D, Flanders RV, Goolsby J (2008) Review of invertebrate biological control agent regulation in Australia, New Zealand, Canada and the USA: recommendations for a harmonised European system. J Appl Entomol 132:89–123CrossRefGoogle Scholar
  39. Jongema Y (2012) List of edible insects of the world. Wageningen University, Wageningen.
  40. Kadoya T, Washitani I (2010) Predicting the rate of range expansion of an invasive alien bumblebee (Bombus terrestris) using a stochastic spatio-temporal model. Biol Conserv 143:1228–1235CrossRefGoogle Scholar
  41. Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Péré C, Cock MJW, Settele J, Augustin S, Lopez-Vaamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45CrossRefGoogle Scholar
  42. Kenis M, Koné N, Chrysostome CAAM, Devic E, Koko GKD, Clottey VA, Nacambo S, Mensah GA (2014) Insects used for animal feed in West Africa. Entomologia 2:107–114CrossRefGoogle Scholar
  43. Kimberling DN (2004) Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biol Invasions 6:301–318CrossRefGoogle Scholar
  44. Kumschick S, Richardson DM (2013) Species-based risk assessments for biological invasions: advances and challenges. Divers Distrib 19:1095–1105CrossRefGoogle Scholar
  45. Kumschick S, Bacher S, Marková Z, Pergl J, Pyšek P, Vaes-Petignat S, van der Veer G, Vilà M, Nentwig W (2015) Comparing impacts of alien plants and animals using a standard scoring system. J Appl Ecol 52:552–561CrossRefGoogle Scholar
  46. Kumschick S, Blackburn TM, Richardson DM (2016) Managing alien bird species: time to move beyond “100 of the Worst” lists? Bird Conserv Int. doi: 10.1017/S0959270915000167 Google Scholar
  47. Levine JM, D’Antonio CM (2003) Forecasting biological invasions with increasing international trade. Conserv Biol 17:322–326CrossRefGoogle Scholar
  48. Liebhold AM (1989) Etienne Leopold Trouvelot, perpetrator of our problem. Gypsy Moth News 20:8–9Google Scholar
  49. Lockwood JA (2012) Insects as weapons of war, terror, and torture. Ann Rev Entomol 57:205–227CrossRefGoogle Scholar
  50. 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
  51. Loomans AJM, van Lenteren JC (2005) Tools for environmental risk assessment of invertebrate biological control agents: a full and quick scan method. In: Hoddle MS (ed) Second international symposium on biological control of arthropods, Davos, Switzerland, 12–16 September. United States Department of Agriculture, Forest Service, Washington, USA, pp 611–619Google Scholar
  52. Louda SM, Arnet AE, Rand TA, Russell FL (2003) Invasiveness of some biological control insects and adequacy of their ecological risk assessment and regulation. Conserv Biol 17:73–82CrossRefGoogle Scholar
  53. McGeoch MA, Butchart SHM, Spear D, Marais E, Kleynhans EJ, Symes A, Chanson J, Hoffmann M (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108CrossRefGoogle Scholar
  54. McMonigle O (2012) Invertebrates for exhibition: Insects, arachnids, and other invertebrates suitable for display in classrooms, museums, and insect zoos. Coachwhip Pubn, 146 ppGoogle Scholar
  55. McPhee DP, Leadbitter D, Skilleter GA (2002) Swallowing the bait: is recreational fishing in Australia ecologically sustainable? Pacific Conservation Biology 8:40–51Google Scholar
  56. Mead AR (1979) Pulmonates, volume 2B. Economic malacology with particular reference to Achatina fulica. Academic Press, LondonGoogle Scholar
  57. Meyer WM, Hayes KA, Meyer AL (2008) Giant African snail, Achatina fulica, as a snail predator. Am Malacol Bull 24:117–119CrossRefGoogle Scholar
  58. Moritz RFA, Härtel S, Neumann P (2005) Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Ecoscience 12:289–301CrossRefGoogle Scholar
  59. Mumford JD (2012) Science, regulation, and precedent for genetically modified insects. PLoS Negl Trop Dis 6(1):e1504. doi: 10.1371/journal.pntd.0001504 CrossRefPubMedPubMedCentralGoogle Scholar
  60. New TR (2008) Are butterfly releases at weddings a conservation concern or opportunity? J Insect Conserv 12:93–95CrossRefGoogle Scholar
  61. Pheloung PC, Williams PA, Halloy SR (1999) A weed risk assessment model for use as a biosecurity tool evaluating plant introductions. J Environ Manage 57:239–251CrossRefGoogle Scholar
  62. Rabitsch W (2010) Pathways and vectors of alien arthropods in Europe. Chapter 3. In: Roques A et al (eds) Alien terrestrial arthropods of Europe. BioRisk 4(1):27–43Google Scholar
  63. Rabitsch W, Milasowszky N, Nehring S, Wiesner C, Wolter C, Essl F (2013) The times are a changing: temporal shifts in patterns of fish invasions in Central European freshwaters. J Fish Biol 82:17–33CrossRefPubMedGoogle Scholar
  64. Raghua S, Dhileepan K, Scanlan JC (2007) Predicting risk and benefit a priori in biological control of invasive plant species: a systems modelling approach. Ecol Model 208:247–262CrossRefGoogle Scholar
  65. Ramani R, Baboo B, Goswami DN (2007) Lac—an introduction. Indian Lac Research Institute, RanchiGoogle Scholar
  66. Raut SK, Barker GM (2002) Achatina fulica Bowdich and other Achatinidae as pests in tropical agriculture. In: Barker GM (ed) Molluscs as crop pests. CABI, pp 55–114Google Scholar
  67. Richardson DM, Cambray JA, Chapman RA, Dean WRJ, Griffiths CL, Le Maitre DC, Newton DJ, Winstanley TJ (2003) Vectors and pathways of biological invasions in South Africa—past, future and present. In: Ruiz G, Carlton J (eds) Invasive species: vectors and management strategies. Island Press, Washington, pp 292–349Google Scholar
  68. Roy HE, Adriaens T, Isaac NB, Kenis M, San Martin y Gomez G, Onkelinx T, Brown PMJ, Poland R, Ravn HP, Roy DB, Comont R, Grégoire JC, de Biseau JC, Hautier L, Eschen R, Frost R, Zindel R, Van Vlaenderen J, Nedved O, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725Google Scholar
  69. Scalera R (2007) Virtues and shortcomings of EU legal provisions for managing NIS: Rana catesbeiana and Trachemys scripta elegans as case studies. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats. Springer Invading nature series in invasion ecology, Dordrecht, pp 669–678CrossRefGoogle Scholar
  70. Schmid-Hempel R, Eckhardt M, Goulson D, Heinzmann D, Lange C, Plischuk S, Escudero LR, Salathé R, Scriven JJ, Schmid-Hempel P (2013) The invasion of southern South America by imported bumblebees and associated parasites. J Anim Ecol 83:823–837CrossRefGoogle Scholar
  71. Schneider SS, DeGrandi-Hoffman G, Smith DR (2004) The African honey bee: factors contributing to a successful biological invasion. Annu Rev Entomol 49:351–376CrossRefGoogle Scholar
  72. Sheppard AW, van Klinken R, Heard T (2005) Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants. Biol Control 35:215–226CrossRefGoogle Scholar
  73. Shockley M, Dossey AT (2014) Insects for human consumption. In: Morales-Ramos J, Rojas G, Shapiro-Ilan DI (eds) Mass production of beneficial organisms: invertebrates and entomopathogens. Elsevier, Oxford, pp 617–652CrossRefGoogle Scholar
  74. Smith DR, Taylor OR, Brown WM (1989) Neotropical Africanized honey bees have African mitochondrial DNA. Nature 339:213CrossRefPubMedGoogle Scholar
  75. Thiengo SC, Faraco FA, Salgado NC, Cowie RH, Fernandez MA (2007) Rapid spread of an invasive snail in South America: the giant African snail, Achatina fulica, in Brasil. Biol Invasions 9:693–702CrossRefGoogle Scholar
  76. Thomas S (2013) Medicinal use of terrestrial molluscs (slugs and snails) with particular reference to their role in the treatment of wounds and other skin lesions. Accessed 25 April 2015
  77. Tobin PC, Bai BB, Eggen DA, Leonard DS (2012) The ecology, geopolitics, and economics of managing Lymantria dispar in the United States. Int J Pest Manag 58:195–210CrossRefGoogle Scholar
  78. Tyndale-Biscoe M (1996) Australia’s introduced dung beetles: original releases and redistributions. Technical Report - CSIRO Division of Entomology 1996. pp iv + 149Google Scholar
  79. USDA-APHIS (2000) Guidelines for pathway-initiated pest risk assessments, version 5.02. US Department of Agriculture, Animal and Plant Health Inspection Service. Plant Protection and Quarantine, RiverdaleGoogle Scholar
  80. Van Driesche RG, Reardon R (2004) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. United States Department of Agriculture Forest Health Technology Enterprise Team, MorgantownGoogle Scholar
  81. Ward DF, Stanley MC, Toft RJ, Forgie SA, Harris RJ (2008) Assessing the risk of invasive ants: a simple and flexible scorecard approach. Insectes Soc 55:360–363CrossRefGoogle Scholar
  82. Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144CrossRefPubMedGoogle Scholar
  83. Winston RL, Schwarzländer M, Hinz HL, Day MD, Cock MJW, Julien MH (2015) Biological control of weeds: a world catalogue of agents and their target weeds, 5th edn. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown. FHTET-2014-04. 838 pGoogle Scholar
  84. Wittenberg R, Cock MJW (2001) Invasive alien species: a toolkit of best prevention and management practices. CAB International, WallingfordCrossRefGoogle Scholar
  85. 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
  86. Zhou F, Tomberlin JK, Zheng L, Yu Z, Zhang J (2013) Developmental and waste reduction plasticity of three black soldier fly strains (Diptera: Stratiomyidae) raised on different livestock manures. J Med Entomol 50:1224–1230CrossRefPubMedGoogle Scholar
  87. Zimmermann H, Bloem S, Klein H (2004) Biology, history, threat, surveillance and control of the cactus moth, Cactoblastis cactorum. CABI, RomeGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Sabrina Kumschick
    • 1
    • 2
  • Adam Devenish
    • 3
  • Marc Kenis
    • 4
  • Wolfgang Rabitsch
    • 5
  • David M. Richardson
    • 1
  • John R. U. Wilson
    • 1
    • 2
  1. 1.Centre for Invasion Biology, Department of Botany and ZoologyStellenbosch UniversityMatielandSouth Africa
  2. 2.Invasive Species Programme, South African National Biodiversity InstituteKirstenbosch National Botanical GardensClaremontSouth Africa
  3. 3.School of Biological Sciences, Life Sciences BuildingUniversity of BristolBristolUK
  4. 4.CABIDelémontSwitzerland
  5. 5.Environment Agency AustriaViennaAustria

Personalised recommendations