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Biocontrol without borders: the unintended spread of introduced weed biological control agents

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Abstract

An underlying assumption of classical biological control implies that intentionally introduced natural enemies will remain within the boundaries that delineate the program’s area of implementation. A weed biological control program targeting Melaleuca quinquenervia in Florida, USA has resulted in the release and establishment of Oxyops vitiosa and Boreioglycaspis melaleucae. An international survey of M. quinquenervia populations in 13 other states or countries where the insects have not been intentionally introduced was initiated to monitor the long range dispersal of O. vitiosa and B. melaleucae beyond the herbivores’ intended geographic range (Florida). Surveys in 2006 resulted in the discovery of B. melaleucae within the canopies of several M. quinquenervia trees near San Juan, Puerto Rico. In 2007, O. vitiosa was observed on the island of New Providence in the Bahamas but neither herbivore was detected on nearby Grand Bahama or Andros islands. In 2009, B. melaleucae was observed attacking M. quinquenervia trees in Los Angeles, California (USA). The herbivores have not been detected on other surveyed M. quinquenervia populations in Cuba, Jamaica, Texas (USA), Costa Rica, Brazil, Hawaii (USA) or South Africa. There is no evidence to suggest that herbivore colonization of New Providence, Puerto Rico, or California was influenced by linear distance between Florida and the recipient M. quinquenervia stand. While the dispersal pathway(s) remains unknown, biological control agents were detected from 200 to >3500 km from their original release location (Florida) and at locations that have strong links via tourism and trade as indicated by the number of airline flights connecting south Florida with colonized tree populations. Implications of this unintended spread are discussed in relation to permeability of biogeographical barriers and risk assessment of biological control agents.

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References

  • Andreas JE, Schwarzländer M, De Clerck-Floate R (2008) The occurrence and potential relevance of post-release, nontarget attack by Mogulones cruciger, a biocontrol agent for Cynoglossum officinale in Canada. Biol Control 46:304–311

    Article  Google Scholar 

  • Animal and Plant Health Inspection Service-Plant Protection and Quarantine (APHIS-PPQ) (1998) Reviewer’s manual for the technical advisory group for biological control of weeds. PPQ 03/98–01 animal and plant health inspection service (APHIS). U.S. Department of Agriculture, Riverdale

    Google Scholar 

  • Arakelian G (2009) Melaleuca psyllid. Co. Los Angeles, Department of Ag. Com. Weights Measures. http://acwm.co.la.ca.us/pdf/Melalpsyllid.pdf. Accessed 10 Mar 2011

  • Balciunas JK, Burrows DW, Purcell MF (1994) Field and laboratory host ranges of the Australian weevil, Oxyops vitiosa, a potential biological control agent of the paperbark tree, Melaleuca quinquenervia. Biol Control 4:351–360

    Article  Google Scholar 

  • Balentine KM, Pratt PD, Dray FA Jr, Rayamajhi MB, Center TD (2009) Geographic distribution and regional impacts of Oxyops vitiosa (Coleoptera: Curculionidae) and Boreioglycaspis melaleucae (Hemiptera: Psyllidae), biological control agents of the invasive tree Melaleuca quinquenervia. Environ Entomol 38:1145–1154

    Article  PubMed  CAS  Google Scholar 

  • Barratt BIP, Howarth FG, Withers TM, Kean JM, Ridley GS (2010) Progress in risk assessment for classical biological control. Biol Control 52:245–254

    Article  Google Scholar 

  • Boland DJ, Brooker MIH, Chippendale GM, Hall N, Hyland BPM, Johnston RD, Kleinig DA, Turner JD (1987) Forest trees of Australia. Nelson Wadsworth, Melbourne

    Google Scholar 

  • Boughton AJ, Bennett CA, Goolsby JA, Pemberton RW (2009) Laboratory host range testing of Neomusotima conspurcatalis (Lepidoptera: Crambidae), a potential biological control agent of the invasive weed, Old World climbing fern, Lygodium microphyllum (Lygodiaceae). Biocontrol Sci Tech 19:369–390

    Article  Google Scholar 

  • Briese DT (2005) Translating host-specificity test results into the real world: the need to harmonize the yin and yang of current testing procedures. Biol Control 35:208–214

    Google Scholar 

  • Briese DT, Walker A (2002) A new perspective on the selection of test plants for evaluating the host-specificity of weed biological control agents: the case of Deuterocampta quadrijuga, a potential insect control agent of Heliotropium amplexicaule. Biol Control 25:273–287

    Article  Google Scholar 

  • Briese DT, Walker A (2008) Choosing the right plants to test: the host-specificity of Longitarsus sp. (Coleoptera: Chrysomelidae) a potential biological control agent of Heliotropium amplexicaule. Biol Control 44:271–285

    Article  Google Scholar 

  • Browne J, Peck SB (1996) The long-horned beetles of south Florida (Cerambycidae: Coleoptera): biogeography and relations with the Bahama Islands and Cuba. Can J Zool 74:2154–2169

    Article  Google Scholar 

  • Center TD, Van TK, Rayachhetry M, Buckingham GR, Dray FA Jr, Wineriter S, Purcell MF, Pratt PD (2000) Field colonization of the melaleuca snout beetle (Oxyops vitiosa) in south Florida. Biol Control 19:112–123

    Article  Google Scholar 

  • Center TD, Pratt PD, Tipping PW, Rayamajhi MB, Van TK, Wineriter S, Dray FA Jr, Purcell MF (2006) Field colonization, population growth, and dispersal of Boreioglycaspis melaleucae Moore, a biological control agent of the invasive tree Melaleuca quinquenervia. Biol Control 39:363–374

    Article  Google Scholar 

  • Center TD, Pratt PD, Tipping PW, Rayamajhi MB, Van TK, Wineriter S, Dray FA Jr (2007) Initial impacts and field validation of host range for Boreioglycaspis melaleucae Moore (Hemiptera: Psyllidae), a biological control agent of the invasive tree Melaleuca quinquenervia (Cav.) Blake. Environ Entomol 36:569–576

    Article  PubMed  Google Scholar 

  • Crawley MJ (1989) Chance and timing in biological invasions. In: Drake JA, Mooney HA, Castri Fd, Groves RH, Kruger FJ, Rejmanek M, Williamson M (eds) Biological invasions: a global perspective. Wiley, New York, pp 407–423

    Google Scholar 

  • DeBach P (1974) Biological control by natural enemies. Cambridge University Press, London

    Google Scholar 

  • Dobbs TT, Brodel CF (2004) Cargo aircraft as a pathway for the entry of nonindigenous pests into south Florida. Fla Entomol 87:65–78

    Article  Google Scholar 

  • Dodd AP (1940) The biological campaign against prickly pear. Commonwealth Prickly Pear Board, Brisbane

  • Drake VA, Farron RA (1998) The influence of atmospheric structure and motions on insect migration. Ann Rev Entomol 33:183–210

    Article  Google Scholar 

  • Dray FA Jr, Bennett BC, Center TD (2006) Invasion history of Melaleuca quinquenervia (Cav.) S.T. Blake in Florida. Castanea 71:210–225

    Article  Google Scholar 

  • Duguma D, Kring TJ, Wiedenmann RN (2009) Seasonal dynamics of Urophora quadrifasciata on spotted knapweed in the Arkansas Ozarks. Can Entomol 141:70–79

    Article  Google Scholar 

  • Forno W, Heard T (1997) Compiling a plant list for testing the host range of agents. In: Julien M, White G (eds) Biological control of weeds: theory and practical application. Australian Centre for International Agricultural Research, Canberra, pp 71–75

    Google Scholar 

  • Franks SJ, Kral AM, Pratt PD (2006) Herbivory by introduced insects reduces growth and survival of Melaleuca quinquenervia seedlings. Environ Entomol 35:366–372

    Article  Google Scholar 

  • Franks SJ, Pratt PD, Tsutsui ND (2011) The genetic consequences of a demographic bottleneck in an introduced biological control insect. Conserv Genet 12:201–211

    Article  Google Scholar 

  • Goeden RD, Andres LA (1999) Biological control of weeds in terrestrial and aquatic environments. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic Press, San Diego, pp 871–890

    Google Scholar 

  • Julien MH, Griffiths W (1998) Biological control of weeds: a catalog of agents and their target weeds, 4th edn. CABI Publishing CAB International, Wallingford

    Google Scholar 

  • Kiritani K, Yamamura K (2003) Exotic insects and their pathways for invasion. In: Ruiz GM, Carlton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington, pp 44–67

    Google Scholar 

  • Louda SM, Stiling P (2004) The double-edged sword of biological control in conservation and restoration. Conserv Biol 18:50–53

    Article  Google Scholar 

  • Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects–the Achilles’ Heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Ann Rev Entomol 48:365–396

    Article  CAS  Google Scholar 

  • Morath SU, Pratt PD, Silvers CS, Center TD (2006) Herbivory by Boreioglycaspis melaleucae (Hemiptera: Psyllidae) accelerates foliar degradation and abscission in the invasive tree Melaleuca quinquenervia. Environ Entomol 35:1372–1378

    Article  Google Scholar 

  • Muniappan R, Reddy GVP (2003) Fortuitous introduction of two natural enemies of Lantana camara to Chuuk. Proc Hawaiian Entomol Soc 36:123–124

    Google Scholar 

  • Pemberton RW (1995) Cactoblastis cactorum in the United States: An immigrant biological control agent or an introduction of the nursery industry? Am Entomol 41:230–232

    Google Scholar 

  • Pemberton RW (2000) Predictable risk to native plants in weed biolgoical control. Oecologia 125:489–494

    Article  Google Scholar 

  • Petit JN, Hoddle MS, Grandgirard J, Roderick GK, Davies N (2009) Successful spread of a biocontrol agent reveals a biosecurity failure: elucidating long distance invasion pathways for Gonatocerus ashmeadi in French Polynesia. BioControl 54:485–495

    Article  Google Scholar 

  • Pratt PD, Arakelian G (2011) First report of the biological control agent Boreioglycaspis melaleucae (Hemitptera: Psyllidae) in California, USA. Fla Entomol 94:724–725

    Article  Google Scholar 

  • Pratt PD, Slone DH, Rayamajhi MB, Van TK, Center TD (2003) Geographic distribution and dispersal rate of Oxyops vitiosa (Coleoptera: Curculionidae), a biological control agent of the invasive tree Melaleuca quinquenervia in south Florida. Environ Entomol 32:397–406

    Article  Google Scholar 

  • Pratt PD, Rayamajhi MB, Van TK, Center TD, Tipping PW (2005) Herbivory alters resource allocation and compensation in the invasive tree Melaleuca quinquenervia. Ecol Entomol 30:316–326

    Article  Google Scholar 

  • Pratt PD, Rayamajhi MB, Bernier LS, Center TD (2006) Geographic range expansion of Boreioglycaspis melaleucae in Puerto Rico. Fla Entomol 89:529–531

    Article  Google Scholar 

  • Pratt PD, Rayamajhi MB, Center TD (2008) Geographic range expansion of Oxyops vitiosa to the Bahamaian Archipelago. Fla Entomol 91:695–697

    Google Scholar 

  • Pratt PD, Rayamajhi MB, Center TD, Tipping PW, Wheeler GS (2009) The ecological host range of an intentionally introduced herbivore: a comparison of predicted versus actual host use. Biol Control 49:146–153

    Article  Google Scholar 

  • Purcell MF, Balciunas JK (1994) Life history and distribution of the Australian weevil Oxyops vitiosa, a potential biological control agent for Melaleuca quinquenervia. Ann Entomol Soc Am 87:867–873

    Google Scholar 

  • Rayamajhi MB, Purcell MF, Van TK, Center TD, Pratt PD, Buckingham GR (2002) Australian paperbark tree (Melaleuca). In: Driesche RGV, Blossey B, Hoddle MS, Lyon S, Reardon R (eds) Biological control of invasive plants in the Eastern United States. Forest Health Technology Enterprise Team, Morgantown, pp 130–171

    Google Scholar 

  • Rayamajhi MB, Pratt PD, Center TD, Tipping PW, Van TK (2009) Decline in exotic tree density facilitates increased plant diversity: the experience from Melaleuca quinquenervia invaded wetlands. Wet Ecol Manage 17:455–467

    Article  Google Scholar 

  • SAS (1999) The SAS System for Windows, Version 8. SAS Institute Inc., Cary

    Google Scholar 

  • Serbesoff-King K (2003) Melaleuca in Florida: a literature review on the taxonomy, distribution, biology, ecology, economic importance and control measures. J Aquatic Plant Manage 41:98–112

    Google Scholar 

  • Sheppard AW, van Klinken RD, Heard TA (2005) Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants. Biol Control 35:215–226

    Article  Google Scholar 

  • Simberloff D (2009) The role of propagule pressure in biological invasions. Ann Rev Ecol Evol Syst 40:81–102

    Article  Google Scholar 

  • Stiling P (2002) Potential non-target effects of a biological control agent, prickly pear moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), in North America, and possible management actions. Biol Invasions 4:273–281

    Article  Google Scholar 

  • Stiling P, Simberloff D (2000) The frequency and strength of nontarget effects of invertebrate biological control agents of plant pests and weeds. In: Follet PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer Academic, Boston, pp 31–43

    Chapter  Google Scholar 

  • Story JM (1985) First report on the dispersal into Montana of Urophora quadrifasciata (Diptera: Tephritidae), a fly released in Canada for biological control of spotted knapweed and diffuse knapweed. Can Entomol 117:1061–1062

    Article  Google Scholar 

  • Thiers B (2011) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/ih/ Accessed 10 Mar 2011

  • Tipping PW, Martin MR, Pratt PD, Center TD, Rayamajhi MB (2008) Suppression of growth and reproduction of an exotic invasive tree by two introduced insects. Biol Control 44:235–241

    Article  Google Scholar 

  • Turner CE, Center TD, Burrows DW, Buckingham GR (1998) Ecology and management of Melaleuca quinquenervia, an invader of wetlands in Florida. USA Wetl Ecol Manage 5:165–178

    Article  Google Scholar 

  • van Klinken RD, Edwards OR (2002) Is host-specificity of weed biological control agents likely to evolve rapidly following establishment? Ecol Lett 5:590–596

    Article  Google Scholar 

  • van Klinken RD, Heard TA (2000) Estimating fundamental host range: a host-specificity study of a potential biocontrol agent for Prosopis species (Leguminosae). Biocontrol Sci Tech 10:331–342

    Article  Google Scholar 

  • Vassiliou VA, Papadoulis G (2008) First record of Acanthoscelides macrophthalmus (Schaeffer) (Coleoptera: Bruchidae) in Cyprus. Entomol Hellenica 17:52–55

    Google Scholar 

  • Vermeij GJ (2005) Invasion as expectation: a historical fact of life. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, Inc., Sunderland, pp 315–340

    Google Scholar 

  • Wang R (1989) Biological control of weeds in China: a status report. In: Delfosse ES (ed) Proceedings of the VII international symposium on biological control of weeds. Istituto Sperimentale per la Patologia Vegetale, Rome, pp 689–693

    Google Scholar 

  • Wapshere AJ (1974) A strategy for evaluating the safety of organisms for biological weed control. Ann Appl Bio 77:201–211

    Article  Google Scholar 

  • 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 24:136–144

    Article  PubMed  Google Scholar 

  • Wineriter SA, Buckingham GR, Frank JH (2003) Host range of Boreioglycaspis melaleucae Moore (Hemiptera: Psyllidae), a potential biocontrol agent of Melaleuca quinquenervia (Cav.) S.T. Blake (Myrtaceae), under quarantine. Biol Control 27:273–292

    Article  Google Scholar 

  • Work TT, McCullough DG, Cavey JF, Komsa R (2005) Arrival rate of nonindigenous insect species into the United States through foreign trade. Biol Invasions 7:323–332

    Article  Google Scholar 

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Acknowledgments

We thank Roy van Driesche and Mark Hoddle for their invitation to present these data as part of the Biological Control for Nature Conference. We are indebted to various collaborators who located and monitored M. quinquenervia populations worldwide, including Dana Prince in Texas, Gevork Arakelian in California, Lourdes Bernier in Puerto Rico, Amy Ferriter and Melanie Williams in the Bahamas, Dan Clark in Hawaii and Costa Rica, Amy Ferriter and Ramona Oviedo in Cuba, Ernita van Wyk in South Africa, Kurt McLaren in Jamaica, and Greg Wheeler in Brazil. We wish to also thank Keith Bradley for conducting the herbaria search, which was completed as part of the TAME Melaleuca Areawide Program (http://tame.ifas.ufl.edu). Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

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Correspondence to P. D. Pratt.

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Pratt, P.D., Center, T.D. Biocontrol without borders: the unintended spread of introduced weed biological control agents. BioControl 57, 319–329 (2012). https://doi.org/10.1007/s10526-011-9412-4

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