Skip to main content

Advertisement

Log in

Two for one: inadvertent introduction of Euglandina species during failed bio-control efforts in Hawaii

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The introduction of the predatory land snail, Euglandina rosea (Férrusac, 1821) from Florida to Hawaii to control the giant African snail, Lissachatina fulica (Bowdich, 1822) is among the most publicized biological control cases gone awry. Following preliminary genetic analyses that revealed a second, possibly undescribed Euglandina species was probably introduced to Hawaii, we used an integrative systematic approach combining both genetic and morphological assessments to examine the taxonomic status of the snail referred to as E. rosea in Hawaii. Genetic and morphological analyses support the interpretation that two Euglandina species were introduced to and have become established in Hawaii and can be readily distinguished based on morphological differences. This finding has significant ramifications for understanding both historical and contemporary biocontrol as it suggests that: (1) other species may have been inadvertently introduced through bio-control programs, (2) inadequate understanding of the taxonomy of bio-control agents has obscured our ability to effectively study their ecological impacts, and (3) while the US has no comprehensive regulatory framework for importing biological control agents, one is urgently needed. This also has wide-ranging implications for conservation efforts throughout the tropics because Euglandina from Oahu, Hawaii were released on other Hawaiian Islands, New Guinea, Okinawa, Palau Islands, Philippines, India, Bonin Islands and Bermuda for use in biological control programs that led to catastrophic loss of endemic land snail diversity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Auffenburg K, Stange LA (2001) Snails eating snails of Florida (Euglandina rosea (Ferussac 1831) (Gastropoda: Spiraxidae), Rumina decollate (Linnaeus 1758) (Gastropod: Subulinidae), Haplotrema concavum (Say 1821) (Gastropoda: Haplotrematidae), Gulella bicolor (Hutton 1834) (Gastropod: Streptaxidae), Varicella gracillima floridana (Pilsbry 1907) (Gastropoda: Oleacinidae). Florida Cooperative Extension Service, EENY-251

  • Bick CS, Foighil DÓ, Coote T (2016) Differential survival among Tahitian tree snails during a mass extinction event: persistence of the rare and fecund. Oryx 50:169–175

    Google Scholar 

  • Bieler R, Slapcinsky J (2000) A case study for development of an island fauna: recent terrestrial mollusks of Bermuda. Nemouria 44:1–99

    Google Scholar 

  • Bungartz F, Ziemmeck F, Tirado N, Jaramillo P, Herrera H, Jiménez-Uzcátegui G (2012) The neglected majority: biodiversity inventories as an integral part of conservation biology. In: Wolff M, Gardener M (eds) The role of science for conservation. Routledge, Oxon, pp 119–142

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    PubMed  CAS  Google Scholar 

  • Chiba S, Cowie RH (2016) Evolution and extinction of land snails on oceanic islands. Annu Rev Ecol Evol Syst 47:123–141

    Google Scholar 

  • Civeyrel L, Simberloff D (1996) A tale of two snails: is the cure worse than the disease? Biodivers Conserv 5:1231–1252

    Google Scholar 

  • Cook A (1985a) The organization of feeding in the carnivorous snail Euglandina rosea. Malacologia 26:183–189

    Google Scholar 

  • Cook A (1985b) Functional aspects of trail following by the carnivorous snail Euglandina rosea. Malacologia 26:173–181

    Google Scholar 

  • Cook A (1989a) Factors affecting prey choice and feeding technique in the carnivorous snail Euglandina rosea Ferussac. J Molluscan Stud 55:469–477

    Google Scholar 

  • Cook A (1989b) The basis of food choice by the carnivorous snail, Euglandina rosea. Br Counc Crop Prot Monogr 41:367–372

    Google Scholar 

  • Coote T, Loève É (2003) From 61 species to five: endemic tree snails of the Society Islands fall prey to an ill-judged biological control progamme. Oryx 37:91–96

    Google Scholar 

  • Cowie RH (2001a) Can snails ever be effective and safe biocontrol agents? Int J Pest Manage 47:23–40

    Google Scholar 

  • Cowie RH (2001b) Invertebrate invasions on Pacific islands and the replacement of unique native faunas: a synthesis of the land and freshwater snails. Biol Invasions 3:119–136

    Google Scholar 

  • Cowie RH, Evenhuis NL, Christensen CC (1995) Catalog of the native land and freshwater molluscs of the Hawaiian Islands. Backhuys Publishers, Leiden

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    PubMed  PubMed Central  CAS  Google Scholar 

  • Davis CJ, Butler GD (1964) Introduced enemies of the giant African snail Achatina fulica Bowdich, in Hawaii (Pulmonata: Achatinidae). Proc Hawaii Entomol Soc 18:377–389

    Google Scholar 

  • Davis EC, Perez KE, Bennett DJ (2004) Euglandina rosea (Férussac, 1821) is found on the ground and in trees in Florida. Nautilus 118:127–128

    Google Scholar 

  • Davis-Berg EC (2012) The predatory snail Euglandina rosea successfully follows mucous trails of both native and non-native prey snails. Invertebr Biol 131:1–10

    Google Scholar 

  • Davison A, Blackie RL, Scothern GP (2009) DNA barcoding of stylommatophoran land snails: a test of existing sequences. Mol Ecol Resour 9:1092–1101

    PubMed  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797

    PubMed  PubMed Central  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Bio Tech 3:294–299

    CAS  Google Scholar 

  • Garey JR, Krotec M, Nelson DR, Brooks J (1996) Molecular analysis supports a tardigrade-arthropod association. Invertebr Biol 115:79–88

    Google Scholar 

  • Gerlach J (1999) The ecology of western Indian Ocean carnivorous land snails. Phelsuma 7:14–24

    Google Scholar 

  • Granjou C, Mauz I, Barbier M, Breucker P (2014) Making taxonomy environmentally relevant: insights from an all taxa biodiversity inventory. Environ Sci Policy 38:254–262

    Google Scholar 

  • Griffiths O, Cook A, Wells SM (1993) The diet of the introduced carnivorous snail Euglandina rosea in Mauritius and its implications for threatened island gastropod faunas. J Zool 229:79–89

    Google Scholar 

  • Hadfield MG, Miller SE, Carwile AH (1993) The decimation of the endemic Hawai‘ian [sic] tree snails by alien predators. Am Zool 33:610–622

    Google Scholar 

  • Holland BS, Christensen CC, Hayes KA, Cowie RH (2008) Biocontrol in Hawaii: a response to Messing (2007). Proc Hawaii Entomol Soc 40:81–83

    Google Scholar 

  • Holland BS, Chock T, Lee A, Sugiura S (2012) Tracking behavior in the snail Euglandina rosea: first evidence of preference for endemic vs. biocontrol target pest species in Hawaii. Am Malacol Bull 30:153–157

    Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    PubMed  PubMed Central  Google Scholar 

  • Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clark SA, Cummings KS, Frest TJ, Gargominy O, Herbert DG, Hershler R (2004) The global decline of nonmarine mollusks. Bioscience 54:321–330

    Google Scholar 

  • Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution. Front Ecol Environ 4:132–140

    Google Scholar 

  • Meyer WM III, Cowie RH (2010) Feeding preferences of two predatory snails introduced to Hawaii and their conservation ramifications. Malacologia 53:135–144

    Google Scholar 

  • Meyer WM III, Cowie RH (2011) Distribution, movement, and microhabitat use of the introduced predatory snail Euglandina rosea in Hawaii: implications for management. Invertebr Biol 130:325–333

    Google Scholar 

  • Murray J, Murray E, Johnson MS, Clarke B (1988) The extinction of Partula on Moorea. Pac Sci 42:150–153

    Google Scholar 

  • Pilsbry HA (1946) Land Mollusca of North America north of Mexico, vol II, part 1. Academy of Natural Sciences, Philadelphia

    Google Scholar 

  • Régnier C, Fontaine B, Bouchet P (2009) Not knowing, not recording, not listing: numerous unnoticed mollusk extinctions. Conserv Biol 23:1214–1221

    PubMed  Google Scholar 

  • Régnier C, Bouchet P, Hayes KA, Yeung NW, Christensen CC, Chung DJ, Fontaine B, Cowie RH (2015) Extinction in a hyperdiverse endemic Hawaiian land snail family and implications for the underestimation of invertebrate extinction. Conserv Biol 29:1715–1723

    PubMed  Google Scholar 

  • Solem A (1990) How many Hawaiian land snail species are left? And what we can do for them. Bishop Mus Occas Pap 30:27–40

    Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    PubMed  PubMed Central  CAS  Google Scholar 

  • Stone R (1999) Keeping paradise safe for the natives. Science 285:1837

    Google Scholar 

  • Suarez AV, Tsutsui ND (2004) The value of museum collections for research and society. Bioscience 54:66–74

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tewksbury JJ, Anderson JG, Bakker JD, Billo TJ, Dunwiddie PW, Groom MJ, Hampton SE, Herman SG, Levey DJ, Machnicki NJ, Del Rio CM (2014) Natural history’s place in science and society. Bioscience 64:300–310

    Google Scholar 

  • United States Department of Agriculture (USDA) (2015) Biological Control Program. https://www.aphis.usda.gov/wps/portal/aphis/ourfocus/planthealth/sa_domestic_pests_and_diseases/sa_bio_control/!ut/p/a0/04_Sj9CPykssy0xPLMnMz0vMAfGjzOK9_D2MDJ0MjDzd3V2dDDz93HwCzL29jAx8TfULsh0VAY_1WkE!/

  • Wen J, Ickert-Bond SM, Appelhans MS, Dorr LJ, Funk VA (2015) Collections-based systematics: opportunities and outlook for 2050. J Syst Evol 53:477–488

    Google Scholar 

Download references

Acknowledgements

We thank D. Ressler, J. Kim, V. Costello, J. Tanino, B. Holland, S. Joe, T. Skelton, C. Tran, K. Bustamante, D. Gary, K. Leung, D. Robinson, D. Sischo and H. Walden for help in collection and processing of samples. We especially thank R.H. Cowie for lab support and helpful discussions. Funding and support was provided by U.S. Army Environmental, Oahu (WMM), the National Science Foundation (DEB-1120906, KAH) and the Smithsonian Institutes. This is contribution No. 2016–109 to the Hawaii Biological Survey and SOEST no. 9877 of the University of Hawaii’s School of Ocean and Earth Science and Technology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wallace M. Meyer III.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 19 kb)

Supplementary material 2 (PDF 262 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meyer, W.M., Yeung, N.W., Slapcinsky, J. et al. Two for one: inadvertent introduction of Euglandina species during failed bio-control efforts in Hawaii. Biol Invasions 19, 1399–1405 (2017). https://doi.org/10.1007/s10530-016-1354-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1354-4

Keywords

Navigation