Skip to main content

Advertisement

SpringerLink
Log in

Testing for multiple invasion routes and source populations for the invasive brown treesnake (Boiga irregularis) on Guam: implications for pest management

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

Abstract

The brown treesnake (Boiga irregularis) population on the Pacific island of Guam has reached iconic status as one of the most destructive invasive species of modern times, yet no published works have used genetic data to identify a source population. We used DNA sequence data from multiple genetic markers and coalescent-based phylogenetic methods to place the Guam population within the broader phylogeographic context of B. irregularis across its native range and tested whether patterns of genetic variation on the island are consistent with one or multiple introductions from different source populations. We also modeled a series of demographic scenarios that differed in the effective size and duration of a population bottleneck immediately following the invasion on Guam, and measured the fit of these simulations to the observed data using approximate Bayesian computation. Our results exclude the possibility of serial introductions from different source populations, and instead verify a single origin from the Admiralty Archipelago off the north coast of Papua New Guinea. This finding is consistent with the hypothesis that B. irregularis was accidentally transported to Guam during military relocation efforts at the end of World War II. Demographic model comparisons suggest that multiple snakes were transported to Guam from the source locality, but that fewer than 10 individuals could be responsible for establishing the population. Our results also provide evidence that low genetic diversity stemming from the founder event has not been a hindrance to the ecological success of B. irregularis on Guam, and at the same time offers a unique ‘genetic opening’ to manage snake density using classical biological approaches.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altizer S, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol 18:589–596

    Article  Google Scholar 

  • Auger-Rozenberg MA, Boivin T, Magnoux E, Courtin C, Roques A, Kerdelhué C (2012) Inferences on population history of a seed chalcid wasp: invasion success despite a severe founder effect from an unexpected source population. Mol Ecol 21:6086–6103

    Article  PubMed  Google Scholar 

  • Austin CC, Rittmeyer EN, Oliver LA, Andermann JO, Zug GR, Rodda GH, Jackson ND (2011) The bioinvasion of Guam: inferring geographic origin, pace, pattern and process of an invasive lizard (Carlia) in the Pacific using multi-locus genomic data. Biol Invasions 13:1951–1967

    Article  Google Scholar 

  • Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035

    PubMed Central  PubMed  Google Scholar 

  • Boissin E, Hurley B, Wingfield MJ, Vasaitis R, Stenlid J, Davis C, de Groot P, Ahumada R, Carnegie A, Goldarazena A, Klasmer P, Wermelinger B, Slippers B (2012) Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp. Mol Ecol 21:5728–5744

    Article  CAS  PubMed  Google Scholar 

  • Cabrera-Pérez MÁ, Gallo-Barneto R, Esteve I, Patiño-Martínez C, López-Jurado LF (2012) The management and control of the California kingsnake in Gran Canaria (Canary Islands): project LIFE+ Lampropeltis. Aliens: the invasive species. Bulletin 32:20–28

    Google Scholar 

  • Campbell EWI (1999) An integrated management plan for the brown treesnake (Boiga irregularis) on Pacific Islands. In: Rodda GH, Sawai Y, Chiszar D, Tanaka H (eds) Problem snake management: the habu and the brown treesnake. Cornell University Press, Ithaca

    Google Scholar 

  • Caudell JN, Conover MR, Whittier J (2002a) Predation of brown tree snakes (Boiga irregularis) in Australia. Int Biodeterior Biodegrad 49:107–111

    Article  Google Scholar 

  • Caudell JN, Whittier J, Conover MR (2002b) The effects of haemogregarine-like parasites on brown tree snakes (Boiga irregularis) and slatey-grey snakes (Stegonotus cucullatus) in Queensland, Australia. Int Biodeterior Biodegrad 49:113–119

    Article  Google Scholar 

  • Clark L, Savarie PJ (2012) Efficacy of aerial broadcast baiting in reducing brown treesnake numbers. Hum Wildl Interact 6:222–236

    Google Scholar 

  • Clark RW, Marchand MN, Clifford BJ, Stechert R, Stephens S (2011) Decline of an isolated timber rattlesnake (Crotalus horridus) population: interactions between climate change, disease, and loss of genetic diversity. Biol Conserv 144:886–891

    Article  Google Scholar 

  • Cleaveland S, Thirgood S, Laurenson K (1999) Pathogens as allies in island conservation? Trends Ecol Evol 14:83–84

    Article  PubMed  Google Scholar 

  • Colvin BA, Wall MW, Fitzgerald LA, Loope LL (2005) Review of brown treesnake problems and control agents. www.fort.usgs.gov/resources/education/bts/resources/pdf/Colvin2005BrownTreesnakeReviewPanelReport.pdf. Report of observations and recommendations, U. S. Department of Interior, Office of Insular Affairs

  • Cornuet J, Santos F, Beaumont MA, Robert CP, Marin J, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY-ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713–2719

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cornuet J-M, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois Rl, Marin J-M, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics. doi:10.1093/bioinformatics/btt1763

  • Courchamp F, Chapuis J, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383

    Article  PubMed  Google Scholar 

  • de Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecol Lett 8:117–126

    Article  Google Scholar 

  • Dmitriev DA, Rakitov RA (2008) Decoding of superimposed traces produced by direct sequencing of heterozygous indels. PLoS Comput Biol 4:e1000113

    Article  PubMed Central  PubMed  Google Scholar 

  • Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Conserv Biol 2:31–39

    Article  Google Scholar 

  • Dobson AP, Altizer SM (2001) Pathogens and the conservation of island biota: modeling the biological control of invasive brown treesnakes on Guam. Final report: USGS Biological Resources Division, National Wildlife Health Center, pp 66, Cooperative agreement no. 99HQA60024, Maddison, WI

  • Dorcas ME, Willson JD, Reed RN, Snow RW, Rochford MR, Miller MA, Meshaka WE, Andreadis PT, Mazzotti FJ, Romagosa CM, Hart KM (2012) Severe mammal declines coincide with proliferation of invasive Burmese pythons in Everglades National Park. Proc Natl Acad Sci USA 109:2418–2422

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Engeman RM, Linnell MA (1998) Trapping strategies for deterring the spread of brown tree snakes from Guam. Pac Conserv Biol 4:348–353

    Google Scholar 

  • Engeman RM, Vice DS, Rodriguez DV, Gruver KS, Santos WS, Pitzler ME (1998) Effectiveness of the detector dogs used for deterring the dispersal of brown tree snakes. Pac Conserv Biol 4:256–260

    Google Scholar 

  • Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Mol Ecol 2010:4113–4130

    Article  Google Scholar 

  • Facon B, Genton BJ, Skykoff J, Jarne P, Estoup A, David P (2006) A general co-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135

    Article  PubMed  Google Scholar 

  • Fauvergue X, Vercken E, Malausa T, Hufbauer RA (2012) The biology of small, introduced populations, with special reference to biological control. Evol Appl 5:424–443

    Article  PubMed Central  PubMed  Google Scholar 

  • Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu Rev Ecol Syst 29:113–140

    Article  Google Scholar 

  • Fritts TH, Scott Jr NJ (1985) The brown tree snake on Guam: studies of its ecology, control, and threats to other islands. Final Report. U.S. Fish and Wildlife Service, Portland, OR

  • Gailey HA (2004) MacArthur’s victory: the war in New Guinea 1943–1944. Random House, New York

    Google Scholar 

  • Gelman A, Carlin JB, Stern HS, Rubin DB (1995) Bayesian data analysis. Chapman and Hall, London

    Google Scholar 

  • Hediger H (1933) Über die von Herrn Dr. A. Bühler auf der Admiralitäts-Gruppe und eingien benachbarten Inseln gesammelten Reptilien und Amphibien. Verh Naturf Ges Basel 44:1–25

  • Hedrick PW, Gutierrez-Espeleta GA, Lee RN (2001) Founder effect in an island population of bighorn sheep. Mol Ecol 10:851–857

    Article  CAS  PubMed  Google Scholar 

  • Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hufbauer RA, Roderick GK (2005) Microevolution in biological control: mechanisms, patterns, and processes. Biol Control 35:227–239

    Article  Google Scholar 

  • Jakes KA, O’Donoghue PJ, Whittier J (2003) Ultrastructure of Hepatozoon boigae (Mackerras, 1961) nov. comb. from brown tree snakes, Boiga irregularis, from northern Australia. Parasitol Res 90:225–231

    Article  CAS  PubMed  Google Scholar 

  • Kang M, Buckley YM, Lowe AJ (2007) Testing the role of genetic factors across multiple independent invasions of the shrub Scotch broom (Cytisus scoparius). Mol Ecol 16:4664–4673

  • Keller SR, Taylor DR (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11:852–866

    Article  PubMed  Google Scholar 

  • Kolbe JJ, Glor RE, Rodriguez Schettino L, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    Article  CAS  PubMed  Google Scholar 

  • Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis. Springer, New York

    Book  Google Scholar 

  • Lawson Handley LJ, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, Aebi A, Roy HE (2011) Ecological genetics of invasive alien species. Biocontrol 56:409–428

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Lopes JS, Boessenkool S (2010) The use of approximate Bayesian computation in conservation genetics and its application in a case study on yellow-eyed penguins. Conserv Genet 11:421–433

    Article  Google Scholar 

  • Lucek K, Sivasundar A, Seehausen O (2012) Evidence of adaptive evolutionary divergence during biological invasion. PLoS One 7:e49377

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lye GC, Lepais O, Goulson D (2011) Reconstructing demographic events from population genetic data: the introduction of bumblebees to New Zealand. Mol Ecol 20:2888–2900

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Morales MA, Cuarón AD (1999) Boa constrictor, an introduced predator threatening the endemic fauna on Cozumel Island, Mexico. Biodivers Conserv 8:957–963

    Article  Google Scholar 

  • Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Kim KS, Reynaud P, Furlan L, Guillemaud T (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992

    Article  CAS  PubMed  Google Scholar 

  • Nichols DK (2000) Pathogenesis of ophidian paramyxovirus infection in the brown tree snake (Boiga irregularis). Final report submitted to the Office of Insular Affairs, Department of the Interior, p 19

  • Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583

    Article  CAS  PubMed  Google Scholar 

  • O’Brien S, Evermann J (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259

    Article  PubMed  Google Scholar 

  • Ploshnitsa AI, Goltsman ME, Macdonald DW, Kennedy LJ, Sommer S (2012) Impact of historical founder effects and a recent bottleneck on MHC variability in Commander Arctic foxes (Vulpes lagopus). Ecol Evol 2:165–180

    Article  PubMed Central  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Quick JS, Reinert HK, de Cuba ER, Odum RA (2005) Recent occurence and dietary habits of Boa constrictor on Aruba, Dutch West Indies. J Herpetol 39:304–307

    Article  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer

  • Rannala B, Yang Z (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164:1645–1656

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rawlings LH (1995) Phylogeography of the brown tree snake, Boiga irregularis, particularly relating to populations in Guam. B. Sc. Diss. Honours thesis, University of Adelaide, Adelaide, Australia

  • Reed RN, Rodda GH (2009) Giant constrictors: biological and management profiles and an establishment risk assessment for nine large species of Pythons, Anacondas, and the Boa constrictor. U. S. Geological Survey Open-File Report 2009–1202, p 302

  • Reynolds RG, Puente-Rolón AR, Reed RN, Revell LJ (2013) Genetic analysis of a novel invasion of Puerto Rico by an exotic constricting snake. Biol Invasions 15:953–959

    Article  Google Scholar 

  • Richmond JQ, Wood DA, Stanford JW, Fisher RN (2011) An evolutionary approach to the biological management of the invasive brown treesnake on Guam. Department of Defense, Strategic Environmental Research and Development Program: SEED and Limited Scope Final Report (Project No. SI-1733), p 46

  • Rodda GH, Savidge JM (2007) Biology and impacts of Pacific Island invasive species. 2. Boiga irregularis, the brown tree snake (Reptilia: Colubridae). Pac Sci 61:307–324

    Article  Google Scholar 

  • Rodda GH, Fritts TH, Conry PJ (1992) Origin and population growth of the brown tree snake, Boiga irregularis. Pac Sci 46:46–57

    Google Scholar 

  • Rodda GH, McCoid MJ, Fritts TH, Campbell EW (1999) Population trends and limiting factors in Boiga irregularis. In: Rodda GH, Sawai Y, Chiszar D, Tanaka H (eds) Problem snake management: the habu and the brown treesnake. Cornell University Press, Ithaca, pp 236–254

    Google Scholar 

  • Roderick GK, Navajas M (2003) Genes in new environments: genetics and evolution in biological control. Nat Rev Genet 4:889–899

    Article  CAS  PubMed  Google Scholar 

  • Rogers H, Lambers JHR, Miller R, Tewksbury JJ (2012) ‘Natural experiment’ demonstrates top-down control of spiders by birds on a landscape level. PLoS One 7:e43446

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Savarie PJ, Shivik JA, White GC, Hurley JC, Clark L (2001) Use of acetaminophen for large-scale control of brown treesnakes. J Wildl Manag 65:356–365

    Article  Google Scholar 

  • Savidge J (1987) Extinction of an island forest avifauna by an introduced snake. Ecology 68:660–668

    Article  Google Scholar 

  • Savidge JA (1991) Population characteristics of the introduced brown tree snake (Boiga irregularis). Biotropica 23:294–300

    Article  Google Scholar 

  • Sawai Y, Kawamura Y, Araki Y, Tomihara Y (1999) A historical outlook on studies of habu (Trimeresurus flavoviridis) bites in the Amami and Okinawa Islands of Japan. In: Rodda GH, Sawai Y, Chiszar D, Tanaka H (eds) Problem snake management, the habu and the brown treesnake. Cornell University Press, Ithaca

    Google Scholar 

  • Seddon JM, Baverstock PR (1999) Variation on islands: major histocompatibility complex (Mhc) polymorphism in populations of the Australian bush rat. Mol Ecol 8:2071–2079

    Article  CAS  PubMed  Google Scholar 

  • Smith MJ, Cogger H, Tiernan B, Maple D, Boland C, Napier F, Detto T, Smith P (2012) An oceanic island reptile community under threat: the decline of reptiles on Christmas Island, Indian Ocean. Herpetol Conserv Biol 7:206–218

    Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction. Am J Hum Genet 73:1162–1169

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sutton JT, Nakagawa S, Robertson BC, Jamieson IG (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol 20:4408–4420

    Article  PubMed  Google Scholar 

  • Telford SR Jr (1999) The possible use of haemogregarine parasites in biological control of the brown treesnake (Boiga irregularis) and the habu (Trimeresurus flavoviridis). In: Rodda GH, Sawai Y, Chiszar D, Tanaka H (eds) Problem snake management: the habu and the brown treesnake. Cornell University Press, Ithaca

    Google Scholar 

  • Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parasitol Today 15:311–313

    Article  CAS  PubMed  Google Scholar 

  • Tonione MA, Reeder N, Moritz CC (2011) High genetic diversity despite the potential for stepping-stone colonizations in an invasive species of gecko on Moorea, French Polynesia. PLoS One 6:e26874

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vázquez-Domínguez E, Suárez-Atilano M, Booth W, González-Baca C, Cuarón AD (2012) Genetic evidence of a recent successful colonization of introduced species on islands: Boa constrictor imperator on Cozumel Island. Biol Invasions 14:2101–2116

    Article  Google Scholar 

  • Wares JP, Hughes AR, Grosberg RK (2005) Mechanisms that drive evolutionary change: insights from species introductions and invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Whittier J, Macrokanis C, Mason RT (2000) Morphology of the brown tree snake, Boiga irregularis, with a comparison of native and extralimital populations. Aust J Zool 48:357–367

    Article  Google Scholar 

Download references

Acknowledgments

B. Iova (PNG National Museum), D. Charles (Wildlife Conservation Society, Manus Island), A. Allison (Bernice P. Bishop Museum), F. Krauss (USDA/APHIS/Wildlife Services) and C. Austin (Louisiana State Univ.) provided valuable guidance through all stages of our work in Papua New Guinea. We are especially indebted to B. Iova and D. Charles for their field work contributions in Papua New Guinea. We thank J. Robbins (PNG National Research Institute) and B. Wilmot (PNG Department of Environment and Conservation) for assistance with research visas and export permits. We thank residents of Kamiali, Sohoniliu, Mokerang and Pityliu for their field assistance, hospitality, and permission to conduct our research on their land in Papua New Guinea, and the Manus Harbourside Hotel for allowing us to set up a lab in their conference room. G. Rodda, R. Reed and S. Siers provided support for fieldwork on Guam, and B. Lardner and J. Savidge provided helpful insight on Boiga life history on Guam. E. Wostl, S. Schuster, C. Rochester, and C. Brown were instrumental in helping us with field work on Guam. We thank the following people for contributing tissue samples: A. Allison, F. Kraus and K. Imada, (Bernice P. Bishop Museum); G. Rodda (U. S. Geological Survey); P. Couper (Queensland Museum of Natural History); R. Brown (Univ. of Kansas); D. Kizirian (American Museum of Natural History); T. LaDuke (Univ. of Texas, Austin); J. McGuire and C. Spencer (Museum of Vertebrate Zoology); B. Shaffer (Univ. of California, Davis); I. Setiadi and B. Evans (McMaster Univ.); W. Wüster and S. Maddock (Univ. of Wales, Bangor). Funding was provided by the U. S. Department of Defense’s Strategic Environmental Research and Development Program (SERDP) and the U. S. Geological Survey. The use of trade, product or firm names in this publication does not imply endorsement by the U. S. Government.

Author information

Authors and Affiliations

  1. Western Ecological Research Center, U. S. Geological Survey, 4165 Spruance Rd. Suite 200, San Diego, CA, 92101, USA

    Jonathan Q. Richmond, Dustin A. Wood & Robert N. Fisher

  2. U. S. Geological Survey, Guam Field Station, P.O. 8255 MOU-3, Dededo, GU, 96912, USA

    James W. Stanford

Authors
  1. Jonathan Q. Richmond
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dustin A. Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James W. Stanford
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert N. Fisher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan Q. Richmond.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 27 kb)

Supplementary material 2 (DOCX 26 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Richmond, J.Q., Wood, D.A., Stanford, J.W. et al. Testing for multiple invasion routes and source populations for the invasive brown treesnake (Boiga irregularis) on Guam: implications for pest management. Biol Invasions 17, 337–349 (2015). https://doi.org/10.1007/s10530-014-0733-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-014-0733-y

Keywords

Search

Navigation