Biological Invasions

, Volume 16, Issue 11, pp 2293–2302 | Cite as

Multiple recent introductions of apid bees into Pacific archipelagos signify potentially large consequences for both agriculture and indigenous ecosystems

  • Scott V. C. Groom
  • Hien T. Ngo
  • Sandra M. Rehan
  • Posa Skelton
  • Mark I. Stevens
  • Michael P. Schwarz
Original Paper


The islands of the south west Pacific (SWP) are highly biodiverse, yet records of their bee fauna suggest a region depauperate of a key pollinator suite. Studies of the bees of Fiji based on molecular data have revealed a recent origin with the majority of species having arrived since the last glacial maximum or introduced since human colonization. Here we use DNA barcodes to provide the first detailed account of Apidae bees from Vanuatu, Fiji, and Samoa. We show that most if not all species in these archipelagos have been recently introduced from Australia and south east Asia, with a further species introduced from the New World. Some of these species have become regionally abundant and we discuss the potential impact of introduced pollinators on endemic plant–pollinator associations. Given the wide-reaching role of native pollinators in island systems, yet lack of understanding of SWP pollinator suites, our study highlights the urgent need for more detailed pollinator research in the region.


Apidae Anthropogenic introductions Exotic species Pollinators Fiji Vanuatu Samoa South west Pacific 



We thank Marika Tuiwawa and all members of the South Pacific Regional Herbarium at the University of the South Pacific for their invaluable assistance with Fijian field logistics and expertise. Linette Berukilukilu and Plant Health and Quarantine oversaw remote field collections and facilitated permit acquisition in Vanuatu. Sampling in Samoa would not have been possible without the assistance of Afele Faiilagi and the Ministry of Natural Resources and Environment. Remko Leijs provided valuable assistance in species identification. We thank Laurence Packer and two anonymous reviewers for valuable suggestions on the manuscript. Funding for this research was gratefully received from the Australia Pacific Science Foundation, Rufford Foundation, National Climate Change Adaptation Research Facility, and the Australia Awards Endeavour Research Fellowship Program. An NSERC Discovery Grant awarded to Dr. Laurence Packer funded collection and sequencing of south east Asian specimens.

Supplementary material

10530_2014_664_MOESM1_ESM.eps (2.6 mb)
Bayesian chronogram derived from an uncorrelated log-normal clock with branch lengths proportional to the number of changes. Data was partitioned with the 3rd codon positions separate from the 1st and 2nd, and a GTR + I + Γ model for each partition, ran for 50 million generations sampling every 10,000 generation. Posterior probability values provided above nodes, values <0.1 were removed. Taxa are colour-coded to collecting locality as indicated by shading colour of the map (EPS 2655 kb)
10530_2014_664_MOESM2_ESM.docx (136 kb)
Supplementary material 2 (DOCX 135 kb)
10530_2014_664_MOESM3_ESM.xlsx (109 kb)
Supplementary material 3 (XLSX 108 kb)


  1. Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, Cane J, Cox PA, Dalton V, Feinsinger P, Ingram M, Inouye D, Jones CE, Kennedy K, Kevan P, Koopowitz H, Medellin R, Medellin-Morales S, Nabhan GP, Pavlik B, Tepedino V, Torchio P, Walker S (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12(1):8–17CrossRefGoogle Scholar
  2. Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593CrossRefGoogle Scholar
  3. Batley M, Hogendoorn K (2009) Diversity and conservation status of native Australian bees. Apidologie 40(3):347–354. doi: 10.1051/apido/2009018 CrossRefGoogle Scholar
  4. Cardinal S, Danforth BN (2013) Bees diversified in the age of eudicots. Proc R Soc B Biol Sci 280(1755):2012–2686Google Scholar
  5. Cardinal S, Straka J, Danforth BN (2010) Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism. Proc Natl Acad Sci USA 107(37):16207–16211. doi: 10.1073/pnas.1006299107 PubMedCrossRefPubMedCentralGoogle Scholar
  6. Chenoweth LB, Schwarz MP (2011) Biogeographical origins and diversification of the exoneurine allodapine bees of Australia (Hymenoptera, Apidae). J Biogeogr 38(8):1471–1483CrossRefGoogle Scholar
  7. Cockerell TDA (1924) Bees from the Tonga and Samoa Islands. Ann Entomol Soc Am 17:392–394Google Scholar
  8. Cooper A, Cooper RA (1995) The Oligocene bottleneck and New Zealand biota: genetic record of a past environmental crisis. Proc R Soc Lond Ser B Biol Sci 261(1362):293–302CrossRefGoogle Scholar
  9. 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. Appl Entomol Zool 45(1):101–113CrossRefGoogle Scholar
  10. Davies O, Groom SVC, Ngo HT, Stevens MI, Schwarz MP (2013) Diversity and origins of Fijian leaf-cutter bees (Megachilidae). Pac Sci 67(4):561–570CrossRefGoogle Scholar
  11. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7. doi: 10.1186/1471-2148-7-214
  12. Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2012) Geneious ver. 5.6.4Google Scholar
  13. Engel MS (2001) A monograph of the Baltic amber bees and evolution of the Apoidea (Hymenoptera). Bull Am Mus Nat Hist 259:1–192CrossRefGoogle Scholar
  14. Evenhuis NL (2007) Checklist of Fiji Hymenoptera. Bishop Museum Technical Report 38 (11)Google Scholar
  15. Fullaway DT (1957) Checklist of Hymenoptera of Fiji. Proc Hawaiian Entomol Soc 16:269–280Google Scholar
  16. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LsG, Harder LD, Afik O (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339(6127):1608–1611PubMedCrossRefGoogle Scholar
  17. Gibbs JJ (2009) New species in the Lasioglossum petrellum species group identified through an integrative taxonomic approach. Can Entomol 141(4):371–396CrossRefGoogle Scholar
  18. Gonzalez-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, Steffan-Dewenter I, Szentgyorgyi H, Woyciechowski M, Vila M (2013) Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 28(9):524–530PubMedCrossRefGoogle Scholar
  19. Goulson D (2003) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34:1–26CrossRefGoogle Scholar
  20. Grandcolas P, Murienne J, Robillard T, Desutter-Grandcolas L, Jourdan H, Guilbert E, Deharveng L (2008) New Caledonia: a very old Darwinian island? Philos Trans R Soc B Biol Sci 363(1508):3309–3317. doi: 10.1098/rstb.2008.0122 CrossRefGoogle Scholar
  21. Groom SVC, Schwarz MP (2011) Bees in the Southwest Pacific: origins, diversity and conservation. Apidologie 42(6):759–770. doi: 10.1007/S13592-011-0079-8 CrossRefGoogle Scholar
  22. Groom SVC, Stevens MI, Schwarz MP (2013) Diversification of Fijian halictine bees: insights into a recent island radiation. Mol Phylogenet Evol 68(3):582–594. doi: 10.1016/J.Ympev.04.015 PubMedCrossRefGoogle Scholar
  23. Gross C, Gorrell L, Macdonald M, Fatemi M (2010) Honeybees facilitate the invasion of Phyla canescens (Verbenaceae) in Australia—no bees, no seed! Weed Res 50(4):364–372Google Scholar
  24. Gunn BF, Baudouin L, Olsen KM (2011) Independent origins of cultivated coconut (Cocos nucifera L.) in the old world tropics. PLoS ONE 6(6):e21143PubMedCrossRefPubMedCentralGoogle Scholar
  25. Heads M (2008) Panbiogeography of New Caledonia, south-west Pacific: basal angiosperms on basement terranes, ultramafic endemics inherited from volcanic island arcs and old taxa endemic to young islands. J Biogeogr 35(12):2153–2175. doi: 10.1111/j.1365-2699.2008.01977.x CrossRefGoogle Scholar
  26. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101(41):14812–14817. doi: 10.1073/Pnas.0406166101 PubMedCrossRefPubMedCentralGoogle Scholar
  27. Ivanova NV, Dewaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6(4):998–1002. doi: 10.1111/J.1471-8286.2006.01428.X CrossRefGoogle Scholar
  28. Kato M, Kawakita A (2004) Plant–pollinator interactions in New Caledonia influenced by introduced honey bees. Am J Bot 91(11):1814–1827PubMedCrossRefGoogle Scholar
  29. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant–pollinator interactions. Annu Rev Ecol Syst 29:83–112CrossRefGoogle Scholar
  30. Keppel G, Lowe AJ, Possingham HP (2009) Changing perspectives on the biogeography of the tropical South Pacific: influences of dispersal, vicariance and extinction. J Biogeogr 36(6):1035–1054CrossRefGoogle Scholar
  31. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B Biol Sci 274(1608):303–313. doi: 10.1098/rspb.2006.3721 CrossRefGoogle Scholar
  32. Magnacca KN, Brown MJ (2010) Tissue segregation of mitochondrial haplotypes in heteroplasmic Hawaiian bees: implications for DNA barcoding. Mol Ecol Res 10(1):60–68CrossRefGoogle Scholar
  33. McGlone MS (2005) Goodbye Gondwana. J Biogeogr 32(5):739–740CrossRefGoogle Scholar
  34. Michener CD (1965) A classification of the bees of the Australian and South Pacific Regions. Bull Am Mus Nat Hist 130:1–362Google Scholar
  35. Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  36. Murienne J, Grandcolas P, Piulachs MD, Bellés X, D’Haese C, Legendre F, Pellens R, Guilbert E (2005) Evolution on a shaky piece of Gondwana: is local endemism recent in New Caledonia? Cladistics 21(1):2–7CrossRefGoogle Scholar
  37. Neall VE, Trewick SA (2008) The age and origin of the Pacific islands: a geological overview. Philos Trans R Soc B Biol Sci 363(1508):3293–3308. doi: 10.1098/rstb.2008.0119 CrossRefGoogle Scholar
  38. Pauly A, Munzinger J (2003) Contribution à la connaissance des Hymenoptera Apoidea de Nouvelle-Calédonie et de leurs relations avec la flore butinée. Ann Soc Entomol Fr 39(2):153–166Google Scholar
  39. Pauly A, Villemant C (2009) Hyménoptères Apoidea (Insecta) de l’archipel du Vanuatu. Zoosystema 31(3):719–730CrossRefGoogle Scholar
  40. Perkins RCL, Cheesman LE (1928) Hymenoptera-Apoidea, Sphecoidea, and Vespoidea. Insects of Samoa Part V. (Fasc. 1) 3:1–32Google Scholar
  41. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818PubMedCrossRefGoogle Scholar
  42. Rambaut A, Drummond AJ (2007) Tracer v.1.5.
  43. Ratnasingham S, Hebert PDN (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8(7):e66213. doi: 10.1371/journal.pone.0066213 PubMedCrossRefPubMedCentralGoogle Scholar
  44. Rehan SM, Chapman TW, Craigie AI, Richards MH, Cooper SJB, Schwarz MP (2010) Molecular phylogeny of the small carpenter bees (Hymenoptera: Apidae: Ceratinini) indicates early and rapid global dispersal. Mol Phylogenet Evol 55(3):1042–1054. doi: 10.1016/j.ympev.2010.01.011 PubMedCrossRefGoogle Scholar
  45. Rehan SM, Leys R, Schwarz MP (2012) A mid-Cretaceous origin of sociality in Xylocopine bees with only two origins of true worker castes indicates severe barriers to eusociality. PLoS ONE 7(4):e34690PubMedCrossRefPubMedCentralGoogle Scholar
  46. Reyes SG (1991) Revision of the bee genus Braunsapis in the oriental region (Apoidea: Xylocopinae: Allodapini). Univ Kansas Sci Bull 54:179–207Google Scholar
  47. Simpson S, Gross C, Silberbauer L (2005) Broom and honeybees in Australia: an alien liaison. Plant Biol 7(5):541–548PubMedCrossRefGoogle Scholar
  48. Smith JA, Chenoweth LB, Tierney SM, Schwarz MP (2013) Repeated origins of social parasitism in allodapine bees indicate that the weak form of Emery’s rule is widespread, yet sympatric speciation remains highly problematic. Biol J Linn Soc 109(2):320–331CrossRefGoogle Scholar
  49. Stokes KE, Buckley YM, Sheppard AW (2006) A modelling approach to estimate the effect of exotic pollinators on exotic weed population dynamics: bumblebees and broom in Australia. Divers Distrib 12(5):593–600CrossRefGoogle Scholar
  50. Swofford DL (1999) PAUP. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
  51. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21(4):208–216PubMedCrossRefGoogle Scholar
  52. Trewick SA, Paterson AM, Campbell HJ (2007) Guest editorial: hello New Zealand. J Biogeogr 34(1):1–6CrossRefGoogle Scholar
  53. van der Vecht J (1952) A preliminary revision of the oriental species of the genus Ceratina (Hymenoptera, Apoidea). Zoologische Verhandelingen 16:1–85Google Scholar
  54. Waters JM, Craw D (2006) Goodbye Gondwana? New Zealand biogeography, geology, and the problem of circularity. Syst Biol 55(2):351–356PubMedCrossRefGoogle Scholar
  55. Zayed A, Constantin ŞA, Packer L (2007) Successful biological invasion despite a severe genetic load. PLoS ONE 2(9):e868PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Scott V. C. Groom
    • 1
  • Hien T. Ngo
    • 2
  • Sandra M. Rehan
    • 3
  • Posa Skelton
    • 4
  • Mark I. Stevens
    • 5
    • 6
  • Michael P. Schwarz
    • 1
  1. 1.School of Biological SciencesFlinders University of South AustraliaAdelaideAustralia
  2. 2.Department of BiologyYork UniversityTorontoCanada
  3. 3.Department of Biological SciencesUniversity of New HampshireDurhamUSA
  4. 4.Secretariat of the Pacific Regional Environment ProgramApiaSamoa
  5. 5.South Australian MuseumAdelaideAustralia
  6. 6.School of Earth and Environmental SciencesUniversity of AdelaideAdelaideAustralia

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