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Biological Invasions

, Volume 16, Issue 12, pp 2563–2575 | Cite as

Patterns of non-randomness in the composition and characteristics of the Taiwanese bird trade

  • Shan Su
  • Phill Cassey
  • Tim M. Blackburn
Original Paper

Abstract

The invasion pathway is composed of a sequential series of stages that need to be quantified separately in order properly to understand the invasion process. Here, we examine the composition and characteristics of bird species being sold in the pet bird market in Taiwan. The bird trade in Taiwan is of high volume and financially lucrative. The identity of species in this trade is vital for informing later stages (introduction, establishment, spread) of the invasion pathway. We conducted interviews and surveys of 72 outlets selling pet birds from seven cities across Taiwan, from which we identified 247 bird species (within 34 families) for sale. Of these, 170 bird species (from 27 families) are exotic to Taiwan. Using randomization tests, we show that nine families are significantly over-represented in the pet trade (Psittacidae, Muscicapidae, Timaliidae, Sturnidae, Turdidae, Estrildidae, Chloropseidae, Zosteropidae and Fringillidae), and three after sequential Bonferroni correction (Psittacidae, Muscicapidae and Sturnidae). Species that have been identified in Taiwanese pet shops tend to have a larger native geographic range, originate further from the equator, are smaller-bodied, and have more aesthetically-pleasing songs than expected by chance. The native ranges of pet shop species are more likely to be situated in the Indo-Malay and Palearctic biogeographic realms, while fewer species than expected derive from the Neotropic, Afrotropic and Nearctic realms. Our results show that bird species for sale in Taiwan are determined by the interaction of species availability and societal demands.

Keywords

Invasion pathway Pet bird trade Randomization test Taiwan 

Notes

Acknowledgments

This study received financial support from Institute of Zoology, Zoological Society of London. We thank C.J. Sha for help with species identification. We also thank Y. Wang and William Chi for providing information on the wild bird trade in Taiwan, and David Orme and Valerie Olson for supplying data on geographic ranges and body sizes.

Supplementary material

10530_2014_686_MOESM1_ESM.pdf (55 kb)
Supplementary material 1 (PDF 54 kb)

References

  1. Bennett PM, Owens IPF (2002) Evolutionary ecology of birds: life histories, mating systems, and extinction. Oxford University Press, OxfordGoogle Scholar
  2. Blackburn TM, Cassey P (2007) Patterns of non-randomness in the exotic avifauna of Florida. Divers Distrib 13:519–526CrossRefGoogle Scholar
  3. Blackburn TM, Duncan RP (2001) Establishment patterns of exotic birds are constrained by non-random patterns in introduction. J Biogeogr 28:927–939CrossRefGoogle Scholar
  4. Blackburn TM, Cassey P, Gaston KJ (2006) Variations on a theme: sources of heterogeneity in the form of the interspecific relationship between abundance and distribution. J Anim Ecol 75:1426–1439. doi: 10.1111/j.1365-2656.2006.01167.x PubMedCrossRefGoogle Scholar
  5. Blackburn TM, Lockwood JL, Cassey P (2009) Avian invasions: the ecology and evolution of exotic birds. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. Blackburn TM, Gaston KJ, Parnell M (2010) Changes in non-randomness in the expanding introduced avifauna of the world. Ecography 33:168–174. doi: 10.1111/j.1600-0587.2009.05882.x CrossRefGoogle Scholar
  7. Blackburn TM, Pyšek P, Bacher S et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339. doi: 10.1016/j.tree.2011.03.023 PubMedCrossRefGoogle Scholar
  8. Blackburn TM, Su S, Cassey P (2014) A potential metric of the attractiveness of bird song to humans. Ethology in pressGoogle Scholar
  9. Brazil M (2010) Field guide to the birds of East Asia Eastern China, Taiwan, Korea, Japan and Eastern Russia. Christopher Helm, LondonGoogle Scholar
  10. Brooks-Moizer F, Roberton SI, Edmunds K, Bell D (2008) Avian Influenza H5N1 and the wild bird trade in Hanoi, Vietnam. Ecol Soc 14:28Google Scholar
  11. Cabezas S, Carrete M, Tella JL et al (2012) Differences in acute stress responses between wild-caught and captive-bred birds: a physiological mechanism contributing to current avian invasions? Biol Invasions 15:521–527. doi: 10.1007/s10530-012-0304-z CrossRefGoogle Scholar
  12. Carrete M, Tella J (2008) Wild-bird trade and exotic invasions: a new link of conservation concern? Front Ecol Environ 6:207–211. doi: 10.1890/070075 CrossRefGoogle Scholar
  13. Cassey P (2008) Are there body size implications for the success of globally introduced land birds? Ecography 24:413–420. doi: 10.1111/j.1600-0587.2001.tb00476.x CrossRefGoogle Scholar
  14. Cassey P, Blackburn TM, Sol D et al (2004a) Global patterns of introduction effort and establishment success in birds. Proc R Soc B Biol Sci 271:S405–S408. doi: 10.1098/rsbl.2004.0199 CrossRefGoogle Scholar
  15. Cassey P, Blackburn TM, Russell GJ et al (2004b) Influences on the transport and establishment of exotic bird species: an analysis of the parrots (Psittaciformes) of the world. Glob Change Biol 10:417–426. doi: 10.1111/j.1529-8817.2003.00748.x CrossRefGoogle Scholar
  16. Chen GH (2005a) The research of exotic species, ornamental species and pet animals. A report of Forestry Bureau, TaiwanGoogle Scholar
  17. Chen JM (2005b) Animal release: the cognition, belief, attitude and behavior of participators. A report of National Science Council, TaiwanGoogle Scholar
  18. Chinese Wild Bird Federation (2012) The checklist of birds of Taiwan Chinese. Wild Bird FederationGoogle Scholar
  19. Chi WL (1995) An investigation report on pet bird trade in Taiwan. Green Consumer’s Foundation, TaiwanGoogle Scholar
  20. Chi WL, Chen AL, Yiau HC et al (1991) The sale status of wild birds in Taipei City. Wildbirds 2:29–36Google Scholar
  21. Colautti RI, Grigorovich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 8:1023–1037. doi: 10.1007/s10530-005-3735-y CrossRefGoogle Scholar
  22. Cooney R, Jepson P (2005) The international wild bird trade: what’s wrong with blanket bans? Oryx 40:18. doi: 10.1017/S0030605306000056 CrossRefGoogle Scholar
  23. Costello CJ, Solow AR (2003) On the pattern of discovery of introduced species. Proc Natl Acad Sci 100:3321–3323. doi: 10.1073/pnas.0636536100 PubMedCentralPubMedCrossRefGoogle Scholar
  24. Crosby AW (2004) Ecological imperialism: the biological expansion of Europe, 900–1900. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  25. Del Hoyo J, Elliott J, Christie D (2005) Handbook of the birds of the world: cuckoo-shrikes to thrushes. Lynx Eds., BarcelonaGoogle Scholar
  26. Duncan RP, Blackburn TM, Sol D (2003) The ecology of bird introduction. Annu Rev Ecol Evol Syst 34:71–98. doi: 10.1146/annurev.ecolsys.34.011802.132353 CrossRefGoogle Scholar
  27. Dunning JB (1992) CRC handbook of avian body masses. CRC Press, Boca Raton, FloridaGoogle Scholar
  28. Environment and Animal Society of Taiwan (2004a) A report of prayer animals in Taiwanese pet shops. Environment and Animal Society of Taiwan, TaiwanGoogle Scholar
  29. Environment and Animal Society of Taiwan (EAST), Kaohsiung Teacher’s Association (2004b) The practices of prayer animal releases conducted by religious organisations in Taiwan. Environment and Animal Society of Taiwan, TaiwanGoogle Scholar
  30. FAO (2011) International trade in wild birds, and related bird movements, in Latin America and the Caribbean. Animal Production and Health Paper, RomeGoogle Scholar
  31. Feare C, Craig A, Croucher B et al (1998) Starlings and mynas. Christopher Helm, LondonGoogle Scholar
  32. Forsyth DM, Duncan RP, Bomford M, Moore G (2004) Climatic suitability, life-history traits, introduction effort, and the establishment and spread of introduced mammals in Australia. Conserv Biol 18:557–569. doi: 10.1111/j.1523-1739.2004.00423.x CrossRefGoogle Scholar
  33. Gaston KJ (1991) How large is a species’ geographic range? Wiley Behalf Nord Soc Oikos 61:434–438Google Scholar
  34. Gaston KJ (1994) Measuring geographic range sizes. Wiley Behalf Nord Soc Oikos 17:198–205Google Scholar
  35. Gaston KJ, Blackburn TM (1995) Birds, body size and the threat of extinction. Philos Trans R Soc B Biol Sci 347:205–212. doi: 10.1098/rstb.1995.0022 CrossRefGoogle Scholar
  36. Gaston KJ, Blackburn TM (2000) Pattern and process in macroecology. Blackwell Science, OxfordCrossRefGoogle Scholar
  37. Hackett SJ, Kimball RT, Reddy S et al (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768. doi: 10.1126/science.1157704 Google Scholar
  38. Heger T, Saul W-C, Trepl L (2013) What biological invasions “are” is a matter of perspective. J Nat Conserv 21:93–96. doi: 10.1016/j.jnc.2012.11.002 CrossRefGoogle Scholar
  39. Hulme PE, Bacher S, Kenis M et al (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414CrossRefGoogle Scholar
  40. Inskipp TP (1990) Overview of the numbers and value of birds in trade. Paper presented at the Symposium on Trade in Wild Birds, Twentieth World Conference of International Council for Bird Preservation, Hamilton, New ZealandGoogle Scholar
  41. Jepson P, Ladle RJ (2005) Bird-keeping in Indonesia: conservation impacts and the potential for substitution-based conservation responses. Oryx 39Google Scholar
  42. Jeschke JM (2005) From the cover: invasion success of vertebrates in Europe and North America. Proc Natl Acad Sci 102:7198–7202. doi: 10.1073/pnas.0501271102 PubMedCentralPubMedCrossRefGoogle Scholar
  43. Jeschke JM, Strayer DL (2006) Determinants of vertebrate invasion success in Europe and North America. Glob Change Biol 12:1608–1619. doi: 10.1111/j.1365-2486.2006.01213.x CrossRefGoogle Scholar
  44. Jetz W, Thomas GH, Joy JB et al (2012) The global diversity of birds in space and time. Nature 491:444–448. doi: 10.1038/nature11631 PubMedCrossRefGoogle Scholar
  45. Juniper T, Parr M (1998) Parrots: a guide to parrots of the world. Yale University Press, New HavenGoogle Scholar
  46. Kark S, Sol D (2005) Establishment success across convergent Mediterranean ecosystems: an analysis of bird introductions. Conserv Biol 19:1519–1527. doi: 10.1111/j.1523-1739.2005.004365.x CrossRefGoogle Scholar
  47. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204PubMedCrossRefGoogle Scholar
  48. Lau MW-N, Bortolotti G, Goodyer N, Zou F (1996) Wildlife Trade in Southern China including Hong Kong and Macao. Biodiversity Working Group of the China Council for International Cooperation on Environment and Development Project, Hong kongGoogle Scholar
  49. Lee TW, Shieh BS (2005) Pet sales of exotic estrildid birds in relation to the field-records in Taiwan. Endem Species Res 7:1–12Google Scholar
  50. Lever C (1994) Naturalized animals: the ecology of successfully introduced species. T & A D Poyser, LondonGoogle Scholar
  51. Li S-H, Li J-W, Han L-X et al (2006) Species delimitation in the Hwamei Garrulax canorus: species delimitation in the Hwamei. Ibis 148:698–706. doi: 10.1111/j.1474-919X.2006.00571.x CrossRefGoogle Scholar
  52. Liao B (2012) Taiwan ye niao tu jian = Wild birds of Taiwan. Chen xing chu ban you xian gong si, Taizhong ShiGoogle Scholar
  53. Lockwood JL (1999) Using taxonomy to predict success among introduced Avifauna: relative importance of transport and establishment. Conserv Biol 13:560–567CrossRefGoogle Scholar
  54. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. doi: 10.1016/j.tree.2005.02.004 PubMedCrossRefGoogle Scholar
  55. Lockwood JL, Hoopes MF, Marchetti MP (2007) Invasion ecology. Blackwell, MaldenGoogle Scholar
  56. Long JL (1981) Introduced birds of the world: the worldwide history, distribution, and influence of birds introduced to new environments. Reed, Terrey HillsGoogle Scholar
  57. MacIsaac HJ, Tedla RA, Ricciardi A (2010) Patterns and rate of growth of studies in invasion ecology. In: Richardson DM (ed) 50 years of invasion ecology: the legacy of Charles Elton. Wiley Blackwell, ChichesterGoogle Scholar
  58. MacKinnon JR (2000) A field guide to the birds of China. Oxford University Press, New YorkGoogle Scholar
  59. McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–727. doi: 10.1650/0010-5422(2002)104[0705:AFHRAR]2.0.CO;2 Google Scholar
  60. Meyerson LA, Mooney HA (2007) Invasive alien species in an era of globalization. Front Ecol Environ 5:199–208. doi: 10.1890/1540-9295(2007)5[199:IASIAE]2.0.CO;2 Google Scholar
  61. Nash SV (1993) Sold for a song: the trade in Southeast Asian Non-CITES birds. Traffic International, CambridgeGoogle Scholar
  62. Olson DM, Dinerstein E, Wikramanayake ED et al (2001) Terrestrial ecoregions of the world: a new map of life on earth. Bioscience 51:933. doi: 10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2
  63. Olson VA, Davies RG, Orme CDL et al. (2009) Global biogeography and ecology of body size in birds. Ecol Lett 12:249–259. doi: 10.1111/j.1461-0248.2009.01281.x Google Scholar
  64. Orme CDL, Davies RG, Olson VA et al (2006) Global patterns of geographic range size in birds. PLoS Biol 4:e208PubMedCentralPubMedCrossRefGoogle Scholar
  65. R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  66. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  67. Richardson DM, Ricciardi A (2013) Misleading criticisms of invasion science: a field guide. Divers Distrib 19:1461–1467. doi: 10.1111/ddi.12150 CrossRefGoogle Scholar
  68. Richardson DM, Pyšek P, Carlton JT (2010) A compendium of essential concepts and terminology in invasion ecology. In: Richardson DM (ed) Fifty years invasion ecol. Wiley-Blackwell, Oxford, pp 409–420CrossRefGoogle Scholar
  69. Severinghaus LL (1999) Exotic birds in Taiwan. Wild Birds 7:45–58Google Scholar
  70. Severinghaus LL (2007) The breeding ecology and dispersal of Taiwan and Light-vented Bulbuls in Kenting National Park. J Natl Park 17:27–41Google Scholar
  71. Severinghaus LL, Chi L (1999) Prayer animal release in Taiwan. Biol Conserv 89:301–304CrossRefGoogle Scholar
  72. Shepherd CR (2006) The bird trade in Medan, north Sumatra: an overview. BirdingASIA 5:16–24Google Scholar
  73. Shepherd CR, Stengel CJ, Nijman V (2012) The export and re-export of CITES-listed birds from the Solomon Islands. TRAFFIC, Southeast AsiaGoogle Scholar
  74. Shieh B, Lin Y, Lee T et al (2006) Pet trade as sources of introduced bird species in Taiwan. Taiwania 51:81–86Google Scholar
  75. Sibley CG, Monroe BL (1990) Distribution and taxonomy of the birds of the world. Yale University Press, New HavenGoogle Scholar
  76. Simberloff D (2003) How much information on population biology is needed to manage introduced species? Conserv Biol 17:83–92. doi: 10.1046/j.1523-1739.2003.02028.x CrossRefGoogle Scholar
  77. Simberloff D (2004) A rising tide of species and literature: a review of some recent books on biological invasions. Bioscience 54:247. doi: 10.1641/0006-3568(2004)054[0247:ARTOSA]2.0.CO;2
  78. Simpson K, Day N, Trusler P (2010) Birds of Australia, 8th edn. Princeton University Press, PrincetonGoogle Scholar
  79. Stevenson T, Fanshawe J (2002) Field guide to the birds of East Africa: Kenya, Tanzania, Uganda, Rwanda, Burundi. Christopher Helm, LondonGoogle Scholar
  80. Taipei Wild Bird Society (1996) Wild bird trade in Taipei City. Taipei Wild Bird Society, TaiwanGoogle Scholar
  81. Tang PC (2011) Enhancement of the management of parrot breeding grounds and parrot reproductive techniques. Council of Agriculture Executive Yuan Forestry Bureau, TaiwanGoogle Scholar
  82. TEIA (2004) An online survey of exotic bird. Taiwan Environmental Info AssociationGoogle Scholar
  83. Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. doi: 10.1111/j.1461-0248.2009.01418.x PubMedCrossRefGoogle Scholar
  84. Wang Y (2010) A Survey on the wild birds trade in Taiwan. Council of Agriculture Executive Yuan Forestry Bureau, TaiwanGoogle Scholar
  85. Williamson M (1997) Biological invasions. Chapman & Hall, LondonGoogle Scholar
  86. Xu WG, Dong RM (2007) The four most popular songbirds in China. ShangHai Scientific and Technological Literature Publishing House Co., Ltd., ShanghaiGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Institute of ZoologyZoological Society of LondonLondonUK
  2. 2.Research Department of Genetics, Evolution and EnvironmentUniversity College LondonLondonUK
  3. 3.School of Earth and Environmental SciencesUniversity of AdelaideAdelaideAustralia
  4. 4.Department of Botany and Zoology, Centre for Invasion BiologyStellenbosch UniversityStellenboschSouth Africa

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