Skip to main content

Elucidating genetic signatures of native and introduced populations of the Cycad Blue, Chilades pandava to Taiwan: a threat both to Sago Palm and to native Cycas populations worldwide

Abstract

Foreign plants are usually introduced for food or aesthetic reasons. Most of these plants are non-invasive, but can alter the evolutionary trajectory of the associated native insects or inadvertently spread potential pests. A hitherto poorly documented example is the rapid expansion of Chilades pandava, a Cycas-feeding butterfly. Since about 1990, large numbers of the Sago Palm Cycas revoluta were introduced into Taiwan. Invading or introduced with this hostplant, Ch. pandava has rapidly spread to all major parts of Taiwan. To trace the source of outbreaks, we sampled 810 specimens covering 50 Taiwanese localities and other regions using mitochondrial COII sequences. Overall haplotype diversity was high (h = 0.791), but only 29 haplotypes were found. The haplotype C which dominates outbreak populations from western Taiwan was endemic to the island. This is consistent with the hypothesis of a local range expansion of Ch. pandava, rather than an introduction. In addition, the Taiwanese Central Mountain Ridge may constitute a primary biogeographic barrier restricting gene flow between eastern and western populations. Our study not only flags an important new invasive insect that needs to be monitored and controlled within the horticultural trade and for in situ cycad conservation, but also provides a clearly documented case of the transformation of a native tropical butterfly into a pest via introduced horticultural plants.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Bascombe MJ, Bascombe FS, Johnston G (1999) The butterflies of Hong Kong. Academic Press, London

    Google Scholar 

  2. Calonje M (2007) Guam and Rota 2007: Working against cycad extinction. Montgomery Botanical Center Expedition Report. http://www.montgomerybotanical.org/media/Newsletters/MBC_SprSumm08_newsltr.pdf. Accessed 21 Apr 2009

  3. Carroll SP (2007) Natives adapting to invasive species: ecology, genes, and the sustainability of conservation. Ecol Res 22:892–901. doi:10.1007/s11284-007-0352-5

    Article  Google Scholar 

  4. Caterino MS, Sperling FAH (1999) Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Mol Phylogenet Evol 11:122–137. doi:10.1006/mpev.1998.0549

    Article  CAS  PubMed  Google Scholar 

  5. Chang YC (1989) Morphology, life history and damage of Cycas blue butterfly (Chilades pandava pandava) as well as pathogenicity of entomogenous fungus to its larva. Bull Taiwan Res Inst New Series 4:43–50

    Google Scholar 

  6. Chapin FS III, Zavaleta ES, Eviner VT et al (2000) Consequences of changing biodiversity. Nature 405:234–242. doi:10.1038/35012241

    Article  CAS  PubMed  Google Scholar 

  7. Chen SF, Rossiter SJ, Faulkes CG, Jones G (2006) Population genetic structure and demographic history of the endemic Formosan lesser horseshoe bat (Rhinolophus monoceros). Mol Ecol 15:1643–1656. doi:10.1111/j.1365-294X.2006.02879.x

    Article  CAS  PubMed  Google Scholar 

  8. Cheng YP, HWang SY, Lin TP (2005) Potential refugia in Taiwan revealed by the phylogeographical study of Castanopsis carlesii Hayata (Fagaceae). Mol Ecol 14:2075–2085. doi:10.1111/j.1365-294X.2005.02567.x

    Article  CAS  PubMed  Google Scholar 

  9. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660. doi:10.1046/j.1365-294x.2000.01020.x

    Article  CAS  PubMed  Google Scholar 

  10. Corbet AS, Pendlebury HM (1992) The butterflies of the Malay Peninsula. United Selangor Press, Kuala Lumpur

    Google Scholar 

  11. Darling JA, Bagley MJ, Roman J et al (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol Ecol 17:4992–5007. doi:10.1111/j.1365-294X.2008.03978.x

    Article  CAS  PubMed  Google Scholar 

  12. Donaldson JS (2003) Cycads: status survey and conservation action plan. IUCN/SSC Cycad Specialist Group. http://data.iucn.org/dbtw-wpd/edocs/2003-010.pdf. Accessed 21 Apr 2009

  13. Ehrlich PR (1984) The structure and dynamics of butterfly populations. In: Vane-Wright RI, Ackery PR (eds) The biology of butterflies. Academic Press, London, pp 25–40

    Google Scholar 

  14. Evans WH (1932) The identification of Indian butterflies. Bombay Natural History Society, Madras

    Google Scholar 

  15. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  16. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed  Google Scholar 

  17. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413

    CAS  PubMed  Google Scholar 

  18. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    CAS  PubMed  Google Scholar 

  19. Gao ZZ, Jian SG, Wei Q, Xie ZH, Wang SP (2004) Wild cycads were harmed by Chilades pandava (Horsfield). Plant Quarantine 18:27–28 (in Chinese)

    Google Scholar 

  20. Germain JF, Hodges GS (2007) First report of Aulacaspis yasumatsui (Hemiptera: Diaspididae) in Africa (Ivory Coast), and update on distribution. Fla Entomol 90:755–756. doi:10.1653/0015-4040(2007)90[755:FROAYH]2.0.CO;2

    Article  Google Scholar 

  21. Gompert Z, Nice CC, Fordyce JA, Forister ML, Shapiro AM (2006) Identifying units for conservation using molecular systematics: the cautionary tale of the Karner Blue Butterfly. Mol Ecol 15:1759–1768. doi:10.1111/j.1365-294X.2600.02905.x

    Article  CAS  PubMed  Google Scholar 

  22. Guillermet C (2009) L’entomologie à l’île de La Réunion. http://chring.club.fr/index.html. Accessed 21 Apr 2009

  23. Habel JC, Finger A, Meyer M, Schmitt T, Assmann T (2008) Polymorphic microsatellite loci in the endangered butterfly Lycaena helle (Lepidoptera: Lycaenidae). Eur J Entomol 105:361–362

    CAS  Google Scholar 

  24. Hall DW, Butler JF (1995) Atala, atala hairstreak, coontie hairstreak, Eumaeus atala Rober (Insecta: Lepidoptera: Lycaenidae). University of Florida IFAS Extension document EENY-169. Available from http://entnemdept.ufl.edu/creatures/bfly/atala_hairstreak.htm. Accessed 30 Aug 2009

  25. Hamano E (1987) Ecological encyclopedia of Taiwanese butterflies. Newton Press, Taipei

    Google Scholar 

  26. Hill KD, Stevenson DW, Osboren R (2004) The world list of cycads. Bot Rev 70:274–298

    Article  Google Scholar 

  27. Hirai N (2009) Records of the cycad blue butterfly, Chilades pandava, in Honshu and Shikoku, Japan. YADORIGA 220:2–19 (in Japanese)

  28. Howard FW, Hamon A, Mclaughlin M, Weissling T, Yang SL (1999) Aulacaspis yasumatsui (Hemiptera: Sternorrhyncha: Diaspididae), a scale insect pest of cycads recently introduced into Florida. Fla Entomol 82:14–27

    Article  Google Scholar 

  29. Hsu YF (1987) Notes on Chilades pandava pandava Horsfield from Taiwan (Lepidoptera, Lycaenidae). Tyô to Ga 38:9–12

    Google Scholar 

  30. Hsu YF (1989) Systematic position and description of Chilades peripatria sp. nov. (Lepidoptera: Lycaenidae). Bull Inst Zool Acad Sin 28:55–62

    Google Scholar 

  31. Hsu YF (2002) Butterflies of Taiwan. National Fonghuanggu Bird Park, Nantou

    Google Scholar 

  32. Hu YF, Chen ZD, Chen CJ, Geng BY (1999) Discoveries of some fossils of cycad reproductive organs from China and their significance to the origin of cycads. In: Chen CJ (ed) Proceedings of the fourth international conference on Cycad biology. International Academic Publishers, Sichuan, pp 135–141

    Google Scholar 

  33. Huang S, Chiang YC, Schaal BA, Chou CH, Chiang TY (2001) Organelle DNA phylogeography of Cycas taitungensis, a relict species in Taiwan. Mol Ecol 10:2669–2681. doi:10.1046/j.0962-1083.2001.01395.x

    Article  CAS  PubMed  Google Scholar 

  34. Igarashi S, Fukuda H (2000) The life histories of Asian butterflies. Tokai University Press, Tokyo

    Google Scholar 

  35. Jian S, Zhong Y, Liu N, Gao Z, Wei Q, Xie Z, Ren H (2006) Genetic variation in the endangered endemic species Cycas fairylakea (Cycadaceae) in China and implications for conservation. Biodivers Conserv 15:1681–1694. doi:10.1007/s10531-004-5017-x

    Article  Google Scholar 

  36. Jones DL (1993) Cycads of the world: ancient plants in today’s landscape. Smithsonian Institution Press, Washington

    Google Scholar 

  37. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. doi:10.1016/S0169-5347(02)02499-0

    Article  Google Scholar 

  38. Konishi T (1987) The collection of one unrecorded Chilades species from Taiwan. Gekkan-Mushi 196:25 (in Japanese)

    Google Scholar 

  39. Lan PL (1999) The population biology of Chilades pandava peripatria (Lepidoptera: Lycaenidae): the fluctuation of population. Dissertation, National Taiwan Normal University

  40. Landolt PJ (1984) The Florida atala butterfly, Eumaeus atala florida Rueber (Lepidoptera: Lycaenidae), in Dade County, Florida. Fla Entomol 67:570–571

    Article  Google Scholar 

  41. Lee JY (1989) Notes on the life history of Chilades pandava pandava Horsfield (Lepidoptera, Lycaenidae) in Taiwan. Gekkan-Mushi 215:4–5 (in Japanese)

    Google Scholar 

  42. Lee YJ, Hwang SY, Ho KC, Lin TP (2006) Source populations of Quercus glauca in the last glacial age in Taiwan revealed by nuclear microsatellite markers. J Hered 97:261–269

    Article  CAS  PubMed  Google Scholar 

  43. Liu YC, Lu FY, Ou CH (1994) Trees of Taiwan. National Chung-Shing University, Taiching (in Chinese)

    Google Scholar 

  44. Liu GH, Lu YY, Gan YH, Zeng L (2003) The biology and population dynamics of the butterfly Chilades pandava. Entomol Knowl 40:426–428 (in Chinese)

    Google Scholar 

  45. Lohman DJ, Peggie D, Pierce NE, Meier R (2008) Phylogeography and genetic diversity of a widespread Old World butterfly, Lampides boeticus (Lepidoptera: Lycaenidae). BMC Evol Biol 8:301. doi:10.1186/1471-2148-8-301

    Article  PubMed  Google Scholar 

  46. Luo J, Cai ZJ (2002) Investigations on the main species of garden plant pests of Fuzhou JinShan school district. Entomol J East China 11:35–40 (in Chinese)

    Google Scholar 

  47. Martiré D, Rochat J (2008) Les Papillons de la Réunion et leurs chenilles. Biotope, Mèze (Collection Parthenope); Muséum national d’Histoire naturelle, Paris

  48. Mitsuhashi W (1992) A new record of Chilades pandava (Lepidoptera, Lycaenidae) from Japan. Choken Field 81:8–9 (in Japanese)

    Google Scholar 

  49. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451

    Article  CAS  PubMed  Google Scholar 

  50. Moore A (2008) Cycad Blue butterfly fact sheet. http://www.guaminsects.net/uogces/kbwiki/index.php?title = Chilades_pandava. Accessed 21 Apr 2009

  51. Moore A, Marler T, Miller RH, Muniappan R (2005) Biological control of cycad Aulacaspis scale on Guam. Cycad Newsl 28:6–8

    Google Scholar 

  52. Norstog KJ, Nicholls TJ (1997) The biology of the Cycads. Cornell University Press, Now York

    Google Scholar 

  53. Oliver JC (2006) Population genetic effects of human-mediated plant range expansions on native phytophagous insects. Oikos 112:456–463. doi:10.1111/j.0030-1299.2006.14185.x

    Article  Google Scholar 

  54. Otto SP (2000) Detecting the form of selection from DNA sequence data. Trends Genet 16:526–529. doi:10.1016/S0168-9525(00)02141-7

    Article  CAS  PubMed  Google Scholar 

  55. Pannell JR, Dorken ME (2006) Colonisation as a common denominator in plant metapopulations and range expansions: effects on genetic diversity and sexual systems. Landsc Ecol 21:837–848. doi:10.1007/s10980-005-5389-7

    Article  Google Scholar 

  56. Parsons M (1999) The butterflies of Papua New Guinea. Academic Press, London

    Google Scholar 

  57. Peng YW (2006) Population genetic structure of Steere’s liocichla (Liocichla steerii) in Taiwan. Dissertation, National Taiwan University. (in Chinese)

  58. Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45. doi:10.1016/S0169-5347(00)02026-7

    Article  PubMed  Google Scholar 

  59. Reichard SH, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51:103–113. doi:10.1641/0006-3568(2001)051[0103:HAAPOI]2.0.CO;2

    Article  Google Scholar 

  60. Rochat J (2008) Terrestrial invertebrate biodiversity of Reunion Island. http://www.regionreunion.com/fr/spip/IMG/pdf/insectarium_in_english.pdf. Accessed 21 Apr 2009

  61. Rothschild M, Nash RJ, Bell EA (1986) Cycasin in the endangered butterfly Eumaeus atala florida. Phytochemistry 25:1853–1854

    Article  CAS  Google Scholar 

  62. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  63. Schneider D, Wink M, Sporer F, Lounibos P (2002) Cycads: their evolution, toxins, herbivores and insect pollinators. Naturwissenschaften 89:281–294

    Article  CAS  PubMed  Google Scholar 

  64. Schreiner IH, Nafus DM (1997) Butterflies of Micronesia. College of Agriculture and Life Sciences University of Guam, Mangilao

    Google Scholar 

  65. Shapiro AM (2002) The Californian urban butterfly fauna is dependent on alien plants. Divers Distrib 8:31–40. doi:10.1046/j.1366-9516.2001.00120.x

    Article  Google Scholar 

  66. Shen CF, Hill KD, Tsou CH, Chen CJ (1994) Cycas taitungensis C. F. Shen, K. D. Hill, C. H. Tsou, C. J. Chen, sp. Nov. (Cycadaceae), a new name for the widely known cycad species endemic in Taiwan. Bot Bull Acad Sinica 35:133–140

    Google Scholar 

  67. Shirôzu T (1960) Butterflies of Formosa. Hoikusha, Osaka. (in Japanese)

  68. Shirôzu T, Ueda K (1992) Lycaenidae. In: Heppner JB, Inoue H (eds) Lepidoptera of Taiwan. Association for Tropical Lepidoptera, Gainesville, pp 140–150

    Google Scholar 

  69. Sibuet JC, Hsu SK (2004) How was Taiwan created? Tectonophysics 379:159–181. doi:10.1016/j.tecto.2003.10.022

    Article  Google Scholar 

  70. Srivstava PC, de Swing CC (2008) Observaciones alarmantes sobre ciertas plagas de cícadas cultivadas y silvestres en la India. http://www.igc.up.ac.pa/vice-ip/Final%20Abstracts%20Only.doc. Accessed 21 April 2009

  71. Stastny M, Battisti A, Petrucco-Toffolo P, Schlyter F, Larsson S (2006) Host-plant use in the range expansion of the pine processionary moth, Thaumetopoea pityocampa. Ecol Entomol 31:481–490. doi:10.1111/j.1365-2311.2006.00807.x

    Article  Google Scholar 

  72. Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374. doi:10.1111/j.1461-0248.2005.00874.x

    Article  PubMed  Google Scholar 

  73. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  Google Scholar 

  74. Takegami A (2001) A record of Chilades pandava at Yonaguni Island. Choken Field 184:28–29 (in Japanese)

    Google Scholar 

  75. Takeuchi T (2006) A new record of Chilades pandava (Horsfield) (Lepidoptera, Lycaenidae) from Korea. Trans Lep Soc Jap 57:325–326 (in Japanese)

    Google Scholar 

  76. Tallamy DW (2004) Do alien plants reduce insect biomass? Conserv Biol 18:1689–1692. doi:10.1111/j.1523-1739.2004.00512.x

    Article  Google Scholar 

  77. Tang W, Oberpreiler R (2006) Pest alert: insect pests of cycads. IUCN/SSC Cycad Specialist group. Available from http://lib.store.yahoo.net/lib/cycads/InsectPestsofCycads.pdf. Accessed 21 Apr 2009

  78. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data III. Genetics 132:619–633

    CAS  PubMed  Google Scholar 

  79. Treutlein J, Wink M (2002) Molecular phylogeny of cycads inferred from rbcL sequences. Naturwissenschaften 89:221–225. doi:10.1007/s00114-002-0308-0

    Article  CAS  PubMed  Google Scholar 

  80. Tzeng CS, Lin YS, Lin SM, Wang TY, Wang FY (2006) The phylogeography and population demographics of selected freshwater fishes in Taiwan. Zool Stud 45:285–297

    CAS  Google Scholar 

  81. Valade R, Kenis M, Hernandez-Lopez A, Augustin S, Mari Mena N, Magnoux E, Rougerie R, Lakatos F, Roques A, Lopez-Vaamonde C (2009) Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae). Mol Ecol 18:3458–3470. doi:10.1111/j.1365-294X.2009.04290.x

    Article  CAS  PubMed  Google Scholar 

  82. Vellend M, Harmon LJ, Lockwood JL, Mayfield MM, Hughes AR, Wares JP, Sax DF (2007) Effects of exotic species on evolutionary diversification. Trends Ecol Evol 22:481–488. doi:10.1016/j.tree.2007.02.017

    Article  PubMed  Google Scholar 

  83. Wang FX, Liang HB, Chen TQ, Wang DY (1996) Cycads in China. Guandong Science and Technology Press, Guandong

    Google Scholar 

  84. Wang TY, Liao TY, Tzeng CS (2007) Phylogeography of the Taiwanese endemic hillstream loaches, Hemimyzon formosanus and H. taitungensis (Cypriniformes: Balitoridae). Zool Stud 46:547–560

    CAS  Google Scholar 

  85. Wei QY (2006) A preliminary study on the bionomics and control of Chilades pandava pandava. Chinese Bull Entomol 43:870–872

    Google Scholar 

  86. Weissling TJ, Howard FW, Hamon AB (1999) Cycad aulascaspis scale, Aulacaspis yasumatsui Takagi (Insecta: Homoptera: Sternorrhyncha: Diaspididae). Florida Coop Ext Service Publication document EENY-096. Available from http://polkhort.ifas.ufl.edu/documents/publications/Cycad%20Scale.pdf Accessed 30 Aug 2009

  87. Whitelock LM (2002) The cycads. Timber Press, Oregon

    Google Scholar 

  88. Williams AAE (2006) Butterfly observations on Mauritius Island, with notes on three recently introduced lycaenids, Leptomyrina phidias (Fabricius), Petrelaea sichela reticulum (Mabille) and Chilades pandava (Horsfield) (Lepidoptera: Lycaenidae). Newsl West Aust Insect Stud Soc. Available from http://www.museum.wa.gov.au/waiss/pages/documents/2006Feb.pdf

  89. Williams JR (2007) Butterflies of Mauritius. Bioculture Press, Rivière des Anguilles

    Google Scholar 

  90. Yago M, Hirai N, Kondo M et al (2008) Molecular systematics and biogeography of the genus Zizina (Lepidoptera: Lycaenidae). Zootaxa 1746:15–38

    Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the National Science Council (NSC), Taiwan under NSC90-2313-B-003-002, NSC91-2313-B-003-002, NSC92-2313-B-003-001, and NSC 96-2621-B-110-001. We would like to thank Dr. Chih-Chien Lu, Pei-Chun Liao, Chia-Hung Hsieh, and Mr. Yik-fui Lo, Chia-Long Huang, Li-Hao Wang, Ming-Chong Ng, Hieng-Ming Ting, Zhi-Yi Shi, Andy Jan, and Miss Nan-Ying Chen, Jin-Rong Zhu and Shu-Ting Ang for providing the specimens from Taiwan, Southeast Asia and some places from mainland China. We also thank Dr. Hideyuki Chiba, and Dr. Masaya Yago for providing specimens from Japan, Dr. Tsuyoshi Takeuchi for providing specimens from Korea, and Dr. Aubrey Moore for providing specimens from Guam. Madagascar specimens were collected under Leverhulme Trust F/696/I and National Geographical Society #7332-02 and Steve Collins and Ichiro Nakamura are thanked also for providing extra data and specimens. One of us (DCL) benefited from a STUDIUM fellowship during the writing of this paper. Carlos Lopez-Vaamonde kindly commented on the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Yu-Feng Hsu.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wu, LW., Yen, SH., Lees, D.C. et al. Elucidating genetic signatures of native and introduced populations of the Cycad Blue, Chilades pandava to Taiwan: a threat both to Sago Palm and to native Cycas populations worldwide. Biol Invasions 12, 2649–2669 (2010). https://doi.org/10.1007/s10530-009-9672-4

Download citation

Keywords

  • Population outbreak
  • Chilades pandava
  • Cycas
  • Range expansion
  • Horticultural trade
  • COII