Journal of Insect Conservation

, Volume 23, Issue 5–6, pp 921–931 | Cite as

Habitat, life history and oviposition choice of the endangered Bhutan Glory swallowtail Bhutanitis lidderdalii (Lepidoptera: Papilionidae) in Yunnan, China

  • Zhizhong Zhang
  • Zhicheng Jiang
  • Zhengyang WangEmail author


The Bhutan Glory, Bhutanitis lidderdalii (Atkinson, 1873) is considered to be an endangered swallowtail butterfly (Lepidoptera: Papilionidae) endemic to the eastern Himalayas and the Hengduan mountains. We describe a newly-discovered habitat for B. lidderdalii in Yunnan, China. We report the life history of B. lidderdalii, observed from 2016 to 2018, both in the butterfly’s natural habitat and in captive breeding. We contrast the life cycle of B. lidderdalii in Yunnan with that of other populations recorded in Bhutan and India, as well as that of other species in the genus. In its natural habitat, the major threats to the larval stages of B. lidderdalii include inclement weather and parasitization. We add Aristolochia ovatifolia (Hwang, 1981) to the list of recorded hostplants of this species. Our biometric measurement of 419 A. ovatifolia hostplants within the study habitat shows that although B. lidderdalii is locally abundant, hostplants preferred for oviposition are < 38 cm in height and are only found within broadleaf forests with abundant nectar plants. We suggest that the conservation management of B. lidderdalii and other butterfly species that rely on patchily distributed Aristolochia hostplants focus on assessing the distribution of isolated broadleaf forest habitats within temperate pine forests and studying the species’ dispersal ability across patches.


Bhutanitis lidderdalii Bhutanitis Bhutan Glory Life history Life cycle Habitat Butterfly conservation Aristolochia ovatifolia Oviposition choice Temporal isolation 



The authors thank Dr. D. P. A. Sands and an anonymous reviewer for providing invaluable suggestions on improving this manuscript. Zhizhong Zhang would like to thank his father Wenhao Zhang and mother Yinping Zhang for cultivating his passion in butterfly conservation and his wife Suochuan Zhao for numerous support in the field. He extends his gratitude to his friend Jiandong Qiu and Qinghua Yang for field assistance, Siyao Li for assistance in photography and Prof. Mingyong Chen from Yunnan University School of Life Sciences for his care and encouragement throughout the project. Zhengyang Wang was supported by a graduate fellowship from Harvard University Department of Organismic and Evolutionary Biology. He thanks his parents Hong Ning and Yalin Wang for supporting his interest in researching endangered butterflies; he thanks Prof. Naomi Pierce and Dr. Kadeem Gilbert from Harvard Museum of Comparative Zoology for providing invaluable advice on an early version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (XLSX 19 kb)


  1. Almada-Villela PC (1988) Checklist of fish and invertebrates listed in the CITES appendices. Nature Conservancy Council, LondonGoogle Scholar
  2. Baidya S, Karmakar T, Dutta PK, Padmanabhan S, Sondhi S, Saito M, Kunte K (2019) Bhutanitis ludlowi Gabriel, 1942—Mystical Bhutan Glory. In: Kunte K, Sondhi S, Roy P (eds) Butterflies of India v. 2.60. Indian Foundation for Butterflies. Accessed 4 Apr 2019
  3. Baldeck CA, Asner GP (2013) Estimating vegetation beta diversity from airborne imaging spectroscopy and unsupervised clustering. Remote Sens 5:2057–2071CrossRefGoogle Scholar
  4. Baughman JF, Murphy DD, Ehrlich PR (1988) Emergence patterns in male checkerspot butterflies: testing theory in the field. Theor Popul Biol 33(1):102–113CrossRefGoogle Scholar
  5. Bonebrake TC, Ponisio LC, Boggs CL, Ehrlich PR (2010) More than just indicators: a review of tropical butterfly ecology and conservation. Biol Conserv 143:1831–1841CrossRefGoogle Scholar
  6. Boufford DE (2004) South-Central China. In: Mittermeier RA, Gil PR, Hoffman M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, da Fonseca GAB (eds) Hotspots revisited, 1st English edn. CEMEX, Mexico City, pp 338–351Google Scholar
  7. Brandt JS, Kuemmerle T, Li H, Ren G, Zhu J, Radeloff VC (2012) Using Landsat imagery to map forest change in southwest China in response to the national logging ban and ecotourism development. Remote Sens Environ 121:358–369CrossRefGoogle Scholar
  8. Brückmann SV, Krauss J, Steffan-Dewenter I (2010) Butterfly and plant species suffer from reduced connectivity in fragmented landscapes. J Appl Ecol 47:799–809CrossRefGoogle Scholar
  9. Campbell RW (1981) Population dynamics. In: Doane CC, McManus ML (eds) The gypsy moth: research toward integrated pest management. United States Department of Agriculture, Washington, D.C., pp 65–241Google Scholar
  10. Chardon JP, Adriaensen F, Matthysen E (2003) Incorporating landscape elements into a connectivity measure: a case study for the Speckled wood butterfly (Pararge aegeria L.). Landsc Ecol 18:561–573CrossRefGoogle Scholar
  11. Chou I (1992) A study on the rare butterflies of the genus Bhutanitis (Lepidoptera: Papilionidae) with descriptions of two new species. Entomotaxonomia 14(1):48–54Google Scholar
  12. Chou I (1994) Monograph of Chinese butterflies. Henan Scientific and Technological Publishing House, Henan (in Chinese) Google Scholar
  13. Collins NM, Morris MG (1985) Threatened swallowtail butterflies of the world: the IUCN red data book. IUCN, GlandGoogle Scholar
  14. Davies WJ, Saccheri IJ (2015) Male emergence schedule and dispersal behaviour are modified by mate availability in heterogeneous landscapes: evidence from the orange-tip butterfly. PeerJ 3(1):e707PubMedPubMedCentralCrossRefGoogle Scholar
  15. Feret JB, Asner GP (2014) Mapping tropical forest canopy diversity using high-fidelity imaging spectroscopy. Ecol Appl 24:1289–1296PubMedCrossRefGoogle Scholar
  16. Gao K, Li X, Guo Z (2014) The bionomics, habitat requirements and population threats of the butterfly Bhutanitis thaidina in Taibai Mountain. J Insect Conserv 18:29–38CrossRefGoogle Scholar
  17. Grömping U (2006) Relative importance for linear regression in R: the package relaimpo. J Stat Softw 17(1):1–27CrossRefGoogle Scholar
  18. Harada M, Wangdi K, Wangdi S, Yago M, Aoki T, Igarashi Y, Yamaguchi S, Watanabe Y, Sherub Wangdi R, Drukpa S, Saito M, Moriyama Y, Uchiyama T (2012) Rediscovery of Ludlow’s Bhutan Glory, Bhutanitis ludlowi Gabriel (Lepidoptera: Papilionidae): morphology and biology. Butterflies (Teinopalpus) 60:4–15Google Scholar
  19. Harrison R (1985) Barriers to gene exchange between closely related cricket species. II. Life cycle variation and temporal isolation. Evolution 39(2):244–259PubMedCrossRefPubMedCentralGoogle Scholar
  20. Hauser CL (2005) Papilionidae—revised GloBIS/GART species checklist (2nd draft). Accessed 4 Apr 2019
  21. Igarashi S (1979) A new papilionid butterfly of the genus Bhutanitis from Northern Thailand. Tyo To Ga 30(1/2):69–72Google Scholar
  22. Igarashi S (1989) On the life history of Bhutanitis lidderdalei Atkinson in Bhutan (Lepidoptera, Papilionidae). Tyo To Ga 40:1–21Google Scholar
  23. Igarashi S (2003) Life history of Bhutanitis mansfieldi in comparison of related species. Butterflies (Teinopalpus) 35:20–39Google Scholar
  24. Igarashi S, Fukuda H (1997) The life histories of Asian butterflies, vol 1. Tokai University Press, TokyoGoogle Scholar
  25. Igarashi S, Harada M (2015) Sequel to “the life histories of Asian butterflies, vols I-II”. JapanGoogle Scholar
  26. Karube H (2010) Endemic insects in the Ogasawara Islands: negative impacts of alien species and a potential mitigation strategy. In: Kawakami K, Okochi I (eds) Restoring the oceanic island ecosystem. Springer, Tokyo, pp 133–137CrossRefGoogle Scholar
  27. Knowles LL, Alvarado-Serrano DF (2010) Exploring the population genetic consequences of the colonization process with spatio-temporally explicit models: insights from coupled ecological, demographic and genetic models in montane grasshoppers. Mol Ecol 19(17):3727–3745PubMedCrossRefPubMedCentralGoogle Scholar
  28. Konig MA, Wiklund C, Ehrien J (2016) Butterfly oviposition preference is not related to larval performance on a polyploid herb. Ecol Evol 6(9):2781–2789PubMedPubMedCentralCrossRefGoogle Scholar
  29. Kunte K, Sondhi S, Roy P (2019) Butterflies of India, v. 2.60. Indian Foundation for Butterflies. Accessed 4 Apr 2019
  30. Lampinen J, Heikkinen RK, Manninen P, Ryttäri T, Kuussaari M (2018) Importance of local habitat conditions and past and present habitat connectivity for the species richness of grassland plants and butterflies in power line clearings. Biodivers Conserv 27:217–233CrossRefGoogle Scholar
  31. Laurin GV, Chan JCW, Chen Q, Lindsell JA, Coomes DA, Guerriero L, Frate FD, Miglietta F, Valentini R (2014) Biodiversity mapping in a tropical West African forest with airborne hyperspectral data. PLoS ONE 9:e97910CrossRefGoogle Scholar
  32. Li X, Luo Y, Zhang Y, Schweiger O, Settele J, Yang Q (2010) On the conservation biology of a Chinese population of the birdwing Troides aeacus (Lepidoptera: Papilionidae). J Insect Conserv 14:257–268CrossRefGoogle Scholar
  33. Li X, Zhang Y, Settele J, Franzén M, Schweiger O (2013) Long-distance dispersal and habitat use of the butterfly Byasa impediens in a fragmented subtropical forest. Insect Conserv Divers 6:170–178CrossRefGoogle Scholar
  34. Li X, Luo Y, Yang H, Yang Q, Settele J, Schweiger O (2016) On the ecology and conservation of Sericinus montelus (Lepidoptera: Papilionidae)—its threats in Xiaolongshan forests area (China). PLoS ONE 11:1–18Google Scholar
  35. Masaki S (1967) Geographic variation and climatic adaptation in a field cricket (Orthoptera: Gryllidae). Evolution 21(4):725–741PubMedCrossRefPubMedCentralGoogle Scholar
  36. Nazari V, Sperling FAH (2007) Mitochondrial DNA divergence and phylogeography in western Palaearctic Parnassiinae (Lepidoptera: Papilionidae): how many species are there? Insect Syst Evol 38(2):123–138Google Scholar
  37. Nazari V, Evgueni VZ, Sperling FAH (2007) Phylogeny, historical biogeography and taxonomic ranking of Parnassiinae (Lepidoptera, Papilionidae) based on morphology and seven genes. Mol Phylogenet Evol 42:131–156PubMedCrossRefGoogle Scholar
  38. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  39. Sands D (2008) Conserving the Richmond birdwing butterfly over two decades: where to next? Ecol Manag Restor 9(1):4–16CrossRefGoogle Scholar
  40. Schultz CB, Crone EC (2005) Patch size and connectivity thresholds for butterfly habitat restoration. Conserv Biol 19(3):887–896CrossRefGoogle Scholar
  41. Sorimachi Y (1994) Geographical and individual variations of Bhutanitis thaidina. Apollo 3:77–87 (in Japanese) Google Scholar
  42. Sternburg JG, Waldbauer GP (1978) Phenological adaptations in diapause termination by Cecropia from different latitudes. Entomol Exp Appl 23(1):48–54CrossRefGoogle Scholar
  43. Studley J (1999) Forests and environmental degradation in SW China. Int For Rev 1(4):260–265Google Scholar
  44. Venables WN, Brian DR (2002) Modern applied statistics with S-PLUS. Springer, New York, pp 301–325CrossRefGoogle Scholar
  45. Wang Z, Huang Y, Luo X, Qin K, Merz R, Zhou S (2018) Habitat monitoring of an endangered Asian butterfly, Teinopalpus aureus (Lepidoptera: Papilionidae) and change in local residents’ conservation awareness. J Insect Conserv 22:721–729CrossRefGoogle Scholar
  46. Wang Z, Huang Y, Pierce NE (2019) Radio telemetry helps record the dispersal patterns of birdwing butterflies in mountainous habitats: golden birdwing (Troides aeacus) as an example. J Insect Conserv 23:729CrossRefGoogle Scholar
  47. Wangdi S, Wangdi K, Sherub Wangdi R, Drukpa S, Harada M, Saito M, Aoki T, Yamaguchi S, Igarashi Y, Watanabe Y, Yago M (2014) Immature stages of Ludlow’s Bhutan Glory, Bhutanitis ludlowi Gabriel (Lepidoptera: Papilionidae): external morphology of last instar larvae and pupae. Butterflies (Teinopalpus) 66:40–43Google Scholar
  48. Wynter-Blyth MA (1957) Butterflies of the Indian region, 1st edn. Bombay Natural History Society, BombayGoogle Scholar
  49. Yi C, He F, He Q, Wang L (2011) The biological characteristics of Bhutanitis yulongensis Chou. Chin J Appl Entomol 48(5):1505–1508 (in Chinese) Google Scholar
  50. Yunlong (2016) Yunnan Yunlong Tianchi Guojiaji Ziran Baohuqu Gaikuang [General introduction to Yunlong Tianchi National Nature Preserve of Yunnan]. Accessed 7 Aug 2019
  51. Zhao H, Wu R, Long Y, Hu J, Yang F, Jin T, Wang J, Hu P, Wu W, Diao Y, Guo Y (2019) Individual-level performance of nature reserves in forest protection and the effects of management level and establishment age. Biol Conserv 233:23–30CrossRefGoogle Scholar
  52. Zhu L, Wu X, Peng Y (2006) Molecular phylogenetic relationships among four species of Bhutanitis (Lepidoptera, Papilionidae)based on partial COI gene sequence. Acta Zootaxonomica Sinica 31(1):25–30 (in Chinese) Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.DaliChina
  2. 2.Yunnan University School of Life SciencesKunmingChina
  3. 3.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA

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