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

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Abstract

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.

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References

  • Almada-Villela PC (1988) Checklist of fish and invertebrates listed in the CITES appendices. Nature Conservancy Council, London

    Google Scholar 

  • 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. http://www.ifoundbutterflies.org/sp/2093/Bhutanitis-ludlowi. Accessed 4 Apr 2019

  • Baldeck CA, Asner GP (2013) Estimating vegetation beta diversity from airborne imaging spectroscopy and unsupervised clustering. Remote Sens 5:2057–2071

    Article  Google Scholar 

  • Baughman JF, Murphy DD, Ehrlich PR (1988) Emergence patterns in male checkerspot butterflies: testing theory in the field. Theor Popul Biol 33(1):102–113

    Article  Google Scholar 

  • Bonebrake TC, Ponisio LC, Boggs CL, Ehrlich PR (2010) More than just indicators: a review of tropical butterfly ecology and conservation. Biol Conserv 143:1831–1841

    Article  Google Scholar 

  • 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 338–351

    Google Scholar 

  • 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 121:358–369

    Article  Google Scholar 

  • Brückmann SV, Krauss J, Steffan-Dewenter I (2010) Butterfly and plant species suffer from reduced connectivity in fragmented landscapes. J Appl Ecol 47:799–809

    Article  Google Scholar 

  • 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 65–241

    Google Scholar 

  • 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 18:561–573

    Article  Google Scholar 

  • Chou I (1992) A study on the rare butterflies of the genus Bhutanitis (Lepidoptera: Papilionidae) with descriptions of two new species. Entomotaxonomia 14(1):48–54

    Google Scholar 

  • Chou I (1994) Monograph of Chinese butterflies. Henan Scientific and Technological Publishing House, Henan (in Chinese)

    Google Scholar 

  • Collins NM, Morris MG (1985) Threatened swallowtail butterflies of the world: the IUCN red data book. IUCN, Gland

    Google Scholar 

  • 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):e707

    Article  PubMed  PubMed Central  Google Scholar 

  • Feret JB, Asner GP (2014) Mapping tropical forest canopy diversity using high-fidelity imaging spectroscopy. Ecol Appl 24:1289–1296

    Article  PubMed  Google Scholar 

  • 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 18:29–38

    Article  CAS  Google Scholar 

  • Grömping U (2006) Relative importance for linear regression in R: the package relaimpo. J Stat Softw 17(1):1–27

    Article  Google Scholar 

  • 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) 60:4–15

    Google Scholar 

  • Harrison R (1985) Barriers to gene exchange between closely related cricket species. II. Life cycle variation and temporal isolation. Evolution 39(2):244–259

    Article  PubMed  Google Scholar 

  • Hauser CL (2005) Papilionidae—revised GloBIS/GART species checklist (2nd draft). http://www.insects-online.de/frames/papilio.htm. Accessed 4 Apr 2019

  • Igarashi S (1979) A new papilionid butterfly of the genus Bhutanitis from Northern Thailand. Tyo To Ga 30(1/2):69–72

    Google Scholar 

  • Igarashi S (1989) On the life history of Bhutanitis lidderdalei Atkinson in Bhutan (Lepidoptera, Papilionidae). Tyo To Ga 40:1–21

    Google Scholar 

  • Igarashi S (2003) Life history of Bhutanitis mansfieldi in comparison of related species. Butterflies (Teinopalpus) 35:20–39

    Google Scholar 

  • Igarashi S, Fukuda H (1997) The life histories of Asian butterflies, vol 1. Tokai University Press, Tokyo

    Google Scholar 

  • Igarashi S, Harada M (2015) Sequel to “the life histories of Asian butterflies, vols I-II”. Japan

  • 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 133–137

    Chapter  Google Scholar 

  • 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):3727–3745

    Article  PubMed  Google Scholar 

  • Konig MA, Wiklund C, Ehrien J (2016) Butterfly oviposition preference is not related to larval performance on a polyploid herb. Ecol Evol 6(9):2781–2789

    Article  PubMed  PubMed Central  Google Scholar 

  • Kunte K, Sondhi S, Roy P (2019) Butterflies of India, v. 2.60. Indian Foundation for Butterflies. http://www.ifoundbutterflies.org/tx/54-Bhutanitis. Accessed 4 Apr 2019

  • 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 27:217–233

    Article  Google Scholar 

  • 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:e97910

    Article  CAS  Google Scholar 

  • 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 14:257–268

    Article  Google Scholar 

  • 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 6:170–178

    Article  Google Scholar 

  • 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 11:1–18

    Google Scholar 

  • Masaki S (1967) Geographic variation and climatic adaptation in a field cricket (Orthoptera: Gryllidae). Evolution 21(4):725–741

    Article  PubMed  Google Scholar 

  • 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):123–138

    Google Scholar 

  • 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 42:131–156

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Sands D (2008) Conserving the Richmond birdwing butterfly over two decades: where to next? Ecol Manag Restor 9(1):4–16

    Article  Google Scholar 

  • Schultz CB, Crone EC (2005) Patch size and connectivity thresholds for butterfly habitat restoration. Conserv Biol 19(3):887–896

    Article  Google Scholar 

  • Sorimachi Y (1994) Geographical and individual variations of Bhutanitis thaidina. Apollo 3:77–87 (in Japanese)

    Google Scholar 

  • Sternburg JG, Waldbauer GP (1978) Phenological adaptations in diapause termination by Cecropia from different latitudes. Entomol Exp Appl 23(1):48–54

    Article  Google Scholar 

  • Studley J (1999) Forests and environmental degradation in SW China. Int For Rev 1(4):260–265

    Google Scholar 

  • Venables WN, Brian DR (2002) Modern applied statistics with S-PLUS. Springer, New York, pp 301–325

    Book  Google Scholar 

  • 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 22:721–729

    Article  CAS  Google Scholar 

  • 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 23:729

    Article  Google Scholar 

  • 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) 66:40–43

    Google Scholar 

  • Wynter-Blyth MA (1957) Butterflies of the Indian region, 1st edn. Bombay Natural History Society, Bombay

    Google Scholar 

  • 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 

  • Yunlong (2016) Yunnan Yunlong Tianchi Guojiaji Ziran Baohuqu Gaikuang [General introduction to Yunlong Tianchi National Nature Preserve of Yunnan]. http://www.yunlongtianchi.com/portal.php?mod=view&aid=15. Accessed 7 Aug 2019

  • 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 233:23–30

    Article  Google Scholar 

  • 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 

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Acknowledgements

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.

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Zhang, Z., Jiang, Z. & Wang, Z. Habitat, life history and oviposition choice of the endangered Bhutan Glory swallowtail Bhutanitis lidderdalii (Lepidoptera: Papilionidae) in Yunnan, China. J Insect Conserv 23, 921–931 (2019). https://doi.org/10.1007/s10841-019-00176-4

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