Advertisement

Journal of Insect Conservation

, Volume 23, Issue 5–6, pp 857–871 | Cite as

Entire-area spring burning versus abandonment in grasslands: butterfly responses associated with hibernating traits

  • Atsushi OhwakiEmail author
ORIGINAL PAPER

Abstract

Entire-area spring burning is a common practice in many grasslands. Although there are many studies on the effects of entire-area spring burning on insects, the underlying mechanism of insect response is not well known. Herbivorous insect responses to spring burning are expected to be related to hibernating traits and grassland quality (host and nectar plants). I surveyed butterfly assemblages and vegetation characteristics (e.g., nectar flower occurrence, host plant richness, vegetation height, and vegetation coverage) as parameters of grassland quality for butterflies over 21 transects in 3 burned and 3 abandoned grasslands. Butterfly species were classified based on their hibernating traits, with a focus on endangered and grassland species. Although grassland quality as measured by nectar resources and host plants did not differ between the abandoned and burned grasslands, butterfly richness and abundance were lower in the burned grasslands. Each grassland, particularly two burned grasslands, supported a lower number of Red List grassland species, considering the presence of their host plants. Butterfly richness and abundance exhibited a unimodal response to vegetation height and were lower in burned grasslands; however, they were not related to other variables. Species associated with burned grasslands hibernated belowground or on the surface in sparse vegetation, whereas species associated with abandoned grasslands hibernated on the surface or aboveground. Therefore, although burning is an effective method to halt grassland decline, entire-area spring burning is detrimental to grassland butterfly species. Rotational patch fire and grassland restoration would be required to maintain grassland butterfly diversity.

Keywords

Biodiversity Fire Management Overwintering Temperate Japan Vegetation height 

Notes

Acknowledgements

I thank Saki Maeda for assistance in the field. I am also grateful to Sho-ichi Hayami, Masahiko Kitahara, and Kyohei Watanabe for providing old butterfly data resources and Saki Maeda and Eri Katsumata for data organization. Comments from two anonymous reviewers greatly help to improve the manuscript. I also thank the local land owners and managers for permission to conduct the research and teaching me the previous grassland management. This study was supported by JSPS KAKENHI Grant Number 16K07800.

Compliance with ethical standards

Conflict of interest

The author declares that there are no conflicts of interest.

Ethical approval

The survey was performed based on observations, without damaging any butterflies, including endangered species.

Supplementary material

10841_2019_181_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 23 kb)
10841_2019_181_MOESM2_ESM.docx (15 kb)
Supplementary material 2 (DOCX 15 kb)
10841_2019_181_MOESM3_ESM.docx (27 kb)
Supplementary material 3 (DOCX 28 kb)

References

  1. Andersen A, Simcox DJ, Thomas JA, Nash DR (2014) Assessing reintroduction schemes by comparing genetic diversity of reintroduced and source populations: a case study of the globally threatened large blue butterfly (Maculinea arion). Biol Conserv 175:34–41.  https://doi.org/10.1016/j.biocon.2014.04.009 CrossRefGoogle Scholar
  2. Babai D, Molnár Z (2014) Small-scale traditional management of highly species-rich grasslands in the Carpathians. Agric Ecosyst Environ 182:123–130.  https://doi.org/10.1016/j.agee.2013.08.018 CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48.  https://doi.org/10.18637/jss.v067.i01 CrossRefGoogle Scholar
  4. Bommarco R, Lindborg R, Marini L, Öckinger E (2014) Extinction debt for plants and flower-visiting insects in landscapes with contrasting land use history. Divers Distrib 20:591–599.  https://doi.org/10.1111/ddi.12187 CrossRefGoogle Scholar
  5. Bond WJ, Keeley JE (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol Evol 20:387–394.  https://doi.org/10.1016/j.tree.2005.04.025 CrossRefPubMedGoogle Scholar
  6. Bond WJ, Woodward FI, Midgley GF (2005) The global distribution of ecosystems in a world without fire. New Phytol 165:525–538.  https://doi.org/10.1111/j.1469-8137.2004.01252.x CrossRefPubMedGoogle Scholar
  7. Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New YorkCrossRefGoogle Scholar
  8. Branson DH, Vermeire LT (2007) Grasshopper egg mortality mediated by oviposition tactics and fire intensity. Ecol Entomol 32:128–134.  https://doi.org/10.1111/j.1365-2311.2006.00847.x CrossRefGoogle Scholar
  9. Branson DH, Vermeire LT (2013) Heat dosage and oviposition depth influence egg mortality of two common rangeland grasshopper species. Rangel Ecol Manag 66:110–113.  https://doi.org/10.2111/REM-D-11-00187.1 CrossRefGoogle Scholar
  10. Choi S, Kim S (2012) The past and current status of endangered butterflies in Korea. Entomol Sci 15:1–12.  https://doi.org/10.1111/j.1479-8298.2011.00478.x CrossRefGoogle Scholar
  11. Collins SL (2000) Disturbance frequency and community stability in native tallgrass prairie. Am Nat 155:31–325CrossRefGoogle Scholar
  12. Cook WM, Holt RD (2006) Fire frequency and mosaic burning effects on a tallgrass prairie ground beetle assemblage. Biodivers Conserv 15:2301–2323.  https://doi.org/10.1007/s10531-004-8227-3 CrossRefGoogle Scholar
  13. Crk T, Uriarte M, Corsi F, Flynn D (2009) Forest recovery in a tropical landscape: what is the relative importance of biophysical, socioeconomic, and landscape variables? Landsc Ecol 24:629–642.  https://doi.org/10.1007/s10980-009-9338-8 CrossRefGoogle Scholar
  14. De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574.  https://doi.org/10.1890/08-1823.1 CrossRefGoogle Scholar
  15. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366.  https://doi.org/10.1890/0012-9615(1997)067%5b0345:saaist%5d2.0.co;2 CrossRefGoogle Scholar
  16. Evans EW (1984) Fire as a natural disturbance to grasshopper assemblages of tallgrass prairie. Oikos 43:9–16CrossRefGoogle Scholar
  17. Fay PA (2003) Insect diversity in two burned and grazed grasslands. Environ Entomol 32:1099–1104CrossRefGoogle Scholar
  18. Feurdean A, Ruprecht E, Molnár Z et al (2018) Biodiversity-rich European grasslands: ancient, forgotten ecosystems. Biol Conserv 228:224–232.  https://doi.org/10.1016/j.biocon.2018.09.022 CrossRefGoogle Scholar
  19. Fukuda H, Hama E, Kuzuya T et al (1982, 1983, 1984a, 1984b) The life histories of butterflies in Japan, vols I, II, III, and IV. Hoikusha, Osaka (in Japanese) Google Scholar
  20. Habel JC, Dengler J, Janišová M et al (2013) European grassland ecosystems: threatened hotspots of biodiversity. Biodivers Conserv 22:2131–2138.  https://doi.org/10.1007/s10531-013-0537-x CrossRefGoogle Scholar
  21. Hartley MK, Rogers WE, Siemann E, Grace J (2007) Responses of prairie arthropod communities to fire and fertilizer: balancing plant and arthropod conservation. Am Mid Nat 157:92–105.  https://doi.org/10.1674/0003-0031(2007)157%5b92:ropact%5d2.0.co;2 CrossRefGoogle Scholar
  22. Henderson RA, Meunier J, Holoubek NS (2018) Disentangling effects of fire, habitat, and climate on an endangered prairie-specialist butterfly. Biol Conserv 218:41–48.  https://doi.org/10.1016/j.biocon.2017.10.034 CrossRefGoogle Scholar
  23. Hiura I (1971) An analysis of butterfly fauna of Japan from the standpoint of historical biogeography. Spec Bull Lep Soc Jpn 5:73–88 (in Japanese) Google Scholar
  24. Japan Butterfly Conservation Society (2012) Field guide to the butterflies of Japan. Seibundo-Shinkosha, Tokyo (in Japanese) Google Scholar
  25. Joern A (2005) Disturbance by fire frequency and bison grazing modulate grasshopper assemblages in tallgrass prairie. Ecology 86:861–873.  https://doi.org/10.1890/04-0135 CrossRefGoogle Scholar
  26. Jonas JL, Joern A (2007) Grasshopper (Orthoptera: Acrididae) communities respond to fire, bison grazing and weather in North American tallgrass prairie: a long-term study. Oecologia 153:699–711.  https://doi.org/10.1007/s00442-007-0761-8 CrossRefPubMedGoogle Scholar
  27. Kahmen S, Poschlod P, Schreiber K-F (2002) Conservation management of calcareous grasslands. Changes in plant species composition and response of functional traits during 25 years. Biol Conserv 104:319–328.  https://doi.org/10.1016/S0006-3207(01)00197-5 CrossRefGoogle Scholar
  28. Kitahara M (2000) Food resource usage patterns of adult butterfly communities in woodland habitats at the northern foot of Mt. Fuji, central Japan. Jpn J Environ Entomol Zool 11:61–81 (in Japanese) Google Scholar
  29. Köhler B, Gigon A, Edwards PJ et al (2005) Changes in the species composition and conservation value of limestone grasslands in Northern Switzerland after 22 years of contrasting managements. Perspect Plant Ecol Evol Syst 7:51–67.  https://doi.org/10.1016/j.ppees.2004.11.003 CrossRefGoogle Scholar
  30. Koyama A, Koyanagi TF, Akasaka M et al (2017) Combined burning and mowing for restoration of abandoned semi-natural grasslands. Appl Veg Sci 20:40–49.  https://doi.org/10.1111/avsc.12268 CrossRefGoogle Scholar
  31. Kral KC, Limb RF, Harmon JP, Hovick TJ (2017) Arthropods and fire: previous research shaping future conservation. Rangel Ecol Manag 70:589–598.  https://doi.org/10.1016/j.rama.2017.03.006 CrossRefGoogle Scholar
  32. Kyser GB, DiTomaso JM (2002) Instability in a grassland community after the control of yellow starthistle (Centaurea solstitialis) with prescribed burning. Weed Sci 50:648–657.  https://doi.org/10.1614/0043-1745 CrossRefGoogle Scholar
  33. Leys BA, Marlon JR, Umbanhowar C, Vannière B (2018) Global fire history of grassland biomes. Ecol Evol 8:8831–8852.  https://doi.org/10.1002/ece3.4394 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mehta CR, Patel NR (1983) A network algorithm for performing fisher’s exact test in r × c contingency tables. J Am Stat Assoc 78:427–434Google Scholar
  35. Milberg P, Akoto B, Bergman K-O et al (2014) Is spring burning a viable management tool for species-rich grasslands? Appl Veg Sci 17:429–441.  https://doi.org/10.1111/avsc.12091 CrossRefGoogle Scholar
  36. Ministry of the Environment, Japan (2017) The 2017 Japanese Red List. Ministry of the Environment, Tokyo (in Japanese) Google Scholar
  37. Moranz RA, Fuhlendorf SD, Engle DM (2014) Making sense of a prairie butterfly paradox: the effects of grazing, time since fire, and sampling period on regal fritillary abundance. Biol Conserv 173:32–41.  https://doi.org/10.1016/j.biocon.2014.03.003 CrossRefGoogle Scholar
  38. Moyes AB, Witter MS, Gamon JA (2005) Restoration of native perennials in a California annual grassland after prescribed spring burning and solarization. Restor Ecol 13:659–666.  https://doi.org/10.1111/j.1526-100X.2005.00084.x CrossRefGoogle Scholar
  39. Nagamori T, Nagamori H, Shibata T, Kuroda S, Ishiguro M (2016) The complete guide to butterflies of Hokkaido. Hokkaido University Press, Sapporo (in Japanese) Google Scholar
  40. Nagata YK, Ushimaru A (2016) Traditional burning and mowing practices support high grassland plant diversity by providing intermediate levels of vegetation height and soil pH. Appl Veg Sci 19:567–577.  https://doi.org/10.1111/avsc.12252 CrossRefGoogle Scholar
  41. Nakahama N, Isagi Y (2018) Recent transitions in genetic diversity and structure in the endangered semi-natural grassland butterfly, Melitaea protomedia, in Japan. Insect Conserv Divers 11:330–340.  https://doi.org/10.1111/icad.12280 CrossRefGoogle Scholar
  42. Nakahama N, Uchida K, Ushimaru A, Isagi Y (2018) Historical changes in grassland area determined the demography of semi-natural grassland butterflies in Japan. Heredity 121:151–168.  https://doi.org/10.1038/s41437-018-0057-2 CrossRefGoogle Scholar
  43. Nakamura Y (2011) Conservation of butterflies in Japan: status, actions and strategy. J Insect Conserv 15:5–22.  https://doi.org/10.1007/s10841-010-9299-x CrossRefGoogle Scholar
  44. Ogura J (2012) History of radically changed vegetation of Japan. Kokon-Shoin, Tokyo (in Japanese) Google Scholar
  45. Ohwaki A (2011) Butterfly assemblage in a snowy temperate satoyama area in Tokamachi City, Niigata Prefecture. Lepid Sci 62:64–74 (in Japanese) Google Scholar
  46. Ohwaki A (2018) How should we view temperate semi-natural grasslands? Insights from butterflies in Japan. Glob Ecol Conserv 16:e00482.  https://doi.org/10.1016/j.gecco.2018.e00482 CrossRefGoogle Scholar
  47. Ohwaki A, Koyanagi TF, Maeda S (2018) Evaluating forest clear-cuts as alternative grassland habitats for plants and butterflies. For Ecol Manag 430:337–345.  https://doi.org/10.1016/j.foreco.2018.08.032 CrossRefGoogle Scholar
  48. Oksanen J, Blanchet FG, Kindt R et al (2015) Vegan: community ecology package. R package version 2.3-1. http://CRAN.R-project.org/package=vegan. Accessed 28 Sept 2019
  49. Panzer R (2002) Compatibility of prescribed burning with the conservation of insects in small, isolated prairie peserves. Conserv Biol 16:1296–1307.  https://doi.org/10.1046/j.1523-1739.2002.01077.x CrossRefGoogle Scholar
  50. Panzer R, Schwartz M (2000) Effects of management burning on prairie insect species richness within a system of small, highly fragmented reserves. Biol Conserv 96:363–369.  https://doi.org/10.1016/S0006-3207(00)00065-3 CrossRefGoogle Scholar
  51. Pärtel M, Bruun HH, Sammul M (2005) Biodiversity in temperate European grasslands: origin and conservation. In: Lillak R, Viiralt R, Linke A, Geherman V (eds) Integrating efficient grassland farming and biodiversity. Greif Printhouse, Tartu, pp 1–14Google Scholar
  52. Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation. Chapman & Hall, LondonGoogle Scholar
  53. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  54. Schmitt T, Rákosy L (2007) Changes of traditional agrarian landscapes and their conservation implications: a case study of butterflies in Romania. Divers Distrib 13:855–862.  https://doi.org/10.1111/j.1472-4642.2007.00347.x CrossRefGoogle Scholar
  55. Shirozu T (2006) The butterflies of Japan in color. Gakken, Tokyo (in Japanese) Google Scholar
  56. Soga M, Koike S (2013) Mapping the potential extinction debt of butterflies in a modern city: implications for conservation priorities in urban landscapes. Anim Conserv 16:1–11.  https://doi.org/10.1111/j.1469-1795.2012.00572.x CrossRefGoogle Scholar
  57. Svenning J-C (2002) A review of natural vegetation openness in north-western Europe. Biol Conserv 104:133–148.  https://doi.org/10.1016/S0006-3207(01)00162-8 CrossRefGoogle Scholar
  58. Swengel AB (1996) Effects of fire and hay management on abundance of prairie butterflies. Biol Conserv 76:73–85CrossRefGoogle Scholar
  59. Swengel AB (2001) A literature review of insect responses to fire, compared to other conservation managements of open habitat. Biodivers Conserv 10:1141–1169.  https://doi.org/10.1023/A:1016683807033 CrossRefGoogle Scholar
  60. Swengel AB, Swengel SR (2001) Effects of prairie and barrens management on butterfly faunal composition. Biodivers Conserv 10:1757–1785.  https://doi.org/10.1023/A:1012051510584 CrossRefGoogle Scholar
  61. Swengel SR, Schlicht D, Olsen F, Swengel AB (2011) Declines of prairie butterflies in the midwestern USA. J Insect Conserv 15:327–339.  https://doi.org/10.1007/s10841-010-9323-1 CrossRefGoogle Scholar
  62. Thomas JA (1995) The ecology and conservation of Maculinea arion and other European species of large blue butterfly. In: Pullin AS (ed) Ecology and conservation of butterflies. Chapman & Hall, London, pp 180–197CrossRefGoogle Scholar
  63. Uchida K, Takahashi S, Shinohara T, Ushimaru A (2016) Threatened herbivorous insects maintained by long-term traditional management practices in semi-natural grasslands. Agric Ecosyst Environ 221:156–162.  https://doi.org/10.1016/j.agee.2016.01.036 CrossRefGoogle Scholar
  64. Ushimaru A, Uchida K, Suka T (2018) Grassland biodiversity in Japan: threats, management and conservation. In: Squires V, Dengler J, Feng H, Hua L (eds) Grassland management: problems and prospects. CRC Press, Boca RatonGoogle Scholar
  65. Valkó O, Török P, Deák B, Tóthmérész B (2014) Review: Prospects and limitations of prescribed burning as a management tool in European grasslands. Basic Appl Ecol 15:26–33.  https://doi.org/10.1016/j.baae.2013.11.002 CrossRefGoogle Scholar
  66. Van Langevelde F, Wynhoff I (2009) What limits the spread of two congeneric butterfly species after their reintroduction: quality or spatial arrangement of habitat? Anim Conserv 12:540–548.  https://doi.org/10.1111/j.1469-1795.2009.00281.x CrossRefGoogle Scholar
  67. van Swaay CAM (2002) The importance of calcareous grasslands for butterflies in Europe. Biol Conserv 104:315–318.  https://doi.org/10.1016/S0006-3207(01)00196-3 CrossRefGoogle Scholar
  68. van Swaay CAM, Warren MS, Loïs G (2006) Biotope use and trends of European butterflies. J Insect Conserv 10:189–209.  https://doi.org/10.1007/s10841-006-6293-4 CrossRefGoogle Scholar
  69. Vera FWM (2000) Grazing ecology and forest history. CABI Publishing, WallingfordCrossRefGoogle Scholar
  70. Vogel JA, Debinski DM, Koford RR, Miller JR (2007) Butterfly responses to prairie restoration through fire and grazing. Biol Conserv 140:78–90CrossRefGoogle Scholar
  71. Vogel JA, Koford RR, Debinski DM (2010) Direct and indirect responses of tallgrass prairie butterflies to prescribed burning. J Insect Conserv 14:663–677.  https://doi.org/10.1007/s10841-010-9295-1 CrossRefGoogle Scholar
  72. Warren SD, Scifres CJ, Teel PD (1987) Response of grassland arthropods to burning: a review. Agric Ecosyst Environ 19:105–130.  https://doi.org/10.1016/0167-8809(87)90012-0 CrossRefGoogle Scholar
  73. Wikström L, Milberg P, Bergman K-O (2009) Monitoring of butterflies in semi-natural grasslands: diurnal variation and weather effects. J Insect Conserv 13:203–211.  https://doi.org/10.1007/s10841-008-9144-7 CrossRefGoogle Scholar
  74. Wu C, Wang M, Lu C et al (2018) Climate-induced fire regimes in the Russian biodiversity hotspots. Glob Ecol Conserv 16:e00495.  https://doi.org/10.1016/j.gecco.2018.e00495 CrossRefGoogle Scholar
  75. Zhang X, Miyashita T (2018) Effects of local and landscape factors on the abundance of an endangered multivoltine butterfly at riverbanks. Entomol Sci 21:133–141.  https://doi.org/10.1111/ens.12291 CrossRefGoogle Scholar
  76. Zuur AE, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New YorkCrossRefGoogle Scholar
  77. Zuur AE, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Division of Natural Environmental Science, Mount Fuji Research Institute (MFRI)Yamanashi Prefectural GovernmentFujiyoshidaJapan

Personalised recommendations