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Potential extinction debt due to habitat loss and fragmentation in subalpine moorland ecosystems

Abstract

Habitat loss and fragmentation would often induce delayed extinction, referred to as extinction debt. Understanding potential extinction debts would allow us to reduce future extinction risk by restoring habitats or implementing conservation actions. Although growing empirical evidence has predicted extinction debts in various ecosystems exposed to direct human disturbances, potential extinction debts in natural ecosystems with minimal direct human disturbance are little studied. Ongoing climate change may cause habitat loss and fragmentation, particularly in natural ecosystems vulnerable to environmental change, potentially leading to future local extinctions. Recent climate change would lead to extended growing season caused by earlier snowmelt in spring, resulting in expansion of shrubby species and thereby habitat loss and fragmentation of mountainous moorlands. We examined the potential extinction debts of species diversity and functional diversity (FD; trait variation or multivariate trait differences within a community) in subalpine moorland ecosystems subjected to few direct human disturbances. Plant species richness for all species and for moorland specialists were primarily explained by the past kernel density of focal moorlands (a proxy for spatial clustering of moorlands around them) but not the past area of the focal moorlands, suggesting potential extinction debt in subalpine moorland ecosystems. The higher kernel density of the focal moorland in the past indicates that it was originally surrounded by more neighborhood moorlands and/or had been locally highly fragmented. Patterns in current plant species richness have been shaped by the historical spatial configuration of moorlands, which have disappeared over time. In contrast, we found no significant relationships between the FD and historical and current landscape variables depicting each moorland. The prevalence of trait convergence might result in a less sensitive response of FD to habitat loss and fragmentation compared to that of species richness. Our finding has an important implication that climate change induced by human activities may threaten biodiversity in natural ecosystems through habitat loss and fragmentation.

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Data is available from the authors upon reasonable request.

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References

  1. Alofs KM, González AV, Fowler NL (2014) Local native plant diversity responds to habitat loss and fragmentation over different time spans and spatial scales. Plant Ecol 215:1139–1151. https://doi.org/10.1007/s11258-014-0372-5

    Article  Google Scholar 

  2. Bagaria G, Rodà F, Clotet M et al (2018) Contrasting habitat and landscape effects on the fitness of a long-lived grassland plant under forest encroachment: do they provide evidence for extinction debt? J Ecol 106:278–288. https://doi.org/10.1111/1365-2745.12860

    CAS  Article  Google Scholar 

  3. 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

    Article  Google Scholar 

  4. Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540. https://doi.org/10.1111/j.1654-1103.2005.tb02393.x

    Article  Google Scholar 

  5. Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445–449. https://doi.org/10.2307/1935620

    Article  Google Scholar 

  6. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  7. Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087. https://doi.org/10.1111/j.1365-2664.2011.02048.x

    Article  Google Scholar 

  8. Carmona CP, Azcárate FM, de Bello F et al (2012) Taxonomical and functional diversity turnover in Mediterranean grasslands: Interactions between grazing, habitat type and rainfall. J Appl Ecol 49:1084–1093. https://doi.org/10.1111/j.1365-2664.2012.02193.x

    Article  Google Scholar 

  9. Chapin FS III, McGuire AD, Randerson J et al (2000) Arctic and boreal ecosystems of western North America as components of the climate system. Glob Chang Biol 6(S1):211–223. https://doi.org/10.1046/j.1365-2486.2000.06022.x

    Article  Google Scholar 

  10. Cornelissen JHC, Lavorel S, Garnier E et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380. https://doi.org/10.1071/BT02124

    Article  Google Scholar 

  11. Cousins SAO, Vanhoenacker D (2011) Detection of extinction debt depends on scale and specialisation. Biol Conserv 144:782–787. https://doi.org/10.1016/j.biocon.2010.11.009

    Article  Google Scholar 

  12. Daubenmire RF (1959) Canopy coverage method of vegetation analysis. Northwest Sci 33:43–64

    Google Scholar 

  13. Daimaru H, Yasuda M (2009) Global warming and mountain wet meadows in Japan. Chikyu Kankyo 14:175–182 ((in Japanese))

    Google Scholar 

  14. Diamond JM (1972) Biogeographic kinetics: Estimation of relaxation times for avifaunas of southwest pacific islands. Proc Natl Acad Sci USA 69:3199–3203. https://doi.org/10.1073/pnas.69.11.3199

    CAS  Article  PubMed  Google Scholar 

  15. Driscoll DA (2008) The frequency of metapopulations, metacommunities and nestedness in a fragmented landscape. Oikos 117:297–309. https://doi.org/10.1111/j.2007.0030-1299.16202.x

    Article  Google Scholar 

  16. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419

    Article  Google Scholar 

  17. Foley JA, Barford C, Coe MT et al (2005) Global consequences of land use. Science 309:570–574. https://doi.org/10.1126/science.1111772

    CAS  Article  PubMed  Google Scholar 

  18. Geospatial Information Authority of Japan (2000) The reports of changes in wetland area in Japan. https://www.gsi.go.jp/kankyochiri/shicchimenseki2.html. Accessed 8 Jan 2020.

  19. González-Varo JP, Albaladejo RG, Aizen MA et al (2015) Extinction debt of a common shrub in a fragmented landscape. J Appl Ecol 52:580–589. https://doi.org/10.1111/1365-2664.12424

    Article  Google Scholar 

  20. Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195

    Article  Google Scholar 

  21. Gorham E, Bayley SE, Schindler DW (1984) Ecological effects of acid deposition upon peatlands: a neglected field in “acid-rain” research. Can J Fish Aquat Sci 41:1256–1268

    CAS  Article  Google Scholar 

  22. Gotelli NJ, McCabe DJ (2002) Species co-occurrence: a meta-analysis of J.M. Diamond’s assembly rules model. Ecology 83:2091–2096. https://doi.org/10.1890/0012-9658(2002)083[2091:SCOAMA]2.0.CO;2

    Article  Google Scholar 

  23. Hájková P, Hájek M, Apostolova I (2006) Diversity of wetland vegetation in the Bulgarian high mountains, main gradients and context-dependence of the pH role. Plant Ecol 184:111–130. https://doi.org/10.1007/s11258-005-9056-5

    Article  Google Scholar 

  24. Hanski I, Ovaskainen O (2002) Extinction debt at extinction threshold. Conserv Biol 16:666–673. https://doi.org/10.1046/j.1523-1739.2002.00342.x

    Article  Google Scholar 

  25. Ibanez I, Katz DSW, Peltier D et al (2014) Assessing the integrated effects of landscape fragmentation on plants and plant communities: the challenge of multiprocess–multiresponse dynamics. J Ecol 102:882–895. https://doi.org/10.1111/1365-2745.12223

    Article  Google Scholar 

  26. Jamin A, Peintinger M, Gimmi U et al (2020) Evidence for a possible extinction debt in Swiss wetland specialist plants. Ecol Evol 10:1–14. https://doi.org/10.1002/ece3.5980

    Article  Google Scholar 

  27. Kamiyama C, Oikawa S, Kubo T, Hikosaka K (2010) Light interception in species with different functional groups coexisting in moorland plant communities. Oecologia 164:591–599. https://doi.org/10.1007/s00442-010-1674-5

    Article  PubMed  Google Scholar 

  28. Keith DA, Rodoreda S, Bedward M (2010) Decadal change in wetland–woodland boundaries during the late 20th century reflects climatic trends. Global Change Biol 16:2300–2306. https://doi.org/10.1111/j.1365-2486.2009.02072.x

    Article  Google Scholar 

  29. Koyanagi T, Kusumoto Y, Yamamoto S et al (2009) Historical impacts on linear habitats: the present distribution of grassland species in forest-edge vegetation. Biol Conserv 142:1674–1684. https://doi.org/10.1016/j.biocon.2009.03.002

    Article  Google Scholar 

  30. Krause B, Culmsee H, Wesche K, Leuschner C (2015) Historical and recent fragmentation of temperate floodplain grasslands: do patch size and distance affect the richness of characteristic wet meadow plant species? Folia Geobot 50:253–266. https://doi.org/10.1007/s12224-015-9220-1

    Article  Google Scholar 

  31. Krauss J, Bommarco R, Guardiola M et al (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605. https://doi.org/10.1111/j.1461-0248.2010.01457.x

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kudo G, Kawai Y, Amagai Y, Winkler DE (2017) Degradation and recovery of an alpine plant community: experimental removal of an encroaching dwarf bamboo. Alp Botany 127:75–83

    Article  Google Scholar 

  33. Kuussaari M, Bommarco R, Heikkinen RK et al (2009) Extinction debt: a challenge for biodiversity conservation. Trends Ecol Evol 24:564–571. https://doi.org/10.1016/j.tree.2009.04.011

    Article  PubMed  Google Scholar 

  34. Laliberté E, Legendre P, Shipley B (2014) Package ‘FD’. Retrieved April 14th, 2020.

  35. Lavorel S, Grigulis K, Lamarque P et al (2011) Using plant functional traits to understand the landscape distribution of multiple ecosystem services. J Ecol 99:135–147. https://doi.org/10.1111/j.1365-2745.2010.01753.x

    Article  Google Scholar 

  36. Lindborg R, Eriksson O (2004) Historical landscape connectivity affects present plant species diversity. Ecol Soc Am 85:1840–1845. https://doi.org/10.1890/04-0367

    Article  Google Scholar 

  37. Limpens J, Berendse F, Blodau C et al (2008) Peatlands and the carbon cycle: from local processes to global implications – a synthesis. Biogeosciences 5:1475–1491

    CAS  Article  Google Scholar 

  38. Muraoka H, Takakura S (1988) Explanatory text of the geological map of the Hakkôda Geothermal area. Miscellaneous Map Series (No. 21–4), Geological Survey of Japan, Tsukuba, 27 p (in Japanese).

  39. Nekola JC (2004) Vascular plant compositional gradients within and between Iowa fens. J Veg Sci 15:771–780. https://doi.org/10.1111/j.1654-1103.2004.tb02320.x

    Article  Google Scholar 

  40. Noh J, Echeverría C, Pauchard A, Cuenca P (2019) Extinction debt in a biodiversity hotspot: the case of the Chilean Winter Rainfall-Valdivian Forests. Landsc Ecol Eng 15:1–12. https://doi.org/10.1007/s11355-018-0352-3

    Article  Google Scholar 

  41. Olsen SL, Evju M, Endrestøl A (2018) Fragmentation in calcareous grasslands: species specialization matters. Biodivers Conserv 27:2329–2361. https://doi.org/10.1007/s10531-018-1540-z7,2329-2361

    Article  Google Scholar 

  42. Otsu C, Iijima H, Nagaike T, Hoshino Y (2017) Evidence of extinction debt through the survival and colonization of each species in semi-natural grasslands. J Veg Sci 28:464–474. https://doi.org/10.1111/jvs.12514

    Article  Google Scholar 

  43. Pakeman RJ, Lennon JJ, Brooker RW (2011) Trait assembly in plant assemblages and its modulation by productivity and disturbance. Oecologia 167:209–218

    Article  Google Scholar 

  44. Parducci L, Bennett KD, Ficetola GF et al (2017) Ancient plant DNA in lake sediments. New Phytol 214:924–942

    CAS  Article  Google Scholar 

  45. Pavoine S, Vallet J, Dufour A-B et al (2009) On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118:391–402. https://doi.org/10.1111/j.1600-0706.2009.16668.x

    Article  Google Scholar 

  46. Pérez-Harguindeguy N, Díaz S, Garnier E et al (2013) New handbook for standardized measurement of plant functional traits worldwide. Aust J Bot 61:167–234. https://doi.org/10.1071/BT12225

    Article  Google Scholar 

  47. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758. https://doi.org/10.1111/j.1461-0248.2006.00924.x

    Article  PubMed  Google Scholar 

  48. R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  49. Rao RC (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 21:24–43. https://doi.org/10.1016/0040-5809(82)90004-1

    Article  Google Scholar 

  50. Ramsar Convention Bureau (2002) What Is the Ramsar Convention on Wetlands? Ramsar Information Paper no. 2. Ramsar Convention Bureau, Gland. https://www.ramsar.org/sites/default/files/documents/library/info2007-02-e.pdf. Accessed 8 Jan 2020.

  51. Rybicki J, Hanski I (2013) Species-area relationships and extinctions caused by habitat loss and fragmentation. Ecol Lett 16:27–38. https://doi.org/10.1111/ele.12065

    Article  PubMed  Google Scholar 

  52. Sasaki T, Katabuchi M, Kamiyama C et al (2013) Variations in species composition of moorland plant communities along environmental gradients within a subalpine zone in northern Japan. Wetlands 33:269–277. https://doi.org/10.1007/s13157-013-0380-6

    Article  Google Scholar 

  53. Sasaki T, Katabuchi M, Kamiyama C et al (2014) Vulnerability of moorland plant communities to environmental change: Consequences of realistic species loss on functional diversity. J Appl Ecol 51:299–308. https://doi.org/10.1111/1365-2664.12192

    Article  Google Scholar 

  54. Sasaki T, Katabuchi M, Kamiyama C et al (2012) Nestedness and niche-based species loss in moorland plant communities. Oikos 121:1783–1790. https://doi.org/10.1111/j.1600-0706.2012.20152.x

    Article  Google Scholar 

  55. Sasaki T, Okubo S, Okayasu T et al (2009) Two-phase functional redundancy in plant communities along a grazing gradient in Mongolian rangelands. Ecology 90:2598–2608. https://doi.org/10.1890/08-1850.1

    Article  PubMed  Google Scholar 

  56. Satake Y, Hara H, Watari S, Tominari T (eds) (1989) Wild flowers of Japan: woody plants. Heibonsha, Tokyo, Japan ((in Japanese))

    Google Scholar 

  57. Satake Y, Ohwi J, Kitamura S, Watari S, Tominari T (eds) (1982) Wild flowers of Japan: herbaceous plants. Heibonsha, Tokyo, Japan ((in Japanese))

    Google Scholar 

  58. Semper-Pascual A, Macchi L, Sabatini FM et al (2018) Mapping extinction debt highlights conservation opportunities for birds and mammals in the South American Chaco. J Appl Ecol 55:1218–1229. https://doi.org/10.1111/1365-2664.13074

    Article  Google Scholar 

  59. Sofaer HR, Skagen SK, Barsugli JJ et al (2016) Projected wetland densities under climate change: habitat loss but little geographic shift in conservation strategy. Ecol Appl 26:1677–1692. https://doi.org/10.1890/15-0750.1

    Article  PubMed  Google Scholar 

  60. 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

    Article  Google Scholar 

  61. Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66. https://doi.org/10.1038/371065a0

    Article  Google Scholar 

  62. Vitt DH, Chee W (1990) The relationship of vegetation to surface water chemistry and peat chemistry in fens of Alberta, Canada. Vegetatio 89:87–106. https://doi.org/10.1007/BF00032163

    Article  Google Scholar 

  63. Wearn OR, Reuman DC, Ewers RM (2012) Extinction debt and windows of conservation opportunity in the Brazilian Amazon. Science 337:228–232. https://doi.org/10.1126/science.1219013

    CAS  Article  PubMed  Google Scholar 

  64. Wheeler BD, Proctor MCF (2000) Ecological gradients, subdivisions and terminology of north-west European mires. J Ecol 88:187–203. https://doi.org/10.1046/j.1365-2745.2000.00455.x

    Article  Google Scholar 

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Acknowledgements

We thank our laboratory members for helping with field work, especially Yuki Iwachido, Misa Nambu, Issei Nishimura and Yutaro Yoshitake. We also thank Koji Yonekura for advice on species identification. This work was funded by Grant-in-Aid for Scientific Research B (no.18H02221 and no. 20H04380) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Funding

This work was funded by a Grant-in-Aid for Scientific Research B (nos. 18H02221 and 20H04380) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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D.M and T.S conceived and designed the study. All authors collected the data. D.M. analyzed the data. D.M and T.S wrote the first draft of the manuscript. All authors contributed to the revisions.

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Correspondence to Takehiro Sasaki.

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Makishima, D., Sutou, R., Goto, A. et al. Potential extinction debt due to habitat loss and fragmentation in subalpine moorland ecosystems. Plant Ecol 222, 445–457 (2021). https://doi.org/10.1007/s11258-021-01118-4

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Keywords

  • Biodiversity loss
  • Functional diversity
  • Kernel density
  • Habitat loss
  • Habitat fragmentation
  • Historical landscape