A global synthesis of biodiversity responses to glacier retreat

Matters Arising to this article was published on 30 March 2020

Abstract

Glaciers cover about 10% of the Earth’s land area but they are retreating rapidly and many will disappear within decades. Glacier retreat is a worldwide phenomenon increasing the threat to water resources, biodiversity and associated ecosystem services for hundreds of millions of people, mostly in developing countries. Our understanding of the ecological consequences of glacier retreat has improved significantly in the past decade, but we still lack a comprehensive framework for predicting biodiversity responses to glacier retreat globally, across diverse habitats and taxa. By conducting a global meta-analysis of 234 published studies, including more than 2,100 biodiversity surveys covering marine, freshwater and terrestrial assemblages, we show here that taxon abundance and richness generally increase at lower levels of glacier influence, suggesting that diversity increases locally as glaciers retreat. However, significant response heterogeneity was observed between study sites and species: 6–11% of the studied populations, particularly in fjords, would lose out from glacier retreat. Most of the losers are specialist species, efficient dispersers, uniquely adapted to glacial conditions, whereas the winners are generalist taxa colonizing from downstream. Our global analyses also identify key geographic variables (glacier cover, isolation and melting rates, but not latitude or altitude) and species traits (body size and trophic position) likely to modulate taxon sensitivity to glacial retreat. Finally, we propose mechanistic diagrams for model development to predict biodiversity change following glacier retreat.

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Fig. 1: Global distribution of the biodiversity surveys analysed in this study.
Fig. 2: Population and community responses to the effects of glaciers in fjords, freshwaters and forefields.
Fig. 3: Population responses to glacier influence in fjords, freshwaters and glacier forefields by taxonomic group, trophic level and organism size.
Fig. 4: Physical forcing of biological processes in the three glacier-influenced ecosystems.

Data availability

Data are available at https://doi.org/10.7910/DVN/ZAREWT.

Code availability

Code from this study is available at https://doi.org/10.7910/DVN/ZAREWT.

References

  1. 1.

    Hock, R. et al. in IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds Pörtner, H.-O. et al.) Ch. 2 (IPCC, 2019).

  2. 2.

    Zemp, M. et al. Global glacier mass changes and their contributions to sea-level rise from 1961 to 2016. Nature 568, 382–386 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  3. 3.

    Sorg, A., Bolch, T., Stoffel, M., Solomina, O. & Beniston, M. Climate change impacts on glaciers and runoff in the Tien Shan (Central Asia). Nat. Clim. Change 2, 725–731 (2012).

    Article  Google Scholar 

  4. 4.

    Milner, A. M. et al. Glacier shrinkage driving global changes in downstream systems. Proc. Natl Acad. Sci. USA 114, 9770–9778 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  5. 5.

    Lee, J. R. et al. Climate change drives expansion of Antarctic ice-free habitat. Nature 547, 49–54 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  6. 6.

    Jacobsen, D., Milner, A. M., Brown, L. E. & Dangles, O. Biodiversity under threat in glacier-fed river systems. Nat. Clim. Change 2, 361–364 (2012).

    Article  Google Scholar 

  7. 7.

    Rabatel, A. et al. Current state of glaciers in the tropical Andes: a multi-century perspective on glacier evolution and climate change. Cryosphere 7, 81–102 (2013).

    Article  Google Scholar 

  8. 8.

    Beniston, M. et al. The European mountain cryosphere: a review of its current state, trends, and future challenges. Cryosphere 12, 759–794 (2018).

    Article  Google Scholar 

  9. 9.

    Huss, M. et al. Toward mountains without permanent snow and ice. Earth’s Future 5, 418–435 (2017).

    Article  Google Scholar 

  10. 10.

    Bell, E. M. Life at Extremes: Environments, Organisms and Strategies for Survival (CABI, 2012).

  11. 11.

    Grange, L. J. & Smith, C. R. Megafaunal communities in rapidly warming fjords along the West Antarctic Peninsula: hotspots of abundance and beta diversity. PLoS ONE 8, e77917 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  12. 12.

    Cauvy-Fraunié, S., Espinosa, R., Andino, P., Jacobsen, D. & Dangles, O. Invertebrate metacommunity structure and dynamics in an Andean glacial stream network facing climate change. PLoS ONE 10, e0136793 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  13. 13.

    Munoz, N. J., Farrell, A. P., Heath, J. W. & Neff, B. D. Adaptive potential of a Pacific salmon challenged by climate change. Nat. Clim. Change 5, 163–166 (2015).

    Article  Google Scholar 

  14. 14.

    Milner, A. M., Taylor, R. C. & Winterbourn, M. J. Longitudinal distribution of macroinvertebrates in two glacier‐fed New Zealand rivers. Freshw. Biol. 46, 1765–1775 (2001).

    Article  Google Scholar 

  15. 15.

    Ronowicz, M., Włodarska-Kowalczuk, M. & Kukliński, P. Patterns of hydroid (Cnidaria, Hydrozoa) species richness and distribution in an Arctic glaciated fjord. Polar Biol. 34, 1437–1445 (2011).

    Article  Google Scholar 

  16. 16.

    Gobbi, M., Isaia, M. & De Bernardi, F. Arthropod colonisation of a debris-covered glacier. Holocene 21, 343–349 (2011).

    Article  Google Scholar 

  17. 17.

    Giersch, J. J., Hotaling, S., Kovach, R. P., Jones, L. A. & Muhlfeld, C. C. Climate‐induced glacier and snow loss imperils alpine stream insects. Glob. Change Biol. 23, 2577–2589 (2017).

    Article  Google Scholar 

  18. 18.

    Jacobsen, D. & Dangles, O. Environmental harshness and global richness patterns in glacier‐fed streams. Glob. Ecol. Biogeogr. 21, 647–656 (2012).

    Article  Google Scholar 

  19. 19.

    Milner, A. M., Fastie, C. L., Chapin, F. S., Engstrom, D. R. & Sharman, L. C. Interactions and linkages among ecosystems during landscape evolution. BioScience 57, 237–247 (2007).

    Article  Google Scholar 

  20. 20.

    Zawierucha, K., Kolicka, M., Takeuchi, N. & Kaczmarek, Ł. What animals can live in cryoconite holes? A faunal review. J. Zool. 295, 159–169 (2015).

    Article  Google Scholar 

  21. 21.

    Cauvy-Fraunié, S. et al. Ecological responses to experimental glacier-runoff reduction in alpine rivers. Nat. Commun. 7, 12025 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  22. 22.

    Arimitsu, M. L. et al. Distribution and spawning dynamics of capelin (Mallotus villosus) in Glacier Bay, Alaska: a cold water refugium. Fish. Oceanogr. 17, 137–146 (2008).

    Article  Google Scholar 

  23. 23.

    Uehlinger, U., Robinson, C., Hieber, M. & Zah, R. The physico-chemical habitat template for periphyton in alpine glacial streams under a changing climate. Hydrobiologia 657, 107–121 (2010).

    CAS  Article  Google Scholar 

  24. 24.

    Dolezal, J. et al. Primary succession following deglaciation at Koryto Glacier Valley, Kamchatka. Arct. Antarct. Alp. Res. 40, 309–322 (2008).

    Article  Google Scholar 

  25. 25.

    Weslawski, J. & Legezynska, J. Glaciers caused zooplankton mortality? J. Plankton Res. 20, 1233–1240 (1998).

    Article  Google Scholar 

  26. 26.

    Řeháková, K., Stibal, M., Šabacká, M. & Řehák, J. Survival and colonisation potential of photoautotrophic microorganisms within a glacierised catchment on Svalbard, High Arctic. Polar Biol. 33, 737–745 (2010).

    Article  Google Scholar 

  27. 27.

    Wilhelm, L., Singer, G. A., Fasching, C., Battin, T. J. & Besemer, K. Microbial biodiversity in glacier-fed streams. ISME J. 7, 1651–1660 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. 28.

    Park, S. J. et al. Influence of deglaciation on microbial communities in marine sediments off the coast of Svalbard, Arctic Circle. Microb. Ecol. 62, 537–548 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  29. 29.

    Breen, K. & Levesque, E. Proglacial succession of biological soil crusts and vascular plants: biotic interactions in the High Arctic. Can. J. Bot. 84, 1714–1731 (2006).

    Article  Google Scholar 

  30. 30.

    Oehl, F., Schneider, D., Sieverding, E. & Burga, C. A. Succession of arbuscular mycorrhizal communities in the foreland of the retreating Morteratsch Glacier in the Central Alps. Pedobiologia 54, 321–331 (2011).

    Article  Google Scholar 

  31. 31.

    Malard, F., Lafont, M., Burgherr, P. & Ward, J. A comparison of longitudinal patterns in hyporheic and benthic oligochaete assemblages in a glacial river. Arct. Antarct. Alp. Res. 33, 457–466 (2001).

    Article  Google Scholar 

  32. 32.

    Schlegel, J. & Riesen, M. Environmental gradients and succession patterns of carabid beetles (Coleoptera: Carabidae) in an Alpine glacier retreat zone. J. Insect Conserv. 16, 657–675 (2012).

    Article  Google Scholar 

  33. 33.

    Seimon, T. A. et al. Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Glob. Change Biol. 13, 288–299 (2007).

    Article  Google Scholar 

  34. 34.

    Arendt, K. E., Nielsen, T. G., Rysgaard, S. & Tönnesson, K. Differences in plankton community structure along the Godthåbsfjord, from the Greenland Ice Sheet to offshore waters. Mar. Ecol. Prog. Ser. 401, 49–62 (2010).

    CAS  Article  Google Scholar 

  35. 35.

    Berge, J. et al. Changes in the decapod fauna of an Arctic fjord during the last 100 years (1908–2007). Polar Biol. 32, 953–961 (2009).

    Article  Google Scholar 

  36. 36.

    Błażewicz-Paszkowycz, M. & Sekulska-Nalewajko, J. Tanaidacea (Crustacea, Malacostraca) of two polar fjords: Kongsfjorden (Arctic) and Admiralty Bay (Antarctic). Polar Biol. 27, 222–230 (2004).

    Article  Google Scholar 

  37. 37.

    Carney, D., Oliver, J. S. & Armstrong, C. Sedimentation and composition of wall communities in Alaskan fjords. Polar Biol. 22, 38–49 (1999).

    Article  Google Scholar 

  38. 38.

    Day, R. H. & Nigro, D. A. Feeding ecology of Kittlitz’s and marbled murrelets in Prince William Sound, Alaska. J. Waterbirds Soc. 23, 1–14 (2000).

    Google Scholar 

  39. 39.

    De Skowronski, R. S. & Corbisier, T. N. Meiofauna distribution in Martel Inlet, King George Island (Antarctica): sediment features versus food availability. Polar Biol. 25, 126–134 (2002).

    Article  Google Scholar 

  40. 40.

    De Skowronski, R. S. et al. Distribution of microphytobenthic biomass in Martel Inlet, King George Island (Antarctica). Polar Biol. 32, 839–851 (2009).

    Article  Google Scholar 

  41. 41.

    Etherington, L. L., Hooge, P. N., Hooge, E. R. & Hill, D. F. Oceanography of Glacier Bay, Alaska: implications for biological patterns in a glacial fjord estuary. Estuar. Coasts 30, 927–944 (2007).

    Article  Google Scholar 

  42. 42.

    Fetzer, I., Lønne, O. & Pearson, T. The distribution of juvenile benthic invertebrates in an arctic glacial fjord. Polar Biol. 25, 303–315 (2002).

    Article  Google Scholar 

  43. 43.

    Gontar, V. I., Hop, H. & Voronkov, A. Y. Diversity and distribution of Bryozoa in Kongsfjorden, Svalbard. Pol. Polar Res. 22, 187–204 (2001).

    Google Scholar 

  44. 44.

    Grzelak, K. & Kotwicki, L. Meiofaunal distribution in Hornsund fjord, Spitsbergen. Polar Biol. 35, 269–280 (2012).

    Article  Google Scholar 

  45. 45.

    Hald, M. & Korsun, S. Distribution of modern benthic foraminifera from fjords of Svalhard, European Arctic. J. Foramin. Res. 27, 101–122 (1997).

    Article  Google Scholar 

  46. 46.

    Jankowska, K. & Wieczorek, P. Abundance and biomass of bacteria in two Arctic glacial fjords. Pol. Polar Res. 26, 77–84 (2005).

    Google Scholar 

  47. 47.

    Kaczmarek, H., Włodarska-Kowalczuk, M., Legezynska, J. & Zajaczkowski, M. Shallow sublittoral macrozoobenthos in Kongsfjord, west Spitsbergen, Svalbard. Pol. Polar Res. 26, 137–155 (2005).

    Google Scholar 

  48. 48.

    Keck, A., Wiktor, J., Hapter, R. & Nilsen, R. Phytoplankton assemblages related to physical gradients in an arctic, glacier-fed fjord in summer. ICES J. Mar. Sci. 56, 203–214 (1999).

    Article  Google Scholar 

  49. 49.

    Kędra, M., Włodarska-Kowalczuk, M. & Węsławski, J. M. Decadal change in macrobenthic soft-bottom community structure in a high Arctic fjord (Kongsfjorden, Svalbard). Polar Biol. 33, 1 (2010).

    Article  Google Scholar 

  50. 50.

    Kędra, M., Legeżyńska, J. & Walkusz, W. Shallow winter and summer macrofauna in a high Arctic fjord (79 N, Spitsbergen). Mar. Biodiv. 41, 425–439 (2011).

    Article  Google Scholar 

  51. 51.

    Kędra, M., Pabis, K., Gromisz, S. & Węsławski, J. M. Distribution patterns of polychaete fauna in an Arctic fjord (Hornsund, Spitsbergen). Polar Biol. 36, 1463–1472 (2013).

    Article  Google Scholar 

  52. 52.

    Kissling, M. L., Reid, M., Lukacs, P. M., Gende, S. M. & Lewis, S. B. Understanding abundance patterns of a declining seabird: implications for monitoring. Ecol. Appl. 17, 2164–2174 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  53. 53.

    Korsun, S., Pogodina, I., Forman, S. & Lubinski, D. Recent foraminifera in glaciomarine sediments from three Arctic fjords of Novaja Zemlja and Svalbard. Polar Res. 14, 15–32 (1995).

    Article  Google Scholar 

  54. 54.

    Korsun, S. & Hald, M. Modern benthic foraminifera off Novaya Zemlya tidewater glaciers, Russian Arctic. Arct. Alp. Res. 30, 61–77 (1998).

    Article  Google Scholar 

  55. 55.

    Korsun, S. & Hald, M. Seasonal dynamics of benthic foraminifera in a glacially fed fjord of Svalbard, European Arctic. J. Foramin. Res. 30, 251–271 (2000).

    Article  Google Scholar 

  56. 56.

    Kotwicki, L., Szymelfenig, M., De Troch, M. & Zajaczkowski, M. Distribution of meiofauna in Kongsfjorden, Spitsbergen. Polar Biol. 27, 661–669 (2004).

    Article  Google Scholar 

  57. 57.

    Kuklinski, P. Fauna of Bryozoa from Kongsfjorden, West Spitsbergen. Pol. Polar Res. 23, 193–206 (2002).

    Google Scholar 

  58. 58.

    Kuklinski, P., Gulliksen, B., Lønne, O. J. & Weslawski, J. M. Composition of bryozoan assemblages related to depth in Svalbard fjords and sounds. Polar Biol. 28, 619–630 (2005).

    Article  Google Scholar 

  59. 59.

    Kuklinski, P., Gulliksen, B., Lønne, O. J. & Weslawski, J. M. Substratum as a structuring influence on assemblages of Arctic bryozoans. Polar Biol. 29, 652–661 (2006).

    Article  Google Scholar 

  60. 60.

    Kwasniewski, S., Hop, H., Falk-Petersen, S. & Pedersen, G. Distribution of Calanus species in Kongsfjorden, a glacial fjord in Svalbard. J. Plankton Res. 25, 1–20 (2003).

    CAS  Article  Google Scholar 

  61. 61.

    Legeżyńska, J. et al. The malacostracan fauna of two Arctic fjords (west Spitsbergen): the diversity and distribution patterns of its pelagic and benthic components. Oceanologia 59, 541–564 (2017).

    Article  Google Scholar 

  62. 62.

    Majewski, W. Benthic foraminiferal communities: distribution and ecology in Admiralty Bay, King George Island, West Antarctica. Pol. Polar Res. 26, 159–214 (2005).

    Google Scholar 

  63. 63.

    Majewski, W. & Olempska, E. Recent ostracods from Admiralty Bay, King George Island, West Antarctica. Pol. Polar Res. 26, 13–36 (2005).

    Google Scholar 

  64. 64.

    Majewski, W., Pawlowski, J. & Zajaczkowski, M. Monothalamous foraminifera from West Spitsbergen fjords, Svalbard: a brief overview. Pol. Polar Res. 26, 269–285 (2005).

    Google Scholar 

  65. 65.

    Moon, H.-W., Hussin, W. M. R. W., Kim, H.-C. & Ahn, I.-Y. The impacts of climate change on Antarctic nearshore mega-epifaunal benthic assemblages in a glacial fjord on King George Island: responses and implications. Ecol. Ind. 57, 280–292 (2015).

    Article  Google Scholar 

  66. 66.

    Murray, C. et al. The influence of glacial melt water on bio-optical properties in two contrasting Greenlandic fjords. Estuar. Coast. Shelf Sci. 163, 72–83 (2015).

    CAS  Article  Google Scholar 

  67. 67.

    Mutschke, E. & Gorny, M. The benthic decapod fauna in the channels and fjords along the South Patagonian Icefield, Southern Chile. Sci. Mar. 63, 315–319 (1999).

    Article  Google Scholar 

  68. 68.

    Okolodkov, Y. B., Hapter, R. & Semovski, S. V. Phytoplankton in Kongsfjorden, Spitsbergen, July 1996. Sarsia 85, 345–352 (2000).

    Article  Google Scholar 

  69. 69.

    Pabis, K. & Sicinski, J. Distribution and diversity of polychaetes collected by trawling in Admiralty Bay: an Antarctic glacial fiord. Polar Biol. 33, 141–151 (2010).

    Article  Google Scholar 

  70. 70.

    Pabis, K., Sicinski, J. & Krymarys, M. Distribution patterns in the biomass of macrozoobenthic communities in Admiralty Bay (King George Island, South Shetlands, Antarctic). Polar Biol. 34, 489–500 (2011).

    Article  Google Scholar 

  71. 71.

    Pabis, K., Hara, U., Presler, P. & Sicinski, J. Structure of bryozoan communities in an Antarctic glacial fjord (Admiralty Bay, South Shetlands). Polar Biol. 37, 737–751 (2014).

    Article  Google Scholar 

  72. 72.

    Pabis, K., Kędra, M. & Gromisz, S. Distinct or similar? Soft bottom polychaete diversity in Arctic and Antarctic glacial fjords. Hydrobiologia 742, 279–294 (2015).

    CAS  Article  Google Scholar 

  73. 73.

    Pabis, K. & Sobczyk, R. Small-scale spatial variation of soft-bottom polychaete biomass in an Antarctic glacial fjord (Ezcurra Inlet, South Shetlands): comparison of sites at different levels of disturbance. Helgol. Mar. Res. 69, 113–121 (2015).

    Article  Google Scholar 

  74. 74.

    Pugh, P. J. A. & Davenport, J. Colonisation vs. disturbance: the effects of sustained ice-scouring on intertidal communities. J. Exp. Mar. Biol. Ecol. 210, 1–21 (1997).

    Article  Google Scholar 

  75. 75.

    Renaud, P. E. et al. Multidecadal stability of benthic community structure in a high-Arctic glacial fjord (van Mijenfjord, Spitsbergen). Polar Biol. 30, 295–305 (2007).

    Article  Google Scholar 

  76. 76.

    Ronowicz, M. Species diversity of Arctic gravel beach: case study for species poor habitats. Pol. Polar Res. 26, 287–297 (2005).

    Google Scholar 

  77. 77.

    Ronowicz, M., Włodarska-Kowalczuk, M. & Kuklinski, P. Factors influencing hydroids (Cnidaria: Hydrozoa) biodiversity and distribution in Arctic kelp forest. J. Mar. Biol. Assoc. UK 88, 1567–1575 (2008).

    Article  Google Scholar 

  78. 78.

    Sabbatini, A., Morigi, C., Negri, A. & Gooday, A. J. Distribution and biodiversity of stained monothalamous foraminifera from Tempelfjord, Svalbard. J. Foramin. Res. 37, 93–106 (2007).

    Article  Google Scholar 

  79. 79.

    Sejr, M. K., Włodarska-Kowalczuk, M., Legeżyńska, J. & Blicher, M. E. Macrobenthic species composition and diversity in the Godthaabsfjord system, SW Greenland. Polar Biol. 33, 421–431 (2010).

    Article  Google Scholar 

  80. 80.

    Siciński, J., Pabis, K., Jażdżewski, K., Konopacka, A. & Błażewicz-Paszkowycz, M. Macrozoobenthos of two Antarctic glacial coves: a comparison with non-disturbed bottom areas. Polar Biol. 35, 355–367 (2012).

    Article  Google Scholar 

  81. 81.

    Taggart, S., Hooge, P., Mondragon, J., Hooge, E. & Andrews, A. Living on the edge: distribution of Dungeness crab Cancer magister in a recently deglaciated fjord. Mar. Ecol. Prog. Ser. 246, 241–252 (2003).

    Article  Google Scholar 

  82. 82.

    Tikhonenkov, D. Species diversity and changes of communities of heterotrophic flagellates (protista) in response to glacial melt in King George Island, the South Shetland Islands, Antarctica. Antarct. Sci. 26, 133–144 (2014).

    Article  Google Scholar 

  83. 83.

    Urban-Malinga, B., Wiktor, J., Jabłońska, A. & Moens, T. Intertidal meiofauna of a high-latitude glacial Arctic fjord (Kongsfjorden, Svalbard) with emphasis on the structure of free-living nematode communities. Polar Biol. 28, 940–950 (2005).

    Article  Google Scholar 

  84. 84.

    Voronkov, A., Stepanjants, S. D. & Hop, H. Hydrozoan diversity on hard bottom in Kongsfjorden, Svalbard. J. Mar. Biol. Assoc. UK 90, 1337–1352 (2010).

    Article  Google Scholar 

  85. 85.

    Voronkov, A. & Hop, H. & Gulliksen, B. Diversity of hard-bottom fauna relative to environmental gradients in Kongsfjorden, Svalbard. Polar Res. 32, 11208 (2013).

    Article  Google Scholar 

  86. 86.

    Walkusz, W. et al. Seasonal and spatial changes in the zooplankton community of Kongsfjorden, Svalbard. Polar Res. 28, 254–281 (2009).

    Article  Google Scholar 

  87. 87.

    Wang, G., Guo, C., Luo, W., Cai, M. & He, J. The distribution of picoplankton and nanoplankton in Kongsfjorden, Svalbard during late summer 2006. Polar Biol. 32, 1233–1238 (2009).

    CAS  Article  Google Scholar 

  88. 88.

    Weslawski, J. M., Wiktor, J. & Kotwicki, L. Increase in biodiversity in the arctic rocky littoral, Sorkappland, Svalbard, after 20 years of climate warming. Mar. Biodiv. 40, 123–130 (2010).

    Article  Google Scholar 

  89. 89.

    Wiktor, J. & Wojciechowska, K. Differences in taxonomic composition of summer phytoplankton in two fjords of West Spitsbergen, Svalbard. Pol. Polar Res. 26, 259–268 (2005).

    Google Scholar 

  90. 90.

    Włodarska-Kowalczuk, M., Szymelfenig, M., Kotwicki, L. & Warszawy, P. Macro- and meiobenthic fauna of the Yoldiabukta glacial bay (Isfjorden, Spitsbergen). Pol. Polar Res. 20, 367–386 (1999).

    Google Scholar 

  91. 91.

    Włodarska-Kowalczuk, M. & Pearson, T. H. Soft-bottom macrobenthic faunal associations and factors affecting species distributions in an Arctic glacial fjord (Kongsfjord, Spitsbergen). Polar Biol. 27, 155–167 (2004).

    Article  Google Scholar 

  92. 92.

    Włodarska-Kowalczuk, M., Pearson, T. H. & Kendall, M. A. Benthic response to chronic natural physical disturbance by glacial sedimentation in an Arctic fjord. Mar. Ecol. Prog. Ser. 303, 31–41 (2005).

    Article  Google Scholar 

  93. 93.

    Włodarska-Kowalczuk, M. & Kedra, M. Surrogacy in natural patterns of benthic distribution and diversity: selected taxa versus lower taxonomic resolution. Mar. Ecol. Prog. Ser. 351, 53–63 (2007).

    Article  Google Scholar 

  94. 94.

    Włodarska-Kowalczuk, M. & Weslawski, J. M. Mesoscale spatial structures of soft-bottom macrozoobenthos communities: effects of physical control and impoverishment. Mar. Ecol. Prog. Ser. 356, 215–224 (2008).

    Article  Google Scholar 

  95. 95.

    Włodarska-Kowalczuk, M., Renaud, P. E., Weslawski, J. M., Cochrane, S. K. & Denisenko, S. G. Species diversity, functional complexity and rarity in Arctic fjordic versus open shelf benthic systems. Mar. Ecol. Prog. Ser. 463, 73–87 (2012).

    Article  Google Scholar 

  96. 96.

    Ziegler, A., Smith, C., Edwards, K. & Vernet, M. Glacial dropstones: islands enhancing seafloor species richness of benthic megafauna in West Antarctic Peninsula fjords. Mar. Ecol. Prog. Ser. 583, 1–14 (2017).

    Article  Google Scholar 

  97. 97.

    Zemko, K., Pabis, K., Siciński, J. & Błażewicz, M. Low abundance and high species richness: the structure of the soft-bottom isopod fauna of a West Antarctic glacial fjord. Polar Biol. 40, 2187–2199 (2017).

    Article  Google Scholar 

  98. 98.

    Battin, T. J., Wille, A., Sattler, B. & Psenner, R. Phylogenetic and functional heterogeneity of sediment biofilms along environmental gradients in a glacial stream. Appl. Environ. Microbiol. 67, 799–807 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. 99.

    Battin, T., Wille, A., Psenner, R. & Richter, A. Large-scale environmental controls on microbial biofilms in high-alpine streams. Biogeosciences 1, 159–171 (2004).

    CAS  Article  Google Scholar 

  100. 100.

    Blaen, P. J., Brown, L. E., Hannah, D. M. & Milner, A. M. Environmental drivers of macroinvertebrate communities in high Arctic rivers (Svalbard). Freshw. Biol. 59, 378–391 (2014).

    Article  Google Scholar 

  101. 101.

    Brittain, J. E. et al. The macroinvertebrate communities of two contrasting Norwegian glacial rivers in relation to environmental variables. Freshw. Biol. 46, 1723–1736 (2001).

    Article  Google Scholar 

  102. 102.

    Brown, L. E., Milner, A. M. & Hannah, D. M. Stability and persistence of alpine stream macroinvertebrate communities and the role of physicochemical habitat variables. Hydrobiologia 560, 159–173 (2006).

    CAS  Article  Google Scholar 

  103. 103.

    Brown, L. E., Hannah, D. M. & Milner, A. M. Vulnerability of alpine stream biodiversity to shrinking glaciers and snowpacks. Glob. Change Biol. 13, 958–966 (2007).

    Article  Google Scholar 

  104. 104.

    Brown, L. E., Milner, A. M. & Hannah, D. M. Predicting river ecosystem response to glacial meltwater dynamics: a case study of quantitative water sourcing and glaciality index approaches. Aquat. Sci. 72, 325–334 (2010).

    Article  Google Scholar 

  105. 105.

    Brown, L. E. & Milner, A. M. Rapid loss of glacial ice reveals stream community assembly processes. Glob. Change Biol. 18, 2195–2204 (2012).

    Article  Google Scholar 

  106. 106.

    Brown, L. E., Dickson, N., Carrivick, J. & Füreder, L. Alpine river ecosystem response to glacial and anthropogenic flow pulses. Freshw. Sci. 34, 1201–1215 (2015).

    Article  Google Scholar 

  107. 107.

    Brown, L. E. et al. Functional diversity and community assembly of river invertebrates show globally consistent responses to decreasing glacier cover. Nat. Ecol. Evol. 2, 325–333 (2018).

    PubMed  Article  PubMed Central  Google Scholar 

  108. 108.

    Burgherr, P. & Ward, J. Longitudinal and seasonal distribution patterns of the benthic fauna of an alpine glacial stream (Val Roseg, Swiss Alps). Freshw. Biol. 46, 1705–1721 (2001).

    CAS  Article  Google Scholar 

  109. 109.

    Cadbury, S. L., Milner, A. M. & Hannah, D. M. Hydroecology of a New Zealand glacier‐fed river: linking longitudinal zonation of physical habitat and macroinvertebrate communities. Ecohydrology 4, 520–531 (2011).

    Article  Google Scholar 

  110. 110.

    Castella, E. et al. Macrobenthic invertebrate richness and composition along a latitudinal gradient of European glacier‐fed streams. Freshw. Biol. 46, 1811–1831 (2001).

    Article  Google Scholar 

  111. 111.

    Cauvy-Fraunié, S., Espinosa, R., Andino, P., Dangles, O. & Jacobsen, D. Relationships between stream macroinvertebrate communities and new flood‐based indices of glacial influence. Freshw. Biol. 59, 1916–1925 (2014).

    Article  Google Scholar 

  112. 112.

    Di Lorenzo, T., Stoch, F. & Galassi, D. M. Incorporating the hyporheic zone within the river discontinuum: longitudinal patterns of subsurface copepod assemblages in an Alpine stream. Limnologica 43, 288–296 (2013).

    CAS  Article  Google Scholar 

  113. 113.

    Eisendle, U. Spatiotemporal distribution of free-living nematodes in glacial-fed stream reaches (Hohe Tauern, Eastern Alps, Austria). Arct. Antarct. Alp. Res. 40, 470–480 (2008).

    Article  Google Scholar 

  114. 114.

    Eisendle-Flöckner, U., Jersabek, C. D., Kirchmair, M., Hashold, K. & Traunspurger, W. Community patterns of the small riverine benthos within and between two contrasting glacier catchments. Ecol. Evol. 3, 2832–2844 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  115. 115.

    Elgmork, K. & Sæther, O. R. Distribution of Invertebrates in a High Mountain Brook in the Colorado Rocky Mountains (Colorado Univ. Press, 1970).

  116. 116.

    Esposito, R. et al. Antarctic climate cooling and response of diatoms in glacial meltwater streams. Geophys. Res. Lett. 33, L07406 (2006).

    Article  Google Scholar 

  117. 117.

    Finn, D. S., Rasanen, K. & Robinson, C. T. Physical and biological changes to a lengthening stream gradient following a decade of rapid glacial recession. Glob. Change Biol. 16, 3314–3326 (2010).

    Article  Google Scholar 

  118. 118.

    Finn, D. S., Khamis, K. & Milner, A. M. Loss of small glaciers will diminish beta diversity in Pyrenean streams at two levels of biological organization. Glob. Ecol. Biogeogr. 22, 40–51 (2013).

    Article  Google Scholar 

  119. 119.

    Fleming, S. W. Comparative analysis of glacial and nival streamflow regimes with implications for lotic habitat quantity and fish species richness. Riv. Res. Appl. 21, 363–379 (2005).

    Article  Google Scholar 

  120. 120.

    Freimann, R., Bürgmann, H., Findlay, S. E. & Robinson, C. T. Bacterial structures and ecosystem functions in glaciated floodplains: contemporary states and potential future shifts. ISME J. 7, 2361–2373 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  121. 121.

    Freimann, R., Bürgmann, H., Findlay, S. E. & Robinson, C. T. Spatio-temporal patterns of major bacterial groups in Alpine waters. PLoS ONE 9, e113524 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  122. 122.

    Friberg, N., Milner, A. M., Svendsen, L. M., Lindegaard, C. & Larsen, S. E. Macroinvertebrate stream communities along regional and physico‐chemical gradients in Western Greenland. Freshw. Biol. 46, 1753–1764 (2001).

    CAS  Article  Google Scholar 

  123. 123.

    Füreder, L., Schütz, C., Wallinger, M. & Burger, R. Physico‐chemistry and aquatic insects of a glacier‐fed and a spring‐fed alpine stream. Freshw. Biol. 46, 1673–1690 (2001).

    Article  Google Scholar 

  124. 124.

    Füreder, L. et al. Reference conditions of alpine streams: physical habitat and ecology. Water Air Soil Poll. 2, 275–294 (2002).

    Article  Google Scholar 

  125. 125.

    Füreder, L. Life at the edge: habitat condition and bottom fauna of Alpine running waters. Int. Rev. Hydrobiol. 92, 491–513 (2007).

    Article  Google Scholar 

  126. 126.

    Gesierich, D. & Rott, E. Benthic algae and mosses from aquatic habitats in the catchment of a glacial stream (Rotmoos, Ötztal, Austria). Ber. Naturwiss.-med. Ver. Innsb. 91, 7–42 (2004).

    Google Scholar 

  127. 127.

    Gesierich, D. & Rott, E. Is diatom richness responding to catchment glaciation? A case study from Canadian headwater streams. J. Limnol. 71, 72–83 (2012).

    Article  Google Scholar 

  128. 128.

    Gislason, G. M., Adalsteinsson, H., Olafsson, J. S. & Hansen, I. Invertebrate communities of glacial and alpine rivers in the central highlands of Iceland. Verh. Int. Ver. Theor. Angew. Limnol. 27, 1602–1606 (2001).

    Google Scholar 

  129. 129.

    Gíslason, G. M., Hansen, I., Ólafsson, J. S. & Svavarsdóttir, K. Longitudinal changes in macroinvertebrate assemblages along a glacial river system in central Iceland. Freshw. Biol. 46, 1737–1751 (2001).

    Article  Google Scholar 

  130. 130.

    Hamerlik, L. & Jacobsen, D. Chironomid (Diptera) distribution and diversity in Tibetan streams with different glacial influence. Insect Conserv. Divers. 5, 319–326 (2012).

    Article  Google Scholar 

  131. 131.

    Hansen, I., Gíslason, G. M. & Olafsson, J. S. Diatoms in glacial and alpine rivers in Central Iceland. Verh. Int. Ver. Theor. Angew. Limnol. 29, 1271–1274 (2006).

    Google Scholar 

  132. 132.

    Hieber, M., Robinson, C. T., Rushforth, S. R. & Uehlinger, U. Algal communities associated with different alpine stream types. Arct. Antarct. Alp. Res. 33, 447–456 (2001).

    Article  Google Scholar 

  133. 133.

    Hieber, M., Robinson, C. T. & Uehlinger, U. Seasonal and diel patterns of invertebrate drift in different alpine stream types. Freshw. Biol. 48, 1078–1092 (2003).

    Article  Google Scholar 

  134. 134.

    Hieber, M., Robinson, C. T., Uehlinger, U. & Ward, J. A comparison of benthic macroinvertebrate assemblages among different types of alpine streams. Freshw. Biol. 50, 2087–2100 (2005).

    Article  Google Scholar 

  135. 135.

    Howard‐Williams, C., Vincent, C. L., Broady, P. A. & Vincent, W. F. Antarctic stream ecosystems: variability in environmental properties and algal community structure. Int. Rev. Ges. Hydrobiol. Hydrogr. 71, 511–544 (1986).

    Article  Google Scholar 

  136. 136.

    Huryn, A. D. et al. Landscape heterogeneity and the biodiversity of Arctic stream communities: a habitat template analysis. Can. J. Fish. Aquat. Sci. 62, 1905–1919 (2005).

    CAS  Article  Google Scholar 

  137. 137.

    Hylander, S. et al. Climate-induced input of turbid glacial meltwater affects vertical distribution and community composition of phyto- and zooplankton. J. Plankton Res. 33, 1239–1248 (2011).

    Article  Google Scholar 

  138. 138.

    Ilg, C. & Castella, E. Patterns of macroinvertebrate traits along three glacial stream continuums. Freshw. Biol. 51, 840–853 (2006).

    Article  Google Scholar 

  139. 139.

    Jacobsen, D. et al. Longitudinal zonation of macroinvertebrates in an Ecuadorian glacier-fed stream: do tropical glacial systems fit the temperate model? Freshw. Biol. 55, 1234–1248 (2010).

    CAS  Article  Google Scholar 

  140. 140.

    Khamis, K., Hannah, D., Brown, L., Tiberti, R. & Milner, A. The use of invertebrates as indicators of environmental change in alpine rivers and lakes. Sci. Total Environ. 493, 1242–1254 (2014).

    CAS  PubMed  Article  Google Scholar 

  141. 141.

    Khamis, K., Brown, L. E., Hannah, D. M. & Milner, A. M. Glacier–groundwater stress gradients control alpine river biodiversity. Ecohydrology 9, 1263–1275 (2016).

    Article  Google Scholar 

  142. 142.

    Knispel, S. & Castella, E. Disruption of a longitudinal pattern in environmental factors and benthic fauna by a glacial tributary. Freshw. Biol. 48, 604–618 (2003).

    Article  Google Scholar 

  143. 143.

    Kuhn, J. et al. Spatial variability in macroinvertebrate assemblages along and among neighbouring equatorial glacier‐fed streams. Freshw. Biol. 56, 2226–2244 (2011).

    Article  Google Scholar 

  144. 144.

    Lencioni, V., Maiolini, B. & Rossaro, B. The kryal and rhithral Chironomid community in the Carè Alto system (Italian central-eastern Alps). Verh. Int. Ver. Theor. Angew. Limnol. 27, 711–715 (2000).

    Google Scholar 

  145. 145.

    Lencioni, V. & Rossaro, B. Microdistribution of chironomids (Diptera: Chironomidae) in Alpine streams: an autoecological perspective. Hydrobiologia 533, 61–76 (2005).

    Article  Google Scholar 

  146. 146.

    Lencioni, V. Glacial influence and stream macroinvertebrate biodiversity under climate change: lessons from the Southern Alps. Sci. Total Environ. 622, 563–575 (2018).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  147. 147.

    Lods-Crozet, B. et al. Macroinvertebrate community structure in relation to environmental variables in a Swiss glacial stream. Freshw. Biol. 46, 1641–1661 (2001).

    Article  Google Scholar 

  148. 148.

    Lods-Crozet, B. et al. Chironomid (Diptera: Chironomidae) communities in six European glacier‐fed streams. Freshw. Biol. 46, 1791–1809 (2001).

    Article  Google Scholar 

  149. 149.

    Lods-Crozet, B., Lencioni, V., Brittain, J. E., Marziali, L. & Rossaro, B. Contrasting chironomid assemblages in two high Arctic streams on Svalbard. Fund. Appl. Limnol. Arch. Hydrobiol. 170, 211–222 (2007).

    Article  Google Scholar 

  150. 150.

    Maiolini, B. & Lencioni, V. Longitudinal distribution of macroinvertebrate assemblages in a glacially influenced stream system in the Italian Alps. Freshw. Biol. 46, 1625–1639 (2001).

    Article  Google Scholar 

  151. 151.

    Malard, F., Galassi, D., Lafont, M., Dolédec, S. & Ward, J. Longitudinal patterns of invertebrates in the hyporheic zone of a glacial river. Freshw. Biol. 48, 1709–1725 (2003).

    CAS  Article  Google Scholar 

  152. 152.

    Milner, A. M. Colonization and ecological development of new streams in Glacier Bay National Park, Alaska. Freshw. Biol. 18, 53–70 (1987).

    Article  Google Scholar 

  153. 153.

    Milner, A. M. et al. Colonization and development of stream communities across a 200-year gradient in Glacier Bay National Park, Alaska, USA. Can. J. Fish. Aquat. Sci. 57, 2319–2335 (2000).

    Article  Google Scholar 

  154. 154.

    Milner, A. M. et al. Evolution of a stream ecosystem in recently deglaciated terrain. Ecology 92, 1924–1935 (2011).

    PubMed  Article  Google Scholar 

  155. 155.

    Miserendino, M. L. et al. Biotic diversity of benthic macroinvertebrates at contrasting glacier-fed systems in Patagonia Mountains: the role of environmental heterogeneity facing global warming. Sci. Total Environ. 622, 152–163 (2018).

    PubMed  Article  CAS  Google Scholar 

  156. 156.

    Molina, J. M. Diversidad de Grupos Functionales Troficos de Macroinvertebrados, en los Rios de la Cordillera Real y las Serranias Altiplanicas de la Hidroecoregion Altoandina. MS thesis, Universidad Mayor de San Andrés (2013).

  157. 157.

    Murakami, T. et al. Limnological features of glacier-fed rivers in the Southern Tibetan Plateau, China. Limnology 13, 301–307 (2012).

    Article  Google Scholar 

  158. 158.

    Olafsson, J. S., Mar, G. G. & Adalsteinsson, H. Chironomids in glacial and non-glacial rivers in Iceland: a comparative study. Verh. Int. Ver. Theor. Angew. Limnol. 27, 720–726 (2001).

    Google Scholar 

  159. 159.

    Parker, S. M. & Huryn, A. D. Effects of natural disturbance on stream communities: a habitat template analysis of arctic headwater streams. Freshw. Biol. 56, 1342–1357 (2011).

    CAS  Article  Google Scholar 

  160. 160.

    Peter, H. & Sommaruga, R. Shifts in diversity and function of lake bacterial communities upon glacier retreat. ISME J. 10, 1545–1554 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  161. 161.

    Quenta, E. et al. Direct and indirect effects of glaciers on aquatic biodiversity in high Andean peatlands. Glob. Change Biol. 22, 3196–3205 (2016).

    Article  Google Scholar 

  162. 162.

    Ren, Z., Gao, H. & Elser, J. J. Longitudinal variation of microbial communities in benthic biofilms and association with hydrological and physicochemical conditions in glacier-fed streams. Freshw. Sci. 36, 479–490 (2017).

    Article  Google Scholar 

  163. 163.

    Robertson, A. & Milner, A. Meiobenthic arthropod communities in new streams in Glacier Bay National Park, Alaska. Hydrobiologia 397, 197–209 (1999).

    Article  Google Scholar 

  164. 164.

    Robertson, A. & Milner, A. The influence of stream age and environmental variables in structuring meiofaunal assemblages in recently deglaciated streams. Limnol. Oceanogr. 51, 1454–1465 (2006).

    Article  Google Scholar 

  165. 165.

    Robinson, C. T., Gessner, M. O., Callies, K. A., Jolidon, C. & Ward, J. V. Larch needle breakdown in contrasting streams of an alpine glacial floodplain. J. N. Am. Benthol. Soc. 19, 250–262 (2000).

    Article  Google Scholar 

  166. 166.

    Robinson, C., Uehlinger, U. & Hieber, M. Spatio‐temporal variation in macroinvertebrate assemblages of glacial streams in the Swiss Alps. Freshw. Biol. 46, 1663–1672 (2001).

    CAS  Article  Google Scholar 

  167. 167.

    Robinson, C. & Jolidon, C. Leaf breakdown and the ecosystem functioning of alpine streams. J. N. Am. Benthol. Soc. 24, 495–507 (2005).

    Article  Google Scholar 

  168. 168.

    Robinson, C. T. & Kawecka, B. Benthic diatoms of an Alpine stream/lake network in Switzerland. Aquat. Sci. 67, 492–506 (2005).

    CAS  Article  Google Scholar 

  169. 169.

    Robinson, C. T., Hieber, M., Wenzelides, V. & Lods-Crozet, B. Macroinvertebrate assemblages of a high elevation stream/lake network with an emphasis on the Chironomidae. Fund. Appl. Limnol. Arch. Hydrobiol. 169, 25–36 (2007).

    Article  Google Scholar 

  170. 170.

    Rott, E., Cantonati, M., Füreder, L. & Pfister, P. Benthic algae in high altitude streams of the Alps—a neglected component of the aquatic biota. Hydrobiologia 562, 195–216 (2006).

    Article  Google Scholar 

  171. 171.

    Sheath, R. G. & Müller, K. M. Distribution of stream macroalgae in four high Arctic drainage basins. Arctic 50, 355–364 (1997).

    Article  Google Scholar 

  172. 172.

    Slemmons, K. E. & Saros, J. E. Implications of nitrogen‐rich glacial meltwater for phytoplankton diversity and productivity in alpine lakes. Limnol. Oceanogr. 57, 1651–1663 (2012).

    CAS  Article  Google Scholar 

  173. 173.

    Snook, D. L. & Milner, A. M. Biological traits of macroinvertebrates and hydraulic conditions in a glacier-fed catchment (French Pyrenees). Arch. Hydrobiol. 153, 245–271 (2002).

    Article  Google Scholar 

  174. 174.

    Thompson, C., David, E., Freestone, M. & Robinson, C. Ecological patterns along two alpine glacial streams in the Fitzpatrick Wilderness, Wind River Range, USA. West. N. Am. Nat. 73, 137–147 (2013).

    Article  Google Scholar 

  175. 175.

    Turner, K. L., Matthews, R. A. & Rawhouser, A. K. Benthic macroinvertebrate assemblages in kryal and rhithral lake outlet streams in the North Cascade Mountains. Northwest Sci. 90, 206–227 (2016).

    Article  Google Scholar 

  176. 176.

    Wesener, M. D. et al. Hyporheic and benthic macroinvertebrate communities in glacial, clearwater, and brownwater streams in Alaska. Pan-Pac. Entomol. 87, 145–160 (2011).

    Article  Google Scholar 

  177. 177.

    Albrecht, M., Riesen, M. & Schmid, B. Plant–pollinator network assembly along the chronosequence of a glacier foreland. Oikos 119, 1610–1624 (2010).

    Article  Google Scholar 

  178. 178.

    Alfredsen, G. & Høiland, K. Succession of terrestrial macrofungi along a deglaciation gradient at Glacier Blåisen, South Norway. Nord. J. Bot. 21, 19–37 (2001).

    Article  Google Scholar 

  179. 179.

    Andreis, C., Caccianiga, M. & Cerabolini, B. Vegetation and environmental factors during primary succession on glacier forelands: some outlines from the Italian Alps. Plant Biosyst. 135, 295–310 (2001).

    Article  Google Scholar 

  180. 180.

    Bajerski, F. & Wagner, D. Bacterial succession in Antarctic soils of two glacier forefields on Larsemann Hills, East Antarctica. FEMS Microbiol. Ecol. 85, 128–142 (2013).

    PubMed  Article  PubMed Central  Google Scholar 

  181. 181.

    Bárcena, T. G., Yde, J. C. & Finster, K. W. Methane flux and high-affinity methanotrophic diversity along the chronosequence of a receding glacier in Greenland. Ann. Glaciol. 51, 23–31 (2010).

    Article  Google Scholar 

  182. 182.

    Birks, H. J. The present flora and vegetation of the moraines of the Klutlan Glacier, Yukon Territory, Canada: a study in plant succession. Quat. Res. 14, 60–86 (1980).

    Article  Google Scholar 

  183. 183.

    Blaalid, R. et al. Changes in the root-associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing. Mol. Ecol. 21, 1897–1908 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  184. 184.

    Bradley, J. A. et al. Microbial dynamics in a High Arctic glacier forefield: a combined field, laboratory, and modelling approach. Biogeosciences 13, 5677–5696 (2016).

    Article  Google Scholar 

  185. 185.

    Bråten, A. T. et al. Primary succession of surface active beetles and spiders in an alpine glacier foreland, central south Norway. Arct. Antarct. Alp. Res. 44, 2–15 (2012).

    Article  Google Scholar 

  186. 186.

    Burga, C. A. Vegetation development on the glacier forefield Morteratsch (Switzerland). Appl. Veg. Sci. 2, 17–24 (1999).

    Article  Google Scholar 

  187. 187.

    Carlson, M. L., Flagstad, L. A., Gillet, F. & Mitchell, E. A. Community development along a proglacial chronosequence: are above‐ground and below‐ground community structure controlled more by biotic than abiotic factors? J. Ecol. 98, 1084–1095 (2010).

    Article  Google Scholar 

  188. 188.

    Conen, F., Yakutin, M., Zumbrunn, T. & Leifeld, J. Organic carbon and microbial biomass in two soil development chronosequences following glacial retreat. Eur. J. Soil Sci. 58, 758–762 (2007).

    Article  Google Scholar 

  189. 189.

    Deiglmayr, K., Philippot, L., Tscherko, D. & Kandeler, E. Microbial succession of nitrate‐reducing bacteria in the rhizosphere of Poa alpina across a glacier foreland in the Central Alps. Environ. Microbiol. 8, 1600–1612 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  190. 190.

    Dong, K. et al. Soil fungal community development in a high Arctic glacier foreland follows a directional replacement model, with a mid-successional diversity maximum. Sci. Rep. 6, 26360 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  191. 191.

    Duc, L., Noll, M., Meier, B. E., Bürgmann, H. & Zeyer, J. High diversity of diazotrophs in the forefield of a receding alpine glacier. Microb. Ecol. 57, 179–190 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  192. 192.

    Erschbamer, B. & Mayer, R. Can successional species groups be discriminated based on their life history traits? A study from a glacier foreland in the Central Alps. Plant Ecol. Divers. 4, 341–351 (2011).

    Article  Google Scholar 

  193. 193.

    Esperschütz, J. et al. Microbial food web dynamics along a soil chronosequence of a glacier forefield. Biogeosciences 8, 3283–3294 (2011).

    Article  CAS  Google Scholar 

  194. 194.

    Fernández-Martínez, M. A. et al. Microbial succession dynamics along glacier forefield chronosequences in Tierra del Fuego (Chile). Polar Biol. 40, 1939–1957 (2017).

    Article  Google Scholar 

  195. 195.

    Franzen, M. & Dieker, P. The influence of terrain age and altitude on the arthropod communities found on recently deglaciated terrain. Curr. Zool. 60, 203–220 (2014).

    Article  Google Scholar 

  196. 196.

    Frenot, Y., Gloaguen, J., Cannavacciuolo, M. & Bellido, A. Primary succession on glacier forelands in the subantarctic Kerguelen Islands. J. Veg. Sci. 9, 75–84 (1998).

    Article  Google Scholar 

  197. 197.

    Frey, B., Bühler, L., Schmutz, S., Zumsteg, A. & Furrer, G. Molecular characterization of phototrophic microorganisms in the forefield of a receding glacier in the Swiss Alps. Environ. Res. Lett. 8, 015033 (2013).

    Article  CAS  Google Scholar 

  198. 198.

    Fujiyoshi, M. et al. Successional changes in ectomycorrhizal fungi associated with the polar willow Salix polaris in a deglaciated area in the High Arctic, Svalbard. Polar Biol. 34, 667–673 (2011).

    Article  Google Scholar 

  199. 199.

    Garibotti, I. A., Pissolito, C. I. & Villalba, R. Vegetation development on deglaciated rock outcrops from Glaciar Frias, Argentina. Arct. Antarct. Alp. Res. 43, 35–45 (2011).

    Article  Google Scholar 

  200. 200.

    Gereben-Krenn, B.-A., Krenn, H. W. & Strodl, M. A. Initial colonization of new terrain in an Alpine glacier foreland by carabid beetles (Carabidae, Coleoptera). Arct. Antarct. Alp. Res. 43, 397–403 (2011).

    Article  Google Scholar 

  201. 201.

    Gobbi, M., Fontaneto, D. & De Bernardi, F. Influence of climate changes on animal communities in space and time: the case of spider assemblages along an alpine glacier foreland. Glob. Change Biol. 12, 1985–1992 (2006).

    Article  Google Scholar 

  202. 202.

    Gobbi, M., Bernardi, F. D., Pelfini, M., Rossaro, B. & Brandmayr, P. Epigean arthropod succession along a 154-year glacier foreland chronosequence in the Forni Valley (Central Italian Alps). Arct. Antarct. Alp. Res. 38, 357–362 (2006).

    Article  Google Scholar 

  203. 203.

    Gobbi, M. et al. Plant adaptive responses during primary succession are associated with functional adaptations in ground beetles on deglaciated terrain. Commun. Ecol. 11, 223–231 (2010).

    Article  Google Scholar 

  204. 204.

    Gobbi, M. et al. Life in harsh environments: carabid and spider trait types and functional diversity on a debris‐covered glacier and along its foreland. Ecol. Entomol. 42, 838–848 (2017).

    Article  Google Scholar 

  205. 205.

    Górniak, D., Marszałek, H., Kwaśniak-Kominek, M., Rzepa, G. & Manecki, M. Soil formation and initial microbiological activity on a foreland of an Arctic glacier (SW Svalbard). Appl. Soil Ecol. 114, 34–44 (2017).

    Article  Google Scholar 

  206. 206.

    Gryziak, G. Colonization by mites of glacier-free areas in King George Island, Antarctica. Pesq. Agropec. Bras. 44, 891–895 (2009).

    Article  Google Scholar 

  207. 207.

    Hågvar, S., Solhøy, T. & Mong, C. E. Primary succession of soil mites (Acari) in a Norwegian glacier foreland, with emphasis on oribatid species. Arct. Antarct. Alp. Res. 41, 219–227 (2009).

    Article  Google Scholar 

  208. 208.

    Hågvar, S. Primary succession of springtails (Collembola) in a Norwegian glacier foreland. Arct. Antarct. Alp. Res. 42, 422–429 (2010).

    Article  Google Scholar 

  209. 209.

    Hodkinson, I. D., Coulson, S. J. & Webb, N. R. Community assembly along proglacial chronosequences in the high Arctic: vegetation and soil development in north‐west Svalbard. J. Ecol. 91, 651–663 (2003).

    Article  Google Scholar 

  210. 210.

    Hodkinson, I. D., Coulson, S. J. & Webb, N. R. Invertebrate community assembly along proglacial chronosequences in the high Arctic. J. Anim. Ecol. 73, 556–568 (2004).

    Article  Google Scholar 

  211. 211.

    Ilieva-Makulec, K. & Gryziak, G. Response of soil nematodes to climate-induced melting of Antarctic glaciers. Pol. J. Ecol. 57, 811–816 (2009).

    Google Scholar 

  212. 212.

    Ingimarsdóttir, M. et al. Primary assembly of soil communities: disentangling the effect of dispersal and local environment. Oecologia 170, 745–754 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  213. 213.

    Insam, H. et al. Soil microbiota along Ayoloco glacier retreat area of Iztaccíhuatl volcano. Mex. Catena 153, 83–88 (2017).

    CAS  Article  Google Scholar 

  214. 214.

    Jones, G. A. & Henry, G. H. Primary plant succession on recently deglaciated terrain in the Canadian High Arctic. J. Biogeogr. 30, 277–296 (2003).

    Article  Google Scholar 

  215. 215.

    Jumpponen, A., Trappe, J. M. & Cázares, E. Occurrence of ectomycorrhizal fungi on the forefront of retreating Lyman Glacier (Washington, USA) in relation to time since deglaciation. Mycorrhiza 12, 43–49 (2002).

    PubMed  Article  PubMed Central  Google Scholar 

  216. 216.

    Jumpponen, A., Brown, S. P., Trappe, J. M., Cázares, E. & Strömmer, R. Twenty years of research on fungal–plant interactions on Lyman Glacier forefront—lessons learned and questions yet unanswered. Fungal Ecol. 5, 430–442 (2012).

    Article  Google Scholar 

  217. 217.

    Kaštovská, K., Elster, J., Stibal, M. & Šantrůčková, H. Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (High Arctic). Microb. Ecol. 50, 396–407 (2005).

    PubMed  Article  PubMed Central  Google Scholar 

  218. 218.

    Kaufmann, R. Invertebrate succession on an alpine glacier foreland. Ecology 82, 2261–2278 (2001).

    Article  Google Scholar 

  219. 219.

    Kim, M., Jung, J. Y., Laffly, D., Kwon, H. Y. & Lee, Y. K. Shifts in bacterial community structure during succession in a glacier foreland of the High Arctic. FEMS Microbiol. Ecol. 93, fiw213 (2017).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  220. 220.

    Lazzaro, A., Risse-Buhl, U. & Brankatschk, R. Molecular and morphological snapshot characterisation of the protist communities in contrasting Alpine glacier forefields. Acta Protozool. 54, 143–154 (2015).

    CAS  Google Scholar 

  221. 221.

    Liu, J. et al. Diversity and succession of autotrophic microbial community in high-elevation soils along deglaciation chronosequence. FEMS Microbiol. Ecol. 92, fiw160 (2016).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  222. 222.

    Mateos-Rivera, A. et al. The effect of temperature change on the microbial diversity and community structure along the chronosequence of the sub-arctic glacier forefield of Styggedalsbreen (Norway). FEMS Microbiol. Ecol. 92, fnw038 (2016).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  223. 223.

    Mizuno, K. Succession processes of alpine vegetation in response to glacial fluctuations of Tyndall Glacier, Mt. Kenya, Kenya. Arct. Alp. Res. 30, 340–348 (1998).

    Article  Google Scholar 

  224. 224.

    Mizuno, K. & Fujita, T. Vegetation succession on Mt. Kenya in relation to glacial fluctuation and global warming. J. Veg. Sci. 25, 559–570 (2014).

    Article  Google Scholar 

  225. 225.

    Müller, E., Eidesen, P. B., Ehrich, D. & Alsos, I. G. Frequency of local, regional, and long-distance dispersal of diploid and tetraploid Saxifraga oppositifolia (Saxifragaceae) to Arctic glacier forelands. Am. J. Bot. 99, 459–471 (2012).

    PubMed  Article  PubMed Central  Google Scholar 

  226. 226.

    Nascimbene, J., Mayrhofer, H., Dainese, M. & Bilovitz, P. O. Assembly patterns of soil‐dwelling lichens after glacier retreat in the European Alps. J. Biogeogr. 44, 1393–1404 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  227. 227.

    Nemergut, D. R. et al. Microbial community succession in an unvegetated, recently deglaciated soil. Microbiol. Ecol. 53, 110–122 (2007).

    Article  Google Scholar 

  228. 228.

    Pérez, C. A. et al. Ecosystem development in short‐term postglacial chronosequences: N and P limitation in glacier forelands from Santa Inés Island, Magellan Strait. Austral Ecol. 39, 288–303 (2014).

    Article  Google Scholar 

  229. 229.

    Philippot, L., Tscherko, D., Bru, D. & Kandeler, E. Distribution of high bacterial taxa across the chronosequence of two alpine glacier forelands. Microbiol. Ecol. 61, 303–312 (2011).

    Article  Google Scholar 

  230. 230.

    Raffl, C., Mallaun, M., Mayer, R. & Erschbamer, B. Vegetation succession pattern and diversity changes in a glacier valley, Central Alps, Austria. Arct. Antarct. Alp. Res. 38, 421–428 (2006).

    Article  Google Scholar 

  231. 231.

    Reiners, W. A., Worley, I. A. & Lawrence, D. B. Plant diversity in a chronosequence at Glacier Bay, Alaska. Ecology 52, 55–69 (1971).

    Article  Google Scholar 

  232. 232.

    Rime, T. et al. Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Mol. Ecol. 24, 1091–1108 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  233. 233.

    Robbins, J. A. & Matthews, J. A. Pioneer vegetation on glacier forelands in southern Norway: emerging communities? J. Veg. Sci. 20, 889–902 (2009).

    Article  Google Scholar 

  234. 234.

    Schlag, R. N. & Erschbamer, B. Germination and establishment of seedlings on a glacier foreland in the Central Alps, Austria. Arct. Antarct. Alp. Res. 32, 270–277 (2000).

    Article  Google Scholar 

  235. 235.

    Schütte, U. M. et al. Bacterial succession in a glacier foreland of the High Arctic. ISME J. 3, 1258–1268 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  236. 236.

    Sigler, W., Crivii, S. & Zeyer, J. Bacterial succession in glacial forefield soils characterized by community structure, activity and opportunistic growth dynamics. Microbiol. Ecol. 44, 306–316 (2002).

    CAS  Article  Google Scholar 

  237. 237.

    Sigler, W. & Zeyer, J. Microbial diversity and activity along the forefields of two receding glaciers. Microbiol. Ecol. 43, 397–407 (2002).

    CAS  Article  Google Scholar 

  238. 238.

    Simmons, B. et al. Long-term experimental warming reduces soil nematode populations in the McMurdo Dry Valleys, Antarctica. Soil Biol. Biochem. 41, 2052–2060 (2009).

    CAS  Article  Google Scholar 

  239. 239.

    Srinivas, T. et al. Comparison of bacterial diversity in proglacial soil from Kafni Glacier, Himalayan Mountain ranges, India, with the bacterial diversity of other glaciers in the world. Extremophiles 15, 673–690 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  240. 240.

    Stöcklin, J. & Bäumler, E. Seed rain, seedling establishment and clonal growth strategies on a glacier foreland. J. Veg. Sci. 7, 45–56 (1996).

    Article  Google Scholar 

  241. 241.

    Tian, J. et al. Ecological succession pattern of fungal community in soil along a retreating glacier. Front. Microbiol. 8, 1028 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  242. 242.

    Trowbridge, J. & Jumpponen, A. Fungal colonization of shrub willow roots at the forefront of a receding glacier. Mycorrhiza 14, 283–293 (2004).

    PubMed  Article  PubMed Central  Google Scholar 

  243. 243.

    Tscherko, D., Rustemeier, J., Richter, A., Wanek, W. & Kandeler, E. Functional diversity of the soil microflora in primary succession across two glacier forelands in the Central Alps. Eur. J. Soil Sci. 54, 685–696 (2003).

    Article  Google Scholar 

  244. 244.

    Tscherko, D., Hammesfahr, U., Zeltner, G., Kandeler, E. & Böcker, R. Plant succession and rhizosphere microbial communities in a recently deglaciated alpine terrain. Basic Appl. Ecol. 6, 367–383 (2005).

    CAS  Article  Google Scholar 

  245. 245.

    Vater, A. E. Insect and arachnid colonization on the Storbreen glacier foreland, Jotunheimen, Norway: persistence of taxa suggests an alternative model of succession. Holocene 22, 1123–1133 (2012).

    Article  Google Scholar 

  246. 246.

    Vater, A. E. & Matthews, J. A. Testing the ‘addition and persistence model’ of invertebrate succession in a subalpine glacier-foreland chronosequence: Fåbergstølsbreen, southern Norway. Holocene 23, 1151–1162 (2013).

    Article  Google Scholar 

  247. 247.

    Vater, A. E. & Matthews, J. A. Succession of pitfall-trapped insects and arachnids on eight Norwegian glacier forelands along an altitudinal gradient: patterns and models. Holocene 25, 108–129 (2015).

    Article  Google Scholar 

  248. 248.

    Wu, X. et al. Bacterial diversity in the foreland of the Tianshan No. 1 glacier, China. Environ. Res. Lett. 7, 014038 (2012).

    Article  Google Scholar 

  249. 249.

    Zimmer, A. et al. Time lag between glacial retreat and upward migration alters tropical alpine communities. Perspect. Plant Ecol. 30, 89–102 (2017).

    Article  Google Scholar 

  250. 250.

    Zumsteg, A. et al. Bacterial, archaeal and fungal succession in the forefield of a receding glacier. Microbiol. Ecol. 63, 552–564 (2012).

    Article  Google Scholar 

  251. 251.

    Lajeunesse, M. J., Koricheva, J., Gurevitch, J. & Mengersen, K. in Handbook of Meta-analysis in Ecology and Evolution 195–206 (2013).

  252. 252.

    Hedges, L. V. & Olkin, I. Statistical Methods for Meta-analysis (Academic Press, 1985).

  253. 253.

    Borenstein, M., Hedges, L. V., Higgins, J. P. & Rothstein, H. R. Introduction to Meta-analysis (John Wiley & Sons, 2009).

  254. 254.

    Gardner, A. S. et al. A reconciled estimate of glacier contributions to sea level rise: 2003 to 2009. Science 340, 852–857 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  255. 255.

    Nakagawa, S., Noble, D. W., Senior, A. M. & Lagisz, M. Meta-evaluation of meta-analysis: ten appraisal questions for biologists. BMC Biol. 15, 18 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  256. 256.

    Nakagawa, S. & Santos, E. S. Methodological issues and advances in biological meta-analysis. Evol. Ecol. 26, 1253–1274 (2012).

    Article  Google Scholar 

  257. 257.

    Konstantopoulos, S. Fixed effects and variance components estimation in three‐level meta‐analysis. Res. Synth. Methods 2, 61–76 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  258. 258.

    Finlay, B. J. Global dispersal of free-living microbial eukaryote species. Science 296, 1061–1063 (2002).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  259. 259.

    Viechtbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).

    Article  Google Scholar 

  260. 260.

    Peters, J. L., Sutton, A. J., Jones, D. R., Abrams, K. R. & Rushton, L. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J. Clin. Epidemiol. 61, 991–996 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  261. 261.

    Egger, M., Smith, G. D., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. Br. Med. J. 315, 629–634 (1997).

    CAS  Article  Google Scholar 

  262. 262.

    Pfeffer, W. T. et al. The Randolph Glacier Inventory: a globally complete inventory of glaciers. J. Glaciol. 60, 537–552 (2014).

    Article  Google Scholar 

  263. 263.

    Raup, B. H. et al. The GLIMS Geospatial Glacier Database: a new tool for studying glacier change. Glob. Planet. Change 56, 101–110 (2007).

    Article  Google Scholar 

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Acknowledgements

We thank C. Randimbivololona and P. Bonneviot for drawing most of the icons in Figs. 3 and 4.

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S.C.-F. and O.D. conceived the study, acquired the data and wrote the manuscript. S.C.-F. performed the analyses and constructed the figures.

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Correspondence to Sophie Cauvy-Fraunié.

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Cauvy-Fraunié, S., Dangles, O. A global synthesis of biodiversity responses to glacier retreat. Nat Ecol Evol 3, 1675–1685 (2019). https://doi.org/10.1038/s41559-019-1042-8

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