Advertisement

Polar Biology

, Volume 41, Issue 8, pp 1619–1633 | Cite as

Macroinvertebrate and soil prokaryote communities in the forest–tundra ecotone of the Subarctic Yukon

  • Shaun Turney
  • Ianina Altshuler
  • Lyle G. Whyte
  • Christopher M. Buddle
Original Paper

Abstract

The forest–tundra interface is the world’s largest ecotone, and is globally important due to its biodiversity, climatic sensitivity, and natural resources. The ecological communities which characterize this ecotone, and which provide local and global ecosystem services, are affected by environmental variation at multiple scales. We explored correlations between environmental variables and macroinvertebrate and soil prokaryote communities in the forest–tundra ecotone of the Yukon, Canada. We found that each tussock tundra site possessed a distinct community of macroinvertebrates and prokaryotes, and therefore represented a unique contribution to regional biodiversity. Prokaryote diversity increased with active layer depth, which could be an effect of temperature, or could be evidence of a species-area effect. Prokaryote diversity decreased with lichen cover, which could be due to antimicrobial properties of lichen. The macroinvertebrate community composition was affected by proximity to a human disturbance, the Dempster Highway. Both macroinvertebrate and prokaryote community compositions changed along the latitudinal transect, as the biome transitioned from taiga to tundra. We also found that the abundance of carnivores relative to herbivores decreased with latitude, which adds to recent evidence that predation decreases with latitude. Our survey yielded new insights about how macro- and microorganisms vary together and independently in relation to environmental variables at multiple scales in a forest–tundra ecotone.

Keywords

Community structure Entomology Bacteria Soil ecology Biodiversity Tundra 

Notes

Acknowledgements

The authors thank Anne-Sophie Caron for her dedicated field work assistance, Scot E. Dowd for his excellent DNA sequencing services, and the anonymous reviewers and the guest editor Lauren Culler who provided helpful feedback. This project was possible due to funding from the National Science and Engineering Research Council of Canada: A Discovery Grant and Northern Research Supplement to CMB and a Postgraduate Scholarship-Doctoral to ST. This study was further supported by a W. Garfield Weston Award for Northern Research (Doctoral) from the Canadian Northern Studies Trust to ST.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This research was permitted under the Yukon Scientists and Explorer’s Act, License Number: 15-10S and E. Research activity within Tombstone Territorial Park (Sites 4 and 5) was permitted by a Research and Education Park Permit, Permit Number 15-RE-TP-01. Additionally, permission was sought and granted from all relevant First Nations (Tr’ondek Hwech’in, Tetlit Gwich’in, and Vuntut Gwitchin). All applicable international, national, and institutional guidelines for the care and use of animals were followed.

Supplementary material

300_2018_2330_MOESM1_ESM.csv (4 kb)
Supplementary material 1 (CSV 4 kb)
300_2018_2330_MOESM2_ESM.csv (3 kb)
Supplementary material 2 (CSV 2 kb)
300_2018_2330_MOESM3_ESM.csv (2.2 mb)
Supplementary material 3 (CSV 2249 kb)
300_2018_2330_MOESM4_ESM.pdf (74 kb)
Supplementary material 4 (PDF 74 kb)
300_2018_2330_MOESM5_ESM.pdf (167 kb)
Supplementary material 5 (PDF 167 kb)
300_2018_2330_MOESM6_ESM.pdf (31 kb)
Supplementary material 6 (PDF 30 kb)
300_2018_2330_MOESM7_ESM.pdf (53 kb)
Supplementary material 7 (PDF 53 kb)
300_2018_2330_MOESM8_ESM.pdf (131 kb)
Supplementary material 8 (PDF 131 kb)
300_2018_2330_MOESM9_ESM.pdf (54 kb)
Supplementary material 9 (PDF 54 kb)

References

  1. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178CrossRefGoogle Scholar
  2. Baas Becking L (1934) Geobiologie of inleiding tot de milieukunde. Van Stockum and Zoon, The HagueGoogle Scholar
  3. Badgley C, Fox DL (2000) Ecological biogeography of North American mammals: species density and ecological structure in relation to environmental gradients. J Biogeogr 27:1437–1467CrossRefGoogle Scholar
  4. Barrio IC, Bueno CG, Hik DS (2016) Warming the tundra: reciprocal responses of invertebrate herbivores and plants. Oikos 125:20–28CrossRefGoogle Scholar
  5. Barton K (2017) MuMIn: multi-model inference. R package version 1.40.0. https://CRAN.R-project.org/package=MuMIn. Accessed 2 Nov 2017
  6. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  7. Beijerinck MW (1913) De infusies en de ontdekking der backteriën. Jaarboek van de Koninklijke Akademie voor Wetenschappen, MüllerGoogle Scholar
  8. Berg M, De Ruiter P, Didden W, Janssen M, Schouten T, Verhoef H (2001) Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil. Oikos 94:130–142CrossRefGoogle Scholar
  9. Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA et al (2011) The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43:1450–1455CrossRefPubMedPubMedCentralGoogle Scholar
  10. Besuchet C, Burckhardt DH, Löbl I (1987) The “Winkler/Moczarski” eclector as an efficient extractor for fungus and litter Coleoptera. Coleopt Bull 41:392–394Google Scholar
  11. Blanc C, Sy M, Djigal D, Brauman A, Normand P, Villenave C (2006) Nutrition on bacteria by bacterial-feeding nematodes and consequences on the structure of soil bacterial community. Eur J Soil Biol 42:70–78CrossRefGoogle Scholar
  12. Bokhorst S, Wardle DA, Nilsson M-C, Gundale MJ (2014) Impact of understory mosses and dwarf shrubs on soil micro-arthropods in a boreal forest chronosequence. Plant Soil 379:121–133CrossRefGoogle Scholar
  13. Bokhorst S, Kardol P, Bellingham PJ, Kooyman RM, Richardson SJ, Schmidt S, Wardle DA (2016) Responses of communities of soil organisms and plants to soil aging at two contrasting long-term chronosequences. Soil Biol Biochem 106:69–79CrossRefGoogle Scholar
  14. Bowden JJ, Buddle CM (2010) Spider assemblages across elevational and latitudinal gradients in the Yukon Territory, Canada. Arctic 63:261–272CrossRefGoogle Scholar
  15. Bowden JJ, Buddle CM (2012a) Egg sac parasitism of Arctic wolf spiders (Araneae: Lycosidae) from northwestern North America. J Arachnol 40:348–350CrossRefGoogle Scholar
  16. Bowden JJ, Buddle CM (2012b) Life history of tundra-dwelling wolf spiders (Araneae: Lycosidae) from the Yukon Territory, Canada. Can J Zool 90:714–721CrossRefGoogle Scholar
  17. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304CrossRefGoogle Scholar
  18. Callaghan TV, Werkman BR, Crawford RM (2002) The tundra-taiga interface and its dynamics: concepts and applications. Ambio 12:6–14Google Scholar
  19. Cameron EA, Lantz TC (2016) Drivers of tall shrub proliferation adjacent to the Dempster Highway, Northwest Territories, Canada. Environ Res Lett 11:045006CrossRefGoogle Scholar
  20. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624CrossRefPubMedPubMedCentralGoogle Scholar
  21. CBC News (2015) Yukon gov’t seeks help as permafrost thaws on Dempster Highway. Canadian Broadcasting Corporation. http://www.cbc.ca/news/canada/north/yukon-gov-t-seeks-help-as-permafrost-thaws-on-dempster-highway-1.3166375. Accessed 6 May 2017
  22. CCEA (2016) Ecozones introduction. CCEA-CCAE. http://www.ccea.org/ecozones-introduction/. Accessed 6 Nov 2017
  23. Chu H, Fierer N, Lauber CL, Caporaso JG, Knight R, Grogan P (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12:2998–3006CrossRefPubMedGoogle Scholar
  24. Chu H, Neufeld JD, Walker VK, Grogan P (2011) The influence of vegetation type on the dominant soil bacteria, archaea, and fungi in a low Arctic tundra landscape. Soil Sci Soc Am J 75:1756–1765CrossRefGoogle Scholar
  25. Coffin AW (2007) From roadkill to road ecology: a review of the ecological effects of roads. J Transp Geogr 15:396–406CrossRefGoogle Scholar
  26. Cornelissen JH, Callaghan TV, Alatalo JM, Michelsen A, Graglia E, Hartley AE, Hik DS, Hobbie SE, Press MC, Robinson CH, Henry GH (2001) Global change and arctic ecosystems: is lichen decline a function of increases in vascular plant biomass? J Ecol 89:984–994CrossRefGoogle Scholar
  27. De Wit R, Bouvier T (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8:755–758CrossRefPubMedGoogle Scholar
  28. Downes JA (1965) Adaptations of insects in the arctic. Annu Rev Entomol 10:257–274CrossRefGoogle Scholar
  29. Environment Canada (2017) Yukon—Weather conditions and forecast by locations. Government of Canada. https://weather.gc.ca/forecast/canada/index_e.html?id=YT. Accessed 18 Aug 2017
  30. Ernst CM, Buddle CM (2015) Drivers and patterns of ground-dwelling beetle biodiversity across Northern Canada. PLoS ONE 10:e0122163CrossRefPubMedPubMedCentralGoogle Scholar
  31. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631CrossRefPubMedGoogle Scholar
  32. Ford JD, Smit B, Wandel J (2006) Vulnerability to climate change in the Arctic: a case study from Arctic Bay, Canada. Glob Environ Change 16:145–160CrossRefGoogle Scholar
  33. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage Publications, Thousand OaksGoogle Scholar
  34. Francoeur A (1997) Ants (Hymenoptera: Formicidae) of the Yukon. In: Danks HV (ed) Insects of the Yukon. Biological survey of Canada (Terrestrial Arthropods), Ottawa, pp 901–910Google Scholar
  35. Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227CrossRefPubMedGoogle Scholar
  36. Gill HK, Lantz TC, O’Neill B, Kokelj SV (2014) Cumulative impacts and feedbacks of a gravel road on shrub tundra ecosystems in the Peel Plateau, Northwest Territories, Canada. Arct Antarct Alp Res 46:947–961CrossRefGoogle Scholar
  37. Graham DE, Wallenstein MD, Vishnivetskaya TA, Waldrop MP, Phelps TJ, Pfiffner SM, Onstott TC, Whyte LG, Rivkina EM, Gilichinsky DA (2012) Microbes in thawing permafrost: the unknown variable in the climate change equation. ISME J 6:709–712CrossRefPubMedGoogle Scholar
  38. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JB (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506CrossRefPubMedGoogle Scholar
  39. Harry M, Gambier B, Garnier-Sillam E (2000) Soil conservation for DNA preservation for bacterial molecular studies. Eur J Soil Biol 36:51–55CrossRefGoogle Scholar
  40. Heiberger RM, Robbins NB (2014) Design of diverging stacked bar charts for Likert scales and other applications. J Stat Softw 57:1–32CrossRefGoogle Scholar
  41. Horner-Devine MC, Lage M, Hughes JB, Bohannan BJ (2004) A taxa–area relationship for bacteria. Nature 432:750–753CrossRefPubMedGoogle Scholar
  42. Hultman J, Waldrop MP, Mackelprang R, David MM, McFarland J, Blazewicz SJ, Harden J, Turetsky MR, McGuire AD, Shah MB (2015) Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521:208–212CrossRefPubMedGoogle Scholar
  43. Johnson EA (1981) Vegetation organization and dynamics of lichen woodland communities in the Northwest Territories, Canada. Ecology 62:200–215CrossRefGoogle Scholar
  44. Kershaw GP, Kershaw LJ (1987) Successful plant colonizers on disturbances in tundra areas of Northwestern Canada. Arct Alp Res 19:451–460CrossRefGoogle Scholar
  45. Kim HM, Jung JY, Yergeau E, Hwang CY, Hinzman L, Nam S et al (2014) Bacterial community structure and soil properties of a subarctic tundra soil in Council, Alaska. FEMS Microbiol Ecol 89:465–475CrossRefPubMedPubMedCentralGoogle Scholar
  46. Kranner I, Beckett R, Hochman A, Nash TH III (2008) Desiccation-tolerance in lichens: a review. The Bryologist 111:576–593CrossRefGoogle Scholar
  47. Lamy SL (2016) The U.S. Arctic Policy Agenda. In future security of the global arctic: state policy, economic security and climate. Palgrave Pivot, LondonGoogle Scholar
  48. Lang SI, Cornelissen JH, Shaver GR, Ahrens M, Callaghan TV, Molau U, Ter Braak CJ, Hölzer A, Aerts R (2012) Arctic warming on two continents has consistent negative effects on lichen diversity and mixed effects on bryophyte diversity. Glob Change Biol 18:1096–1107CrossRefGoogle Scholar
  49. Lavelle P, Decaëns T, Aubert M, Barot S, Blouin M, Bureau F et al (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:3–15CrossRefGoogle Scholar
  50. Mackelprang R, Saleska SR, Jacobsen CS, Jansson JK, Taş N (2016) Permafrost meta-omics and climate change. Annu Rev Earth Planet Sci 44:439–462CrossRefGoogle Scholar
  51. MacLean SF, Douce GK, Morgan EA, Skeel MA (1977) Community organization in the soil invertebrates of Alaskan arctic tundra. Ecol Bull 25:90–101Google Scholar
  52. Martiny JBH, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112CrossRefPubMedGoogle Scholar
  53. McGuire AD, Anderson LG, Christensen TR, Dallimore S, Guo L, Hayes DJ, Heimann M, Lorenson TD, Macdonald RW, Roulet N (2009) Sensitivity of the carbon cycle in the Arctic to climate change. Ecol Monogr 79:523–555CrossRefGoogle Scholar
  54. Muñoz PT, Torres FP, Megías AG (2015) Effects of roads on insects: a review. Biodivers Conserv 24:659–682CrossRefGoogle Scholar
  55. Myers-Smith IH, Elmendorf SC, Beck PS, Wilmking M, Hallinger M, Blok D et al (2015) Climate sensitivity of shrub growth across the tundra biome. Nat Clim Change 5:887–891CrossRefGoogle Scholar
  56. Myers-Smitt IH, Arnesen BK, Thompson RM, Chapin FS III (2006) Cumulative impacts on Alaskan arctic tundra of a quarter century of road dust. Ecoscience 13:503–510CrossRefGoogle Scholar
  57. Nielsen UN, Osler GH, Campbell CD, Burslem DF, van der Wal R (2010) The influence of vegetation type, soil properties and precipitation on the composition of soil mite and microbial communities at the landscape scale. J Biogeogr 37:1317–1328CrossRefGoogle Scholar
  58. O’Malley MA (2007) The nineteenth century roots of “everything is everywhere”. Nat Rev Microbiol 5:647–651CrossRefPubMedGoogle Scholar
  59. O’Neill HB, Burn CR (2015) Permafrost degradation adjacent to snow fences along the Dempster Highway, Peel Plateau, NWT. In: 7th Canadian Permafrost Conference: Proceedings of a conference held 20–23 September 2015 at the Quebec City Convention CentreGoogle Scholar
  60. Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P, et al (2016) vegan: community ecology package. R package version 2.4-0. CRAN https://CRAN.R-project.org/package=vegan. Accessed 20 Jan 2017
  61. Oswood MW (1989) Community structure of benthic invertebrates in interior Alaskan (USA) streams and rivers. Hydrobiologia 172:97–110CrossRefGoogle Scholar
  62. Petersen H, Luxton M (1982) A comparative analysis of soil fauna populations and their role in decomposition. Oikos 39:287–388Google Scholar
  63. Polis GA (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86:3–15CrossRefGoogle Scholar
  64. Post DM (2002) The long and short of food-chain length. Trends Ecol Evol 17:269–277CrossRefGoogle Scholar
  65. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 20 Jan 2017
  66. Ranson KJ, Sun G, Kharuk VI, Kovacs K (2004) Assessing tundra–taiga boundary with multi-sensor satellite data. Remote Sens Environ 93:283–295CrossRefGoogle Scholar
  67. Rich ME, Gough L, Boelman NT (2013) Arctic arthropod assemblages in habitats of differing shrub dominance. Ecography 36:994–1003CrossRefGoogle Scholar
  68. Rodrı́guez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339CrossRefPubMedGoogle Scholar
  69. Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269CrossRefPubMedGoogle Scholar
  70. Roslin T, Hardwick B, Novotny V, Petry WK, Andrew NR, Asmus A et al (2017) Higher predation risk for insect prey at low latitudes and elevations. Science 356:742–744CrossRefPubMedGoogle Scholar
  71. Sabu TK, Shiju RT, Vinod KV, Nithya S (2011) A comparison of the pitfall trap, Winkler extractor and Berlese funnel for sampling ground-dwelling arthropods in tropical montane cloud forests. J Insect Sci 11:1–19CrossRefGoogle Scholar
  72. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269CrossRefGoogle Scholar
  73. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMedGoogle Scholar
  74. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRefPubMedPubMedCentralGoogle Scholar
  75. Shelford VE (1963) The ecology of North America. University of Illinois Press, UrbanaGoogle Scholar
  76. Shukla V, Joshi GP, Rawat MSM (2010) Lichens as a potential natural source of bioactive compounds: a review. Phytochem Rev 9:303–314CrossRefGoogle Scholar
  77. Smith J, Potts S, Eggleton P (2008) Evaluating the efficiency of sampling methods in assessing soil macrofauna communities in arable systems. Eur J Soil Biol 44:271–276CrossRefGoogle Scholar
  78. Sørensen LI, Holmstrup M, Maraldo K, Christensen S, Christensen B (2006) Soil fauna communities and microbial respiration in high Arctic tundra soils at Zackenberg, Northeast Greenland. Polar Biol 29:189–195CrossRefGoogle Scholar
  79. Stanek W, Alexander K, Simmons CS (1981) Reconnaissance of vegetation and soils along the Dempster Highway, Yukon Territory, I: vegetation types. Environment Canada, Canadian Forestry Service, Pacific Forest Research Centre, VictoriaGoogle Scholar
  80. Ste-Marie E, Turney S, Buddle CM (2018) The effect of road proximity on arthropod communities in the Yukon, Canada. Arctic 71:89–98CrossRefGoogle Scholar
  81. Stewart AL, Wright AF (1995) A new inexpensive suction apparatus for sampling arthropods in grassland. Ecol Entomol 20:98–102CrossRefGoogle Scholar
  82. Sweet SK, Asmus A, Rich ME, Wingfield J, Gough L, Boelman NT (2015) NDVI as a predictor of canopy arthropod biomass in the Alaskan arctic tundra. Ecol Appl 25:779–790CrossRefPubMedGoogle Scholar
  83. Turney S, Buddle CM (2016) Pyramids of species richness: the determinants and distribution of species diversity across trophic levels. Oikos 125:1224–1233CrossRefGoogle Scholar
  84. Van Der Heijden MG, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefPubMedGoogle Scholar
  85. Voigt C, Lamprecht RE, Marushchak ME, Lind SE, Novakovskiy A, Aurela M et al (2016) Warming of subarctic tundra increases emissions of all three important greenhouse gases–carbon dioxide, methane, and nitrous oxide. Glob Change Biol.  https://doi.org/10.1111/gcb.13563 Google Scholar
  86. Wallenstein MD, McMahon S, Schimel J (2007) Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiol Ecol 59:428–435CrossRefPubMedGoogle Scholar
  87. Wardle DA, Yeates GW, Williamson WM, Bonner KI, Barker GM (2004) Linking aboveground and belowground communities: the indirect influence of aphid species identity and diversity on a three trophic level soil food web. Oikos 107:283–294CrossRefGoogle Scholar
  88. Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886CrossRefPubMedGoogle Scholar
  89. Xue K, Yuan MM, Shi ZJ, Qin Y, Deng Y, Cheng L et al (2016) Tundra soil carbon is vulnerable to rapid microbial decomposition under climate warming. Nat Clim Change 6:595–600CrossRefGoogle Scholar
  90. Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA (2007) Patterns of bacterial diversity across a range of antarctic terrestrial habitats. Environ Microbiol 9:2670–2682CrossRefPubMedGoogle Scholar
  91. Yergeau E, Schoondermark-Stolk SA, Brodie EL, Déjean S, DeSantis TZ, Gonçalves O et al (2009) Environmental microarray analyses of antarctic soil microbial communities. ISME J 3:340–351CrossRefPubMedGoogle Scholar
  92. Yergeau E, Hogues H, Whyte LG, Greer CW (2010) The functional potential of high arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses. ISME J 4:1206–1214CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Shaun Turney
    • 1
  • Ianina Altshuler
    • 1
  • Lyle G. Whyte
    • 1
  • Christopher M. Buddle
    • 1
  1. 1.Department of Natural Resource SciencesMcGill University Macdonald CampusSt. Anne de BellevueCanada

Personalised recommendations