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.
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References
Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178
Baas Becking L (1934) Geobiologie of inleiding tot de milieukunde. Van Stockum and Zoon, The Hague
Badgley C, Fox DL (2000) Ecological biogeography of North American mammals: species density and ecological structure in relation to environmental gradients. J Biogeogr 27:1437–1467
Barrio IC, Bueno CG, Hik DS (2016) Warming the tundra: reciprocal responses of invertebrate herbivores and plants. Oikos 125:20–28
Barton K (2017) MuMIn: multi-model inference. R package version 1.40.0. https://CRAN.R-project.org/package=MuMIn. Accessed 2 Nov 2017
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beijerinck MW (1913) De infusies en de ontdekking der backteriën. Jaarboek van de Koninklijke Akademie voor Wetenschappen, Müller
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 94:130–142
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 43:1450–1455
Besuchet C, Burckhardt DH, Löbl I (1987) The “Winkler/Moczarski” eclector as an efficient extractor for fungus and litter Coleoptera. Coleopt Bull 41:392–394
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 42:70–78
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 379:121–133
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 106:69–79
Bowden JJ, Buddle CM (2010) Spider assemblages across elevational and latitudinal gradients in the Yukon Territory, Canada. Arctic 63:261–272
Bowden JJ, Buddle CM (2012a) Egg sac parasitism of Arctic wolf spiders (Araneae: Lycosidae) from northwestern North America. J Arachnol 40:348–350
Bowden JJ, Buddle CM (2012b) Life history of tundra-dwelling wolf spiders (Araneae: Lycosidae) from the Yukon Territory, Canada. Can J Zool 90:714–721
Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304
Callaghan TV, Werkman BR, Crawford RM (2002) The tundra-taiga interface and its dynamics: concepts and applications. Ambio 12:6–14
Cameron EA, Lantz TC (2016) Drivers of tall shrub proliferation adjacent to the Dempster Highway, Northwest Territories, Canada. Environ Res Lett 11:045006
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 6:1621–1624
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
CCEA (2016) Ecozones introduction. CCEA-CCAE. http://www.ccea.org/ecozones-introduction/. Accessed 6 Nov 2017
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 12:2998–3006
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 75:1756–1765
Coffin AW (2007) From roadkill to road ecology: a review of the ecological effects of roads. J Transp Geogr 15:396–406
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 89:984–994
De Wit R, Bouvier T (2006) ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environ Microbiol 8:755–758
Downes JA (1965) Adaptations of insects in the arctic. Annu Rev Entomol 10:257–274
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
Ernst CM, Buddle CM (2015) Drivers and patterns of ground-dwelling beetle biodiversity across Northern Canada. PLoS ONE 10:e0122163
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631
Ford JD, Smit B, Wandel J (2006) Vulnerability to climate change in the Arctic: a case study from Arctic Bay, Canada. Glob Environ Change 16:145–160
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage Publications, Thousand Oaks
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 901–910
Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227
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 46:947–961
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 6:709–712
Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JB (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506
Harry M, Gambier B, Garnier-Sillam E (2000) Soil conservation for DNA preservation for bacterial molecular studies. Eur J Soil Biol 36:51–55
Heiberger RM, Robbins NB (2014) Design of diverging stacked bar charts for Likert scales and other applications. J Stat Softw 57:1–32
Horner-Devine MC, Lage M, Hughes JB, Bohannan BJ (2004) A taxa–area relationship for bacteria. Nature 432:750–753
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 521:208–212
Johnson EA (1981) Vegetation organization and dynamics of lichen woodland communities in the Northwest Territories, Canada. Ecology 62:200–215
Kershaw GP, Kershaw LJ (1987) Successful plant colonizers on disturbances in tundra areas of Northwestern Canada. Arct Alp Res 19:451–460
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 89:465–475
Kranner I, Beckett R, Hochman A, Nash TH III (2008) Desiccation-tolerance in lichens: a review. The Bryologist 111:576–593
Lamy SL (2016) The U.S. Arctic Policy Agenda. In future security of the global arctic: state policy, economic security and climate. Palgrave Pivot, London
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 18:1096–1107
Lavelle P, Decaëns T, Aubert M, Barot S, Blouin M, Bureau F et al (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:3–15
Mackelprang R, Saleska SR, Jacobsen CS, Jansson JK, Taş N (2016) Permafrost meta-omics and climate change. Annu Rev Earth Planet Sci 44:439–462
MacLean SF, Douce GK, Morgan EA, Skeel MA (1977) Community organization in the soil invertebrates of Alaskan arctic tundra. Ecol Bull 25:90–101
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 4:102–112
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 79:523–555
Muñoz PT, Torres FP, Megías AG (2015) Effects of roads on insects: a review. Biodivers Conserv 24:659–682
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 5:887–891
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 13:503–510
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 37:1317–1328
O’Malley MA (2007) The nineteenth century roots of “everything is everywhere”. Nat Rev Microbiol 5:647–651
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 Centre
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
Oswood MW (1989) Community structure of benthic invertebrates in interior Alaskan (USA) streams and rivers. Hydrobiologia 172:97–110
Petersen H, Luxton M (1982) A comparative analysis of soil fauna populations and their role in decomposition. Oikos 39:287–388
Polis GA (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86:3–15
Post DM (2002) The long and short of food-chain length. Trends Ecol Evol 17:269–277
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
Ranson KJ, Sun G, Kharuk VI, Kovacs K (2004) Assessing tundra–taiga boundary with multi-sensor satellite data. Remote Sens Environ 93:283–295
Rich ME, Gough L, Boelman NT (2013) Arctic arthropod assemblages in habitats of differing shrub dominance. Ecography 36:994–1003
Rodrı́guez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339
Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269
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 356:742–744
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 11:1–19
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 40:245–269
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 9:676–682
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Shelford VE (1963) The ecology of North America. University of Illinois Press, Urbana
Shukla V, Joshi GP, Rawat MSM (2010) Lichens as a potential natural source of bioactive compounds: a review. Phytochem Rev 9:303–314
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 44:271–276
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 29:189–195
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, Victoria
Ste-Marie E, Turney S, Buddle CM (2018) The effect of road proximity on arthropod communities in the Yukon, Canada. Arctic 71:89–98
Stewart AL, Wright AF (1995) A new inexpensive suction apparatus for sampling arthropods in grassland. Ecol Entomol 20:98–102
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 25:779–790
Turney S, Buddle CM (2016) Pyramids of species richness: the determinants and distribution of species diversity across trophic levels. Oikos 125:1224–1233
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 11:296–310
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
Wallenstein MD, McMahon S, Schimel J (2007) Bacterial and fungal community structure in Arctic tundra tussock and shrub soils. FEMS Microbiol Ecol 59:428–435
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 107:283–294
Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886
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 6:595–600
Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA (2007) Patterns of bacterial diversity across a range of antarctic terrestrial habitats. Environ Microbiol 9:2670–2682
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 3:340–351
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 4:1206–1214
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.
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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.
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This article belongs to the special issue on the “Ecology of tundra arthropods,” coordinated by Toke T. Høye and Lauren E. Culler.
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Turney, S., Altshuler, I., Whyte, L.G. et al. Macroinvertebrate and soil prokaryote communities in the forest–tundra ecotone of the Subarctic Yukon. Polar Biol 41, 1619–1633 (2018). https://doi.org/10.1007/s00300-018-2330-5
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DOI: https://doi.org/10.1007/s00300-018-2330-5