Abstract
Invertebrate herbivores depend on external temperature for growth and metabolism. Continued warming in tundra ecosystems is proposed to result in increased invertebrate herbivory. However, empirical data about how current levels of invertebrate herbivory vary across the Arctic is limited and generally restricted to a single host plant or a small group of species, so predicting future change remains challenging. We investigated large-scale patterns of invertebrate herbivory across the tundra biome at the community level and explored how these patterns are related to long-term climatic conditions and year-of-sampling weather, habitat characteristics, and aboveground biomass production. Utilizing a standardized protocol, we collected samples from 92 plots nested within 20 tundra sites during summer 2015. We estimated the community-weighted biomass lost based on the total leaf area consumed by invertebrates for the most common plant species within each plot. Overall, invertebrate herbivory was prevalent at low intensities across the tundra, with estimates averaging 0.94% and ranging between 0.02 and 5.69% of plant biomass. Our results suggest that mid-summer temperature influences the intensity of invertebrate herbivory at the community level, consistent with the hypothesis that climate warming should increase plant losses to invertebrates in the tundra. However, most of the observed variation in herbivory was associated with other site level characteristics, indicating that other local ecological factors also play an important role. More details about the local drivers of invertebrate herbivory are necessary to predict the consequences for rapidly changing tundra ecosystems.
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References
Asmus AL, Chmura HE, Høye TT et al (2018) Shrub shading moderates the effects of weather on arthropod activity in arctic tundra. Ecol Entomol 43(5):647–655. https://doi.org/10.1111/een.12644
Bale JS, Masters GJ, Hodkinson ID et al (2002) Herbivory in global climate change research: direct effects of rising temperatures on insect herbivores. Glob Change Biol 8:1–16. https://doi.org/10.1046/j.1365-2486.2002.00451.x
Barrio IC, Hik DS, Peck K, Bueno CG (2013) After the frass: foraging pikas select patches previously grazed by caterpillars. Biol Lett 9:20130090. https://doi.org/10.1098/rsbl.2013.0090
Barrio IC, Bueno CG, Hik DS (2016a) Warming the tundra: reciprocal responses of invertebrate herbivores and plants. Oikos 125:20–28. https://doi.org/10.1111/oik.02190
Barrio IC, Hik DS, Jónsdóttir IS, Bueno CG, Mörsdorf MA, Ravolainen VT (2016b) Herbivory network: an international, collaborative effort to study herbivory in Arctic and alpine ecosystems. Polar Sci 10:297–302. https://doi.org/10.1016/j.polar.2016.03.001
Barrio IC, Lindén E, Te Beest M et al (2017) Background invertebrate herbivory on dwarf birch (Betula glandulosa-nana complex) increases with temperature and precipitation across the tundra biome. Polar Biol 40:2265–2278. https://doi.org/10.1007/s00300-017-2139-7
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Berg TB, Schmidt NM, Høye TT, Aastrup PJ, Hendrichsen DK, Forchhammer MC, Klein DR (2008) High-Arctic plant-herbivore interactions under climate influence. Adv Ecol Res 40:275–298. https://doi.org/10.1016/S0065-2504(07)00012-8
Bintanja R, Andry O (2017) Towards a rain-dominated Arctic. Nat Clim Change 7:263–267
Birkemoe T, Bergmann S, Hasle TE, Klanderud K (2016) Experimental warming increases herbivory by leaf-chewing insects in an alpine plant community. Ecol Evol 6(19):6955–6962. https://doi.org/10.1002/ece3.2398
Bolduc E, Casajus N, Legagneux P et al (2013) Terrestrial arthropod abundance and phenology in the Canadian Arctic: modelling resource availability for Arctic-nesting insectivorous birds. Can Entomol 145:155–170. https://doi.org/10.4039/tce.2013.4
Bonser SP, Reader RJ (1995) Plant competition and herbivory in relation to vegetation biomass. Ecology 76:2176–2183
Bråthen KA, Hagberg O (2004) More efficient estimation of plant biomass. J Veg Sci 15:653–660
Coupe MD, Cahill JFJ (2003) Effects of insects on primary production in temperate herbaceous communities: a meta-analysis. Ecol Entomol 28:511–521. https://doi.org/10.1046/j.1365-2311.2003.00540.x
Danks HV (1992) Arctic insects as indicators of environmental change. Arctic 45:159–166
Danks HV (2004) Seasonal adaptations in arctic insects. Integr Comp Biol 44:85–94. https://doi.org/10.1093/icb/44.2.85
Day TA, Ruhland CT, Xiong FS (2008) Warming increases aboveground plant biomass and C stocks in vascuar-plant-dominated Antarctic tundra. Glob Change Biol 14:1827–1843
Gamarra JGP, Callaghan TV, Bylund H, Gwynn-Jones D (2018) Larval crowding during an insect outbreak reduces herbivory pressure on preferred shrubs in a warmer environment. Agric For Meteorol 263:180–187. https://doi.org/10.1016/j.agrformet.2018.08.016
Gillespie MAK, Alfredsson M, Barrio IC et al (2019) Status and trends of terrestrial arthropod abundance and diversity in the North Atlantic region of the Arctic. Ambio. https://doi.org/10.1007/s13280-019-01162-5
Hansen RR, Hansen OLP, Bowden JJ, Treier UA, Normand S, Høye T (2016) Meter scale variation in shrub dominance and soil moisture structure Arctic arthropod communities. PeerJ 4:e2224. https://doi.org/10.7717/peerj.2224
Harris I, Jones PD, Osborn TJ, Lister DH (2014) Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 Dataset. Int J Climatol 34:623–642. https://doi.org/10.1002/joc.3711
Hodkinson ID, Bird J (1998) Host-specific insect herbivores as sensors of climate change in arctic and alpine environments. Arct Alp Res 30:78–83
Høye TT, Forchhammer MC (2008) The influence of weather conditions on the activity of high-arctic arthropods inferred from long-term observations. BMC Ecol 8(1):8. https://doi.org/10.1186/1472-6785-8-8
IPCC [Intergovernmental Panel on Climate Change] (2013) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Jactel H, Brockerhoff EG (2007) Tree diversity reduces herbivory by forest insects. Ecol Lett 10:835–848
Jepsen JU, Kapari L, Hagen SB, Schott T, Vindstad OPL, Nilssen AC, Ims RA (2011) Rapid northwards expansion of a forest insect pest attributed to spring phenology matching with sub-Arctic birch. Glob Change Biol 17:2071–2083. https://doi.org/10.1111/j.1365-2486.2010.02370.x
Jepsen JU, Biuw M, Ims RA, Kapari L, Schott T, Vindstad OPL, Hagen SB (2013) Ecosystem impacts of a range expanding forest defoliator at the forest-tundra ecotone. Ecosystems 16:561–575. https://doi.org/10.1007/s10021-012-9629-9
Kankaanpää T, Skov K, Abrego N, Lund M, Schmidt NM, Roslin T (2018) Spatiotemporal snowmelt patterns within a high Arctic landscape—with implications for flora and fauna. Arctic, Antarct Alp Res 50:e115624. https://doi.org/10.1080/15230430.2017.1415624
Karlsen SR, Jepsen JU, Odland A, Ims RA, Elvebakk A (2013) Outbreaks by canopy-feeding geometrid moth cause state-dependent shifts in understorey plant communities. Oecologia 173:859–870. https://doi.org/10.1007/s00442-013-2648-1
Kaukonen M, Ruotsalainen AL, Wäli PR et al (2013) Moth herbivory enhances resource turnover in subarctic mountain birch forests? Ecology 94:267–272
Kharouba HM, Vellend M, Sarfraz RM, Myers JH (2015) The effects of experimental warming on the timing of a plant—insect herbivore interaction. J Anim Ecol 84:785–796. https://doi.org/10.1111/1365-2656.12328
Kotanen PM, Rosenthal JP (2000) Tolerating herbivory: does the plant care if the herbivore has a backbone? Evol Ecol 14:537–549. https://doi.org/10.1023/A:1010862201331
Kozlov MV (2008) Losses of birch foliage due to insect herbivory along geographical gradients in Europe: a climate-driven pattern? Clim Change 87:107–117. https://doi.org/10.1007/s10584-007-9348-y
Kozlov MV, Zvereva EL (2015) Changes in the background losses of woody plant foliage to insects during the past 60 years: are the predictions fulfilled? Biol Lett 11(7):20150480. https://doi.org/10.1098/rsbl.2015.0480
Kozlov MV, Zvereva EL (2017) Background insect herbivory: impacts, patterns and methodology. Prog Bot 79:315–355. https://doi.org/10.1007/124_2017_4
Kozlov MV, van Nieukerken EJ, Zverev V, Zvereva EL (2013) Abundance and diversity of birch-feeding leafminers along latitudinal gradients in northern Europe. Ecography (Cop) 36:1138–1149. https://doi.org/10.1111/j.1600-0587.2013.00272.x
Kozlov MV, Zverev V, Zvereva EL (2014) Confirmation bias leads to overestimation of losses of woody plant foliage to insect herbivores in tropical regions. PeerJ 2:e709. https://doi.org/10.7717/peerj.709
Kozlov MV, Filippov BY, Zubrij NA, Zverev V (2015a) Abrupt changes in invertebrate herbivory on woody plants at the forest–tundra ecotone. Polar Biol 38:967–974. https://doi.org/10.1007/s00300-015-1655-6
Kozlov MV, Lanta V, Zverev V, Zvereva EL (2015b) Global patterns in background losses of woody plant foliage to insects. Glob Ecol Biogeogr 24:1126–1135. https://doi.org/10.1111/geb.12347
Kozlov MV, Zverev V, Zvereva EL (2017) Combined effects of environmental disturbance and climate warming on insect herbivory in mountain birch in subarctic forests: results of 26-year monitoring. Sci Total Environ 601–602:802–811. https://doi.org/10.1016/j.scitotenv.2017.05.230
Lund M, Raundrup K, Westergaard-nielsen A, López-Blanco E, Nymand J, Aastrup P (2017) Larval outbreaks in West Greenland: instant and subsequent effects on tundra ecosystem productivity and CO2 exchange. Ambio 46:26–38. https://doi.org/10.1007/s13280-016-0863-9
MacLean SF Jr, Jensen TS (1985) Food plant selection by insect herbivores in Alaskan arctic tundra: the role of plant life form. Oikos 44:211–221
Metcalfe DB, Crutsinger GM, Kumordzi BB, Wardle DA (2016) Nutrient fluxes from insect herbivory increase during ecosystem retrogression in boreal forest. Ecology 97:124–132. https://doi.org/10.1890/15-0302.1
Myers-Smith IH, Elmendorf SC, Beck PSA et al (2015) Climate sensitivity of shrub growth across the tundra biome. Nat Clim Change 5:887–891. https://doi.org/10.1038/nclimate2697
Onoda Y, Westoby M, Adler PB et al (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312
Overland JE, Hanna E, Hanssen-Bauer I, et al (2017) Surface air temperature in Arctic Report Card 2017
Post E, Pedersen C (2008) Opposing plant community responses to warming with and without herbivores. Proc Natl Acad Sci USA 105:12353–12358. https://doi.org/10.1073/pnas.0802421105
Post E, Forchhammer MC, Bret-Harte MS et al (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358. https://doi.org/10.1126/science.1173113
Pureswaran DS, Neau M, Marchand M, de Grandpré L, Kneeshaw D (2019) Phenological synchrony between eastern spruce budworm and its host trees increases with warmer temperatures in the boreal forest. Ecol Evol 9:576–586. https://doi.org/10.1002/ece3.4779
R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rheubottom SI (2018) Measuring background levels of invertebrate herbivory in the arctic tundra. MSc thesis, University of Alberta, Canada
Rich ME, Gough L, Boelman NT (2013) Arctic arthropod assemblages in habitats of differing shrub dominance. Ecography 36:001–010. https://doi.org/10.1111/j.1600-0587.2012.00078.x
Roskov, Y, Abucay, L, Orrell T, et al (2017) Species 2000 & ITIS Catalogue of life, 2017 annual checklist. www.catalogueoflife.org/annual-checklist/2017
Semenchuk PR, Elberling B, Amtorp C, Winkler J, Rumpf S, Michelsen A, Cooper EJ (2015) Deeper snow alters soil nutrient availability and leaf nutrient status in high Arctic tundra. Biogeochemistry 124:81–94. https://doi.org/10.1007/s10533-015-0082-7
Strathdee AT, Bale JS (1998) Life on the edge: insect ecology in arctic environments. Annu Rev Entomol 43:85–106. https://doi.org/10.1146/annurev.ento.43.1.85
Suominen O, Danell K, Bryant JP (1999) Indirect effects of mammalian browsers on vegetation and ground-dwelling insects in an Alaskan floodplain. Ecoscience 6:505–510. https://doi.org/10.1080/11956860.1999.11682554
Suominen O, Niemelä J, Martikainen P, Niemelä P, Kojola I (2003) Impact of reindeer grazing on ground-dwelling Carabidae and Curculionidae assemblages in Lapland. Ecography 26:503–513. https://doi.org/10.1034/j.1600-0587.2003.03445.x
Torp M, Olofsson J, Witzell J, Baxter R (2010a) Snow-induced changes in dwarf birch chemistry increase moth larval growth rate and level of herbivory. Polar Biol 33:693–702. https://doi.org/10.1007/s00300-009-0744-9
Torp M, Witzell J, Baxter R, Olofsson J (2010b) The effect of snow on plant chemistry and invertebrate herbivory: experimental manipulations along a natural snow gradient. Ecosystems 13:741–751. https://doi.org/10.1007/s10021-010-9351-4
Tscharntke T, Greiler H-J (1995) Insect communities, grasses, and grasslands. Annu Rev Entomol 40:535–558
Turcotte MM, Davies TJ, Thomsen CJM, Johnson MTJ (2014) Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants. Proc R Soc B 281:20140555
Virtanen R, Oksanen L, Oksanen T et al (2016) Where do the treeless tundra areas of northern highlands fit in the global biome system: toward an ecologically natural subdivision of the tundra biome. Ecol Evol 6:143–158. https://doi.org/10.1002/ece3.1837
Walker DA, Raynolds MK, Daniëls FJA et al (2005) The circumpolar Arctic vegetation map. J Veg Sci 16:267–282
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Zvereva EL, Kozlov MV (2019) Biases in studies of spatial patterns in insect herbivory. Ecol Monogr 89(3):e01361. https://doi.org/10.1002/ecm.1361
Zvereva EL, Zverev V, Kozlov MV (2012) Little strokes fell great oaks: Minor but chronic herbivory substantially reduces birch growth. Oikos 121:2036–2043. https://doi.org/10.1111/j.1600-0706.2012.20688.x
Zvereva EL, Hunter MD, Zverev V, Kozlov MV (2016) Factors affecting population dynamics of leaf beetles in a subarctic region: the interplay between climate warming and pollution decline. Sci Total Environ 566–567:1277–1288
Acknowledgements
This study is a contribution of the Herbivory Network (https://herbivory.lbhi.is). SIR and DSH were supported by the Natural Sciences and Engineering Research Council of Canada (RGPNS-305471); ICB was supported by a postdoctoral fellowship funded by the Icelandic Research Fund (Rannsóknasjóður, Grant nr 152468–051) and AXA Research Fund (15-AXA-PDOC-307); JMA was supported by Carl Tryggers Stiftelse för Vetenskaplig Forskning (Sweden) and Qatar Petroleum; MVK and VZ were supported by the Academy of Finland (Project 276671); AS and NS were supported by the Grant of Russian fund for basic research (18-05-60261); Field work on Bylot Island was supported by the Natural Sciences and Engineering Research Council of Canada, the network of Center of excellence ArcticNet, and the Polar Continental Shelf Program to GG and EL; SK and the Burntpoint Creek Research Station was supported by the Waterfowl, Wetlands and Far North research unit of the Ontario Ministry of Natural Resources and Forestry, with assistance from K. Bennet, R. Brook, and L. Pollock; O. Krasheninnikova assisted with the collection plant samples on Erkuta; SS was partly supported by a state assignment of the Institute of Plant and Animal Ecology UB RAS; DDE was supported by a Grant to JO from the Swedish Research Council Formas 2012–1039, 2012–230, 2015–1091 and a Grant to DDE from Gunnar and Ruth Björkmans fund for botanical research in northern Sweden; Sampling in Svalbard was conducted during an UNIS field course (ISJ); JSP was supported by the WSL Institute for Snow and Avalanche Research, and an INTERACT Transnational Access Research Grant; Research at Toolik Field Station by ALA was supported by National Science Foundation Grants DEB 102683 to support the Arctic LTER and OPP 0908502; JDMS was supported by the Research Council of Norway (262064); C. Brachmann assisted with Fig. 1; H.C. Proctor and B.A. Keddie assisted with gall damage determination.
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Rheubottom, S.I., Barrio, I.C., Kozlov, M.V. et al. Hiding in the background: community-level patterns in invertebrate herbivory across the tundra biome. Polar Biol 42, 1881–1897 (2019). https://doi.org/10.1007/s00300-019-02568-3
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DOI: https://doi.org/10.1007/s00300-019-02568-3