Abstract
Chronic, low intensity herbivory by invertebrates, termed background herbivory, has been understudied in tundra, yet its impacts are likely to increase in a warmer Arctic. The magnitude of these changes is however hard to predict as we know little about the drivers of current levels of invertebrate herbivory in tundra. We assessed the intensity of invertebrate herbivory on a common tundra plant, the dwarf birch (Betula glandulosa-nana complex), and investigated its relationship to latitude and climate across the tundra biome. Leaf damage by defoliating, mining and gall-forming invertebrates was measured in samples collected from 192 sites at 56 locations. Our results indicate that invertebrate herbivory is nearly ubiquitous across the tundra biome but occurs at low intensity. On average, invertebrates damaged 11.2% of the leaves and removed 1.4% of total leaf area. The damage was mainly caused by external leaf feeders, and most damaged leaves were only slightly affected (12% leaf area lost). Foliar damage was consistently positively correlated with mid-summer (July) temperature and, to a lesser extent, precipitation in the year of data collection, irrespective of latitude. Our models predict that, on average, foliar losses to invertebrates on dwarf birch are likely to increase by 6–7% over the current levels with a 1 °C increase in summer temperatures. Our results show that invertebrate herbivory on dwarf birch is small in magnitude but given its prevalence and dependence on climatic variables, background invertebrate herbivory should be included in predictions of climate change impacts on tundra ecosystems.
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12 March 2018
The above mentioned article was originally scheduled for publication in the special issue on Ecology of Tundra Arthropods with guest editors Toke T. Høye . Lauren E. Culler. Erroneously, the article was published in Polar Biology, Volume 40, Issue 11, November, 2017. The publisher sincerely apologizes to the guest editors and the authors for the inconvenience caused.
References
Agrawal A, Weber M (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18:985–991
Andrew NR, Hughes L (2005) Herbivore damage along a latitudinal gradient: relative impacts of different feeding guilds. Oikos 108:176–182
Anstett DN, Naujokaitis-Lewis I, Johnson MTJ (2014) Latitudinal gradients in herbivory on Oenothera biennis vary according to herbivore guild and specialization. Ecology 95:2915–2923
Anstett D, Ahern J, Glinos J et al (2015) Can genetically based clines in plant defence explain greater herbivory at higher latitudes? Ecol Lett 18:1376–1386
Anstett DN, Nunes KA, Baskett C, Kotanen PM (2016) Sources of controversy surrounding latitudinal patterns in herbivory and defense. Trends Ecol Evol 31:789–802
Bale JS, Masters GJ, Hodkinson ID et al (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Chang Biol 8:1–16
Barrio IC, Bueno CG, Hik DS (2016) Warming the tundra: reciprocal responses of invertebrate herbivores and plants. Oikos 125:20–28
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Batzli GO, White RG, MacLean SF et al (1980) The herbivore-based ecosystem. In: Brown J, Miller PC, Tieszen LL, Bunnell FL (eds) An arctic ecosystem: the coastal tundra at Barrow. Hutchinson & Ross, Alaska, pp 335–410
Birkemoe T, Bergmann S, Hasle TE, Klanderud K (2016) Experimental warming increases herbivory by leaf-chewing insects in an alpine plant community. Ecol Evol 6:6955–6962
Björkman C, Berggren A, Bylund H (2011) Causes behind insect folivory patterns in latitudinal gradients. J Ecol 99:367–369
Bret-Harte MS, Shaver GR, Zoerner JP et al (2001) Developmental plasticity allows Betula nana to dominate tundra subjected to an altered environment. Ecology 82:18–32
Bryant JP, Joly K, Chapin FS et al (2014) Can antibrowsing defense regulate the spread of woody vegetation in arctic tundra? Ecography 37:204–211
Carmona D, Lajeunesse MJ, Johnson MT (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367
Carneiro MAA, Fernandes GW, De Souza OFF (2005) Convergence in the variation of local and regional galling species richness. Neotrop Entomol 34:547–553
CAVM Team (2003) Circumpolar Arctic Region Bioclimate Subzones. Scale 1:7,500,000
Coley P, Aide T (1991) Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In: Price P, Lewinsohn T, Fernandes G, Benson W (eds) Plant-animal interaction: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 25–49
Cook BI, Smerdon JE, Seager R, Coats S (2014) Global warming and 21st century drying. Clim Dyn 43:2607–2627
Danks HV (1986) Insect plant interactions in arctic regions. Rev d’Entomologie du Québec 31:52–75
DeAngelis DL, Bryant JP, Liu R et al (2015) A plant toxin mediated mechanism for the lag in snowshoe hare population recovery following cyclic declines. Oikos 124:796–805
Elmendorf SC, Henry GHR, Hollister RD et al (2012) Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol Lett 15:164–175
Euskirchen ES, Mcguire AD, Chapin FS et al (2009) Changes in vegetation in Northern Alaska under scenarios of climate change, 2003–2100: implications for climate feedbacks. Ecol Appl 19:1022–1043
Feilberg J (1984) A phytogeographical study of South Greenland: vascular plants. Medd Grønland Biosci 15:70
Fisher AE, Hartley S, Young M (1999) Behavioural responses of the leaf-chewing guild to the presence of Eriocrania mines on silver birch (Betula pendula). Ecol Entomol 24:156–162
Graglia E, Julkunen-Tiitto R, Shaver GR et al (2001) Environmental control and intersite variations of phenolics in Betula nana in tundra ecosystems. New Phytol 151:227–236
Greyson-Gaito CJ, Barbour MA, Rodriguez-Cabal MA et al (2016) Freedom to move: arctic caterpillar (Lepidoptera) growth rate increases with access to new willows (Salicaceae). Can Entomol 148:673–682
Haukioja E (1981) Invertebrate herbivory at tundra sites. In: Bliss LC, Heal OW, Moore JJ (eds) Tundra ecosystems: a comparative analysis. Cambridge University Press, New York, pp 547–555
Hiura T, Nakamura M (2013) Different mechanisms explain feeding type-specific patterns of latitudinal variation in herbivore damage among diverse feeding types of herbivorous insects. Basic Appl Ecol 14:480–488
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
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
Jepsen JU, Hagen SB, Ims RA, Yoccoz NG (2008) Climate change and outbreaks of the geometrids Operophtera brumata and Epirrita autumnata in subarctic birch forest: evidence of a recent outbreak range expansion. J Anim Ecol 77:257–264
Jepsen JU, Biuw M, Ims RA et al (2013) Ecosystem impacts of a range expanding forest defoliator at the forest-tundra ecostone. Ecosystems 16:561–575
Johnson MTJ, Rasmann S (2011) The latitudinal herbivory-defence hypothesis takes a detour on the map. New Phytol 191:589–592
Kaukonen M, Ruotsalainen AL, Wali P et al (2013) Moth herbivory enhances resource turnover in subarctic mountain birch forests? Ecology 94:267–272
Koponen S (1984) Abundance of herbivorous insects on dwarf birch near the treeline in Alaska. Rep Kevo Subarct Res Stn 19:19–24
Kotanen PM, Rosenthal JP (2000) Tolerating herbivory: does the plant care if the herbivore has a backbone? Evol Ecol 14:537–549
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
Kozlov MV, Zvereva EL (2017) Background insect herbivory: impacts, patterns and methodology. In: Cánovas FM, Lüttge U, Matyssek R (eds) Progress in Botany, vol 79. Springer, Heidelberg. doi: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 36:1138–1149
Kozlov MV, Lanta V, Zverev V, Zvereva EL (2015a) Global patterns in background losses of woody plant foliage to insects. Glob Ecol Biogeogr 24:1126–1135
Kozlov MV, Filippov BY, Zubrij NA, Zverev V (2015b) Abrupt changes in invertebrate herbivory on woody plants at the forest-tundra ecotone. Polar Biol 38:967–974
Kozlov MVM, Skoracka A, Zverev V et al (2016) Two birch species demonstrate opposite latitudinal patterns in infestation by gall-making mites in Northern Europe. PLoS ONE 11:e0166641
Lawrimore JH, Menne MJ, Gleason BE et al (2011) An overview of the global historical climatology network monthly mean temperature data set, version 3. J Geophys Res 116:D19121
Leckey EH, Smith DM, Nufio CR, Fornash KF (2014) Oak-insect herbivore interactions along a temperature and precipitation gradient. Acta Oecologica 61:1–8
Lim JY, Fine PVA, Mittelbach GG (2015) Assessing the latitudinal gradient in herbivory. Glob Ecol Biogeogr 24(10):1–7
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
Moles AT, Bonser SP, Poore AGB et al (2011) Assessing the evidence for latitudinal gradients in plant defence and herbivory. Funct Ecol 25:380–388
Moreira X, Abdala-Roberts L, Parra-Tabla V, Mooney KA (2015) Latitudinal variation in herbivory: influences of climatic drivers, herbivore identity and natural enemies. Oikos 124:1444–1452
Myers-Smith IH, Forbes BC, Wilmking M et al (2011) Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett 6:45509
Myers-Smith IH, Elmendorf SC, Beck PSA et al (2015) Climate sensitivity of shrub growth across the tundra biome. Nat Clim Chang 5:887–891
Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268
Olofsson J, te Beest M, Ericson L (2013) Complex biotic interactions drive long-term vegetation dynamics in a subarctic ecosystem. Philos Trans R Soc Lond B 368:20120486
Onoda Y, Westoby M, Adler PB et al (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312
Parker TC, Sadowsky J, Dunleavy H et al (2017) Slowed biogeochemical cycling in sub-arctic birch forest linked to reduced mycorrhizal growth and community change after a defoliation event. Ecosystems 20:316–330
Pennings SC, Ho C, Salgado CS et al (2009) Latitudinal variation in herbivore pressure in Atlantic coast salt marshes. Ecology 90:183–195
Post E, Pedersen C (2008) Opposing plant community responses to warming with and without herbivores. Proc Natl Acad Sci USA 105:12353–12358
Prevéy J, Vellend M, Rüger N et al (2017) Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes. Glob Chang Biol. doi:10.1111/gcb.13619
R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Richardson SJ, Press MC, Parsons AN, Hartley SE (2002) How do nutrients and warming impact on plant communities and their insect herbivores? A 9 year study from a sub-Arctic heath. J Ecol 90:544–556
Roy BA, Gusewell S, Harte J (2004) Response of plant pathogens and herbivores to a warming experiment. Ecology 85:2570–2581
Sinclair RJ, Hughes L (2008) Incidence of leaf mining in different vegetation types across rainfall, canopy cover and latitudinal gradients. Austral Ecol 33:353–360
Speed JD, Austrheim G, Hester AJ, Mysterud A (2011) Browsing interacts with climate to determine tree-ring increment. Funct Ecol 25:1018–1023
Speed JDM, Austrheim G, Hester AJ, Mysterud A (2013) The response of alpine Salix shrubs to long-term browsing varies with elevation and herbivore density. Arctic, Antarct Alp Res 45:584–593
Stark S, Väisänen M, Ylänne H et al (2015) Decreased phenolic defence in dwarf birch (Betula nana) after warming in subarctic tundra. Polar Biol 38:1993–2005
Torp M, Witzell J, Baxter R, Olofsson J (2010) The effect of snow on plant chemistry and invertebrate herbivory: experimental manipulations along a natural snow gradient. Ecosystems 13:741–751
Viramo J (1962) Über die an der Zwergbirke (Betula nana L.) minierenden Insektenarten. Ann Entomol Fenn 28:118–126
Wilf P, Labandeira CC (1999) Response of plant-insect associations to Paleocene–Eocene warming. Science 284:2153–2156
Wilf P, Labandeira CC, Johnson KR et al (2001) Insect herbivory, plant defense and early Cenozoic climate change. Proc Natl Acad Sci 98:6221–6226
Wolf A, Kozlov MV, Callaghan TV (2008) Impact of non-outbreak insect damage on vegetation in northern Europe will be greater than expected during a changing climate. Clim Chang 87:91–106
Zhang S, Zhang Y, Ma K, Shefferson R (2016) Latitudinal variation in herbivory: hemispheric asymmetries and the role of climatic drivers. J Ecol 104:1089–1095
Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Zvereva EL, Zverev V, Kozlov MV (2012) Little strokes fell great oaks: minor but chronic herbivory substantially reduces birch growth. Oikos 121:2036–2043
Acknowledgements
This study is a joint contribution of the Herbivory Network (http://herbivory.biology.ualberta.ca) and the Network for Arthropods of the Tundra (NeAT; https://tundraarthropods.wordpress.com/). Dwarf birch distribution maps were kindly provided by Kyle Joly. Sample collection during 2014 was facilitated by INTERACT (http://www.eu-interact.org/). 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); MtB and EK were supported by the Nordic Centre of Excellence TUNDRA, funded by the Norden Top-Level Research Initiative ‘‘Effect Studies and Adaptation to Climate Change’’; EMS and KAB were supported by COAT (Climate-ecological Observatory of the Arctic Tundra); AB was supported by MOBILITY PLUS (1072/MOB/2013/0) and the Polish-American Fulbright Commission; CGB was supported by IUT 20-28, EcolChang e Center of Excellence; BCF and TK were supported by the Academy of Finland (project 256991); MMPDH was supported by The Netherlands Organization for Scientific Research (NWO-ALW, VIDI grant 864.09.014); DSH was supported by the Natural Sciences and Engineering Research Council of Canada; AH was supported by the Research Council of Norway (grant 244557/E50); JL was funded by the German Research Foundation DFG (project WI 2680/8-1); MM-F was supported by a NERC IRF fellowship NE/L011859/1; SN was supported by the Villum foundation’s Young Investigator Programme (VKR023456); JS was supported by Kempestiftelserna and the Research Foundation Flanders (FWO); AS and NS were supported by the grant of RFBR (project 16-44-890108), grant of UB of RAS (project 15-15-4-35) and IEC “Arctic” of Yamal Government Department of Science and Innovation; LES and PAW were supported by the UK Natural Environment Research Council (NERC) grant NE/K000284/1; MVK and VZ were supported by the Academy of Finland (project 276671).
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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.
A correction to this article is available online at https://doi.org/10.1007/s00300-018-2305-6.
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Barrio, I.C., Lindén, E., Te Beest, M. et al. Background invertebrate herbivory on dwarf birch (Betula glandulosa-nana complex) increases with temperature and precipitation across the tundra biome. Polar Biol 40, 2265–2278 (2017). https://doi.org/10.1007/s00300-017-2139-7
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DOI: https://doi.org/10.1007/s00300-017-2139-7