Abstract
Rates of decomposition in Arctic soils are regulated by temperature and moisture, but substrate availability is dictated by vegetation inputs, which are also subject to biotic influences. Here, we examine how leaf and litter inputs from individual dwarf shrub species influence soil enzyme activity in a sub-Arctic heath community in Abisko, Sweden. We further consider how foliar damage via insect herbivory (and outbreak) affects the soil community and decomposition. During the peak growing season (July 2011), we assessed how shrub community composition (Empetrum hermaphroditum, Vaccinium myrtillus, V. uliginosum and V. vitis-idaea) determined litter and soil phenol oxidase activity. A periodic severe outbreak of autumn moth larvae (Epirrita autumnata) affected this community in the following year (July 2012), and we used this to investigate its impact on relationships with phenol oxidase activity, soil respiration, soluble NH4 + and soluble phenolics; the soluble factors being directly associated with inputs from insect larval waste (frass). Pre-outbreak (2011), the strongest relationship observed was higher phenol oxidase activity with E. hermaphroditum cover. In the outbreak year (2012), phenol oxidase activity had the strongest relationship with damage to the deciduous species V. myrtillus, with greater herbivory lowering activity. For the other deciduous species, V. uliginosum, soil NH4 + and phenolics were negatively correlated with foliar larval damage. Phenol oxidase activity was not affected by herbivory of the evergreen species, but there was a strong positive relationship observed between E. hermaphroditum community abundance and soil respiration. We highlight the dominant role of E. hermaphroditum in such sub-Arctic shrub communities and show that even during insect outbreaks, it can dictate soil processes.
Similar content being viewed by others
References
Allen SE (1974) Chemical analysis of ecological materials. Wiley, New York
Allison SD (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochemistry 81:361–373
Bajwa R, Abuarghub S, Read DJ (1985) The biology of mycorrhiza in the Ericaceae. N Phytol 101:469–486
Barbehenn RV, Martin MM (1992) The protective role of the peritrophic membrane in the tannin-tolerant larvae of Orgyia leucostigma (Lepidoptera). J Insect Physiol 38:973–980
Bardgett RD, Wardle DA (2003) Herbivore mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268
Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641
Bardgett RD, Manning P, Morrien E, Vries FT (2013) Hierarchical responses of plant–soil interactions to climate change: consequences for the global carbon cycle. J Ecol 101:334–343
Bending GD, Read DJ (1995) The structure and function of the vegetative mycelium of ectomycorrhizal plants. V. Foraging behaviour and translocation of nutrients from exploited litter. N Phytol 130:401–409
Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49:637–644
Cornelissen JHC, Aerts R, Cerabolini B, Werger MJA, van der Heijden MGA (2001) Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129:611–619
Crawley MJ (2009) The R book. Wiley, New York
Dorrepaal E, Cornelissen JHC, Aerts R (2007) Changing leaf litter feedbacks on plant production across contrasting sub-arctic peatland species and growth forms. Oecologia 151:251–261
Dorrepaal E, Toet S, van Logtestijn RSP, Swart E, van de Weg MJ, Callaghan TV, Aerts R (2009) Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460:616–619
Flanagan PW, Veum AK (1974) Relationships between respiration, weight loss, temperature and moisture in organic residues in tundra. In: Holding AJ, Heal OW, MacLean SF Jr, Flanagan PW (eds) Soil organisms and decomposition in tundra. Tundra Biome Steering Committee, Stockholm, pp 249–278
Freeman C, Ostle NJ, Kang H (2001) An enzymic ‘latch’ on a global carbon store. Nature 401:149
Frost C, Hunter MD (2004) Insect canopy herbivory and frass deposition affect soil nutrient dynamics and export in oak mesocosms. Ecology 85:3335–3347
German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397
Gundale MJ, Sverker J, Albrectsen BR, Nilsson MC, Wardle DA (2010) Variation in protein complexation capacity among and within six plant species across a boreal forest chronosequence. Plant Ecol 211:253–266
Hagen SB, Jepsen JU, Ims RA, Yoccoz NG (2007) Shifting altitudinal distribution of outbreak zones of winter moth Operophtera brumata in sub-arctic birch forest: a response to recent climate warming? Ecography 30:299–307
Hansen AH, Jonasson S, Michelsen A, Julkunen-Tiitto R (2006) Long-term experimental warming, shading and nutrient addition affect the concentration of phenolic compounds in arctic-alpine deciduous and evergreen dwarf shrubs. Oecologia 147:1–11
Hattenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243
Henry HAL (2012) Soil extracellular enzyme dynamics in a changing climate. Soil Biol Biochem 47:53–59
Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol Evol 7:336–339
Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Mono 66:503–522
Hobbie SE (2008) Nitrogen effects on decomposition: a five-year experiment in eight temperate sites. Ecology 89:2633–2644
Hobbie SE, Schimel JP, Trumbore SE, Randerson JR (2000) Controls over carbon storage and turnover in high-latitude soils. Glob Change Biol 6:196–210
Hobbie SE, Nadelhoffer KJ, Högberg P (2002) A synthesis: the role of nutrients as constraints on carbon balances in boreal and arctic regions. Plant Soil 242:163–170
Jefferies RL, Walker NA, Edwards KA, Dainty J (2010) Is the decline of soil microbial biomass in late winter coupled to changes in the physical state of cold soils? Soil Biol Biochem 42:129–135
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
Kardol P, Cregger MA, Campany CE, Classen AT (2010) Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91:767–781
Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143
Kourtev PS, Ehrenfeld JG, Haggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905
Lovett GM, Christenson LM, Groffman PM, Jones CG, Hart JE, Mitchell MJ (2002) Insect defoliation and nitrogen cycling in forests. Bioscience 52:335–341
Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS III (2004) Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–443
Metcalfe DB, Asner GP, Martin RE et al (2014) Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol Lett 17:324–332
Morin K (2013) Mapping moth induced birch forest damage in northern Sweden, with MODIS satellite data. Student thesis series INES nr 267. Lund University
Nemergut DR, Townsend AR, Sattin SR et al (2008) The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ Microbiol 10:3093–3105
Oksanen L, Virtanen R (1995) Topographic, altitudinal and regional patterns in North Fennoscandian continental and suboceanic heath vegetation. Acta Botanica Fennica 153:1–80
Olofsson J, Oksanen L, Gallaghan T, Hulme PE, Oksanen T, Suominen O (2009) Herbivores inhibit climate-driven shrub expansion on the tundra. Glob Change Biol 15:2681–2693
Pind A, Freeman C, Lock MA (1994) Enzymatic degradation of phenolic materials in peatlands-measurement of phenol oxidase activity. Plant Soil 159:227–231
Post E, Forchhammer MC, Bret-Harte MS et al (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358
R Development Core Team (2011) R: a language and environment for statistical computing, reference index version 2.12.2. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 11 Feb 2011
Semerdjieva SI, Sheffield E, Phoenix GK, Gwynn-Jones D, Callaghan TV, Johnson GN (2003) Contrasting strategies for UV-B screening in sub-arctic dwarf shrubs. Plant Cell Environ 26:957–964
Shaver GR, Chapin FS III (1980) Response to fertilisation by various plant growth forms in an Alaskan tundra: nutrient accumulation and growth. Ecology 61:662–675
Shen SM, Pruden G, Jenkinson DS (1984) Mineralization and immobilization of nitrogen in fumigated soil and the measurement of microbial biomass nitrogen. Soil Biol Biochem 16:437–444
Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Methods Enzymol 299:152–178
Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404
Sinsabaugh RL, Lauber CL, Weintraub MN (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264
Sistla SA, Schimel JP (2013) Seasonal patterns of microbial extracellular enzyme activities in an arctic tundra soil: identifying direct and indirect effects of long-term summer warming. Soil Biol Biochem 66:119–129
Sonesson M, Lundberg B (1974) Late Quaternary forest development of the Torneträsk area, North Sweden. Oikos 25:121–133
Stafford HA (1988) Proanthocyanidins and the lignin connection. Phytochemistry 27:1–6
Tenow O (1972) The outbreaks of Oporinia autumnata Bkh. and Operopthera spp. (Lep., Geometridae) in the Scandinavian mountain chain and northern Finland 1862–1968. Zoologiska bidrag från Uppsala Suppl 2:1–107
Tukey HB, Morgan JV (1963) Injury to foliage and its effects upon the leaching of nutrients from above-ground plant parts. Physiologia Planta 16:557–564
Tybirk K, Nilsson MC, Michelsen A, Kristensen HL, Shevtsova A, Strandberg TM, Johansson M, Nielsen KE, Riis-Nielsen T, Strandberg B, Johnsen I (2000) Nordic Empetrum dominated ecosystems: function and susceptibility to environmental changes. Ambio 29:90–97
Ushio M, Kitayama K, Balser TC (2010) Tree species effects on soil enzyme activities through effects on soil physicochemical and microbial properties in a tropical montane forest on Mt. Kinabalu, Borneo. Pedobiologia 53:227–233
van Aarle IM, Plassard C (2010) Spatial distribution of phosphatase activity associated with ectomycorrhizal plants is related to soil type. Soil Bio Biochem 42:324–330
Wallenstein MD, McMahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Change Biol 15:1631–1639
Weedon J, Aerts R, Kowalchuk G, van Bodegom P (2011) Enzymology under global change: organic nitrogen turnover in alpine and sub-Arctic soils. Biochem Soc Trans 39:309
Wookey PA, Aerts R, Bardgett RD et al (2009) Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change. Glob Change Biol 15:1153–1172
Zak DR, Kling GW (2006) Microbial community composition and function across an Arctic tundra landscape. Ecology 87:1659–1670
Acknowledgments
The authors gratefully acknowledge the support of NERC Grant NE/H021949/1 and staff at Abisko Scientific Research (Naturvetenskapliga) Station, Sweden.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jones, A.G., Scullion, J., Ostle, N. et al. Plant community composition and an insect outbreak influence phenol oxidase activity and soil–litter biochemistry in a sub-Arctic birch heath. Polar Biol 38, 505–516 (2015). https://doi.org/10.1007/s00300-014-1613-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-014-1613-8