Ungulates can greatly affect forest ecosystems’ functional characteristics. However, limited information is available about their influence on litter decomposition, a major ecosystem process, despite disturbance of ungulates on vegetation through selective browsing and trampling. This study focused on effects of the presence/absence of deer herbivory on decomposition of leaves and roots of three major tree species in a Hokkaido, Japan forest. Our litterbag experiment showed that litter decomposition was significantly faster for both leaves and roots in a deer exclosure than in a control site with deer herbivory. Possible factors for this slowed decomposition because of deer presence include their physical disturbance on soil through trampling. In both sites, the remaining mass of litter was positively correlated with the C:N ratio and lignin content. When analyzed for leaf litter, species with lower C:N ratio and lignin content showed lower litter mass remaining in both sites. Deer generally prefer species with a low leaf C:N ratio and lignin content; the results suggest that leaves of palatable species were less resistant to decomposition. A similar interspecific difference in decomposition was not observed for roots, most likely resulting from the small difference in root litter quality among species. In this forest, tree species with unpalatable leaves, which are becoming predominant, likely decreases leaf litter decomposition, as leaves of palatable plants decompose more rapidly. Roots, however, are not exposed to browsing, regardless of aboveground palatability, and remain within soil as a recalcitrant slowly decomposing litter substrate. These synergetic influences could allow deer herbivory to reduce overall plant decomposition rates aboveground and belowground via changes in plant species composition.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Aber JD, Melillo JM, McClaugherty CA (1990) Predicting long-term patterns of mass loss, nitrogen dynamics and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems. Can J Bot 68:2201–2208
Bardgett RD (2005) The biology of soil: a community and ecosystem approach. Oxford University Press, Oxford
Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268
Bardgett RD, Wardle DA, Yeates GW (1998) Linking above-ground and below-ground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30:1867–1878
Berg B, McClaugherty C (2003) Plant litter: decomposition, humus formation, carbon sequestration. Springer, Tokyo
Blair JM (1988) Nitrogen, sulfur and phosphorus dynamics in decomposing deciduous leaf litter in the southern appalachians. Soil Biol Biochem 20:693–701
Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci USA 104:4990–4995
Chen H, Harmon ME, Sexton J, Fasth B (2002) Fine-root decomposition and N dynamics in coniferous forests of the Pacific Northwest, USA. Can J For Res 32:320–331
Connor HE, Bailey RW (1972) Leaf strength in four species of Chionochloa (Arundineae). N Z J Bot 10:515–532
Cooke AS (1997) Effects of grazing by muntjac (Muntiacus reevesi) on bluebells (Hyacinthoides non-scripta) and a technique for assessing feeding activity. J Zool 242:365–369
Cornelissen JHC, Pérez-Harguindeguy N, Díaz S, Grime JP, Marzano B, Cabido M, Vendramini F, Cerabolini B (1999) Leaf structure and defence control litter decomposition rate across species and life forms in regional floras on two continents. New Phytol 143:191–200
Craine JM, Lee WG, Bond WJ, Williams RJ, Johnson LC (2005) Environmental constraints on a global relationship among leaf and root traits of grasses. Ecology 86:12–19
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Fahey TJ, Hughes JW, Mou Pu, Arthur MA (1988) Root decomposition and nutrient flux following whole-tree harvest of northern hardwood forest. For Sci 34:744–768
Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004) Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–320
Freschet GT, Cornwell WK, Wardle DA, Elumeeva TG, Liu W, Jackson BG, Onipchenko VG, Soudzilovskaia NA, Tao J, Cornelissen JHC (2013) Linking litter decomposition of above- and below-ground organs to plant-soil feedbacks worldwide. J Ecol 101:943–952
Fujii S, Takeda H (2010) Dominant effects of litter substrate quality on the difference between leaf and root decomposition process above- and belowground. Soil Biol Biochem 42:2224–2230
Fujii S, Takeda H (2012) Succession of collembolan communities during decomposition of leaf and root litter: effects of litter type and position. Soil Biol Biochem 54:77–85
Fujii S, Makita N, Mori AS, Takeda H (2016) A stronger coordination of litter decomposability between leaves and fine roots for woody species in a warmer region. Trees 30:395–404
Gill RMA (1992) A review of damage by mammals in north temperate forests: 1. Deer. Forestry 65:145–169
Grime JP, Cornelissen JHC, Thompson K, Hodgson JG (1996) Evidence of a causal connection between anti-herbivore defence and the decomposition rate of leaves. Oikos 77:489–494
Gulis V, Suberkropp K (2003) Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshw Biol 48:123–134
Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522
Hobbie SE, Reich PB, Oleksyn J, Ogdahl M, Zytkowiak R, Hale C, Karolewski P (2006) Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–2297
Hobbie SE, Oleksyn J, Eissenstat DM, Reich PB (2010) Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia 162:505–513
Hokkaido Forest Administration Bureau, Forestry Agency (2013) Action of the forest conservation activity that cooperated with the present conditions and an area of the Ezo deer bark feeding damage in Shiretoko. http://www.rinya.maff.go.jp/hokkaido/policy/business/pr/siritoko_wh/pdf/h25houkokusyo.pdf (in Japanese)
Ichikawa T, Fukazawa F, Takahashi T, Asano Y (2002) Effects of the conversion of the forest management type from natural deciduous broad-leaved forests to artificial Japanese cypress and Japanese cedar forests on soil fertility. Bull Jpn Soc For Environ 44:23–29
Kemp PR, Reynolds JF, Virginia RA, Whitford WG (2003) Decomposition of leaf and root litter of Chihuahuan desert shrubs: effects of 3 years of summer drought. J Arid Environ 53:21–39
King HGC, Heath GW (1967) The chemical analysis of small samples leaf material and the relationship between the disappearance and composition of leaves. Pedobiologia 7:192–197
Kumbasli M, Makineci E, Cakir M (2010) Long term effects of red deer (Cervus elaphus) grazing on soil in a breeding area. J Environ Biol 31:185–188
Kurokawa H, Peltzer DA, Wardle DA (2010) Plant traits, leaf palatability and litter decomposability for co-occurring woody species differing in invasion status and nitrogen fixation ability. Funct Ecol 24:513–523
Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498
Ma C, Xiong Y, Li L, Guo D (2016) Root and leaf decomposition become decoupled over time: Implications for below—and above-ground relationships. Funct Ecol (in press)
Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626
Mohr D, Cohnstaedt LW, Topp W (2005) Wild boar and red deer affect soil nutrients and soil biota in steep oak stands of the Eifel. Soil Biol Biochem 37:693–700
Olofsson J, Oksanen L (2002) Role of litter decomposition for the increased primary production in areas heavily grazed by reindeer: a litterbag experiment. Oikos 96:507–515
Osono T, Hagiwara Y, Masuya H (2011) Effects of temperature and litter type on fungal growth and decomposition of leaf litter. Mycoscience 52:327–332
Pastor J, Dewey B, Naiman RJ, Mcinnes PF, Cohen Y (1993) Moose browsing and soil fertility in the boreal forests of Isle Royale National Park. Ecology 74:467–480
Pérez-Harguindeguy N, Díaz S, Cornelissen JHC, Vendramini F, Cabido M, Castellanos A (2000) Chemistry and toughness predict leaf litter decomposition rates over a wide spectrum of functional types and taxa in central Argentina. Plant Soil 218:21–30
Persson I-L, Danell K, Bergström R (2000) Disturbance by large herbivores in boreal forests with special reference to moose. Ann Zool Fenn 37:251–263
Peterson CA, Enstone DE, Taylor JH (1999) Pine root structure and its potential significance for root function. Plant Soil 217:205–213
Ritchie ME, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177
Sayer EJ (2005) Using experimental manipulation to assess the roles of leaf litter in the functioning of forest ecosystems. Biol Rev 80:1–31
Shiretoko Data Center, Ministry of the Environment (2014) Meeting Document 1–4 Results of monitoring business related to the amount of deer. http://dc.shiretoko-whc.com/data/meeting/ezoshika_wg/h26/shikawg_H2601_shiryo1-4.pdf (in Japanese)
Silver WL, Miya RK (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419
Stewart AJA (2001) The impact of deer on lowland woodland invertebrates: a review of the evidence and priorities for future research. Forestry 74:259–270
Taylor BR, Parkinson D, Parsons WFJ (1989) Nitrogen and lignin content as predictors of litter decay rates: a microcosm test. Ecology 70:97–104
Tian G, Kang BT, Brussaard L (1992) Biological effects of plant residues with contrasting chemical compositions under humid tropical conditions: decomposition and nutrient release. Soil Biol Biochem 24:1051–1060
Väre H, Ohtonen R, Mikkola K (1996) The effect and extent of heavy grazing by reindeer in oligotrophic pine heaths in northeastern Fennoscandia. Ecography 19:245–253
Wardle DA, Bonner KI, Barker GM (2002) Linkages between plant litter decomposition, litter quality, and vegetation responses to herbivores. Funct Ecol 16:585–595
Yasui Y, Orihashi K, Kojima Y, Terazawa M, Kamoda S, Kasahara H, Takahashi Y (2002) Bark selection of free ranging sika deer (Cervus nippon yesoensis Heude): cafeteria tests during snow season. Trans Meet Hokkaido Branch Jpn For Soc 50:79–81
Yoshida M, Miyachi N, Kikuchi S, Yajima T (2003) Effects of selection cutting on forest dynamics in the Shiretoko National Forest: stand structure and regeneration pattern 15 years after cutting. Res Bull Hokkaido Univ For 60:79–90
Zhao Y, Peth S, Krümmelbein J, Horn R, Wang Z, Steffens M, Hoffmann C, Peng X (2007) Spatial variability of soil properties affected by grazing intensity in Inner Mongolia grassland. Ecol Model 205:241–254
This study was supported by the Mitsui & Co., Ltd. Environment Fund, the Japanese Ministry of Education, Culture, Sports, Science and Technology (Grant No. 23770083), and a Japanese Society for the Promotion of Science Fellowship for Japanese Young Scientists (Grant No. 13J00547). The Shiretoko Foundation provided logistical support for the field study. We thank the students at the Yokohama National University and members of the Shiretoko Forest Biodiversity Evaluation Project for their assistance with the field and laboratory work.
ASM and SF designed the study. All authors collected data. MK analyzed the data and drafted the manuscript with critical inputs from all authors.
Conflict of interest
The authors declare that they have no conflict of interest.
Communicated by Dr. Jarmo Holopainen.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Changes in the dissimilarity of the plant species composition between the exclosure and control sites from 2003 to 2013. β-diversity was measured as the Bray–Curtis index (DOCX 24 kb)
About this article
Cite this article
Kasahara, M., Fujii, S., Tanikawa, T. et al. Ungulates decelerate litter decomposition by altering litter quality above and below ground. Eur J Forest Res 135, 849–856 (2016). https://doi.org/10.1007/s10342-016-0978-3
- Cervus nippon yesoensis
- Ezo deer
- Leaf and root litter
- Nutrient cycling