Perspectives in Plant Ecology, Evolution and Systematics
ForumAn integrated perspective to explain nitrogen mineralization in grazed ecosystems
Introduction
Large vertebrate herbivores are key determinants of plant community composition, productivity and the functioning of many ecosystems worldwide (Olff and Ritchie, 1998, Knapp et al., 1999, Bardgett and Wardle, 2003, Cromsigt and Kuijper, 2011). One of the major pathways through which large herbivores affect the plant community is via their influence on nutrient cycling and soil nutrient availability (Fig. 1, McNaughton, 1984, Georgiadis et al., 1989, Hobbs, 1996, Frank et al., 2000, Bardgett and Wardle, 2003). Herbivores can either speed up or slow down rates of nitrogen (N) mineralization (Hobbs, 1996, Bardgett and Wardle, 2003). Classical theories that explain the impact of large herbivores on N cycling primarily focus on herbivore-induced changes in the quality and quantity of resources that are returned to the soil food web, i.e. dung, urine and plant litter (Fig. 1; McNaughton, 1984, McNaughton et al., 1997b, Bardgett and Wardle, 2003, Pastor et al., 2006). Herbivores speed up N mineralization through the deposition of dung and urine and by promotion of fast growing species and high quality (palatable) regrowth (with a low C/N-ratio), hence enhancing litter quality. In contrast, they slow down N mineralization rates when promoting low-quality plant species (with a high C/N ratio), hence decreasing litter quality (Hobbs, 1996, Ritchie et al., 1998). The acceleration of N mineralization rates through nutrient deposition and stimulation of plant growth is the basis of the grazing optimization hypothesis (McNaughton, 1979) which may apply under a restricted set of conditions (De Mazancourt et al., 1998).
Although changes in the quality of resource input into the soil food web can explain the impact of large herbivores on N cycling in a number of ecosystems (McNaughton, 1984, Pastor et al., 1993, Ritchie et al., 1998, Wardle et al., 2002, Harrison and Bardgett, 2004, Persson et al., 2005), they cannot explain contrasting effects of large herbivores on N mineralization in many other situations (e.g. Biondini et al., 1998, van Wijnen et al., 1999, Kiehl et al., 2001, Bakker et al., 2004, Su et al., 2004, Pei et al., 2008, Wang et al., 2010, Shan et al., 2011, Gass and Binkley, 2011). For example, in some systems plant quality increased under grazing, but mineralization rates were reduced (Chaneton and Lavado, 1996, van Wijnen et al., 1999, Kiehl et al., 2001). Even in a large-scale comparison across different sites herbivore effects on soil N cycling could not be understood from changes in plant quality (Bakker et al., 2006, Bakker et al., 2009). Therefore, there is a need to explore additional mechanisms that can explain herbivore-induced changes in N cycling (Gass and Binkley, 2011).
In the current theories on large herbivores and N mineralization (McNaughton et al., 1997a, Bardgett and Wardle, 2003), impacts that run via soil physical conditions received little attention (Gass and Binkley, 2011). However, large herbivores can be major drivers of changes in soil physical conditions, for example, of soil moisture and oxygen contents and soil temperature (Fig. 2). This can in turn have important consequences for N mineralization rates (Hamza and Anderson, 2005). Therefore, in this paper we explore whether integrating herbivore-induced changes in soil physical conditions into current theories on N cycling in grazed systems will help us to understand when herbivores speed up or slow down N mineralization. We aim to reconcile contrasting observations into a novel perspective, to be able to understand the impact of herbivores on N mineralization across a wide range of ecosystems.
We start by proposing the key drivers of soil N mineralization, i.e. resource quality and quantity and soil physical conditions, that should be integrated into theories on N mineralization in grazed ecosystems. Then we use trampling-induced soil compaction as an example to illustrate in detail how herbivores can alter N mineralization via changing soil physical conditions and how an integrated perspective can help us to understand the impact of herbivores on N mineralization across a range of ecosystems. Finally, we will discuss the implications of the integrated perspective for plant communities and we indicate directions for future research.
Section snippets
Herbivore effects on N mineralization
The net soil N mineralization rate is defined as the rate at which mineral forms of N (ammonium and nitrate) become available for uptake by plants through a complex of biological decomposition and transformation processes (Swift et al., 1979, Chapin et al., 2002). Mineral N is mainly released in the form of ammonium through decomposition of plant litter by soil organisms. Ammonium can be transformed into nitrate. Mineral N is used by soil microbes and plants, and it can be lost from a system
Integrated perspective
Large herbivores can strongly modify both key drivers of N mineralization, i.e. resource quality and quantity (Bardgett and Wardle, 2003, Pastor et al., 2006), as well as soil physical conditions (Asner et al., 2004, Bilotta et al., 2007, Gass and Binkley, 2011). Therefore, we propose that integrating the modification of soil physical properties by herbivores with the longer acknowledged effects on the quality and quantity of resource input will advance our understanding of N mineralization in
Application of our integrated perspective: does it increase our understanding?
We use herbivore-induced soil compaction and subsequent changes in soil moisture content as an example to examine whether our integrative perspective improves our understanding of herbivore effects on N cycling.
We hypothesize that the importance of compaction-induced changes in soil physical conditions varies across ecosystems. We expect that the magnitude of compaction effects varies along a gradient of soil moisture and soil texture (Fig. 2). In compactable, wet or dry soils the impact of
N mineralization and plant communities
Generally, rates of N cycling are strongly linked to the quality of the plants and plant litter (Wardle et al., 2004). As described in the classical theories on N cycling in grazed ecosystems, large herbivores can strengthen this positive feedback. This leads to enhanced N mineralization when herbivores increase plant quality (McNaughton et al., 1997a), and to a reduction in N mineralization when they decrease plant quality (Pastor et al., 1993, Ritchie, 1998, Kooijman and Smit, 2001, Wardle et
Other factors influencing N mineralization
We showed that in systems where quality and N cycling are decoupled, grazing-induced changes in soil moisture and soil texture can explain the impact of grazing on N cycling relatively well. Nonetheless, herbivores can also influence N mineralization via other abiotic pathways, for example by changing soil temperature, soil pH, P content, lateral water transport and soil organic matter content (Hassink et al., 1993, Mwendera and Saleem, 1997, Curtin et al., 1998, Cornelissen et al., 2007,
The way forward
We showed that using our integrated perspective may advance the understanding of the effect of herbivores on N mineralization. However, there is little experimental evidence to support our novel perspective on herbivores and N mineralization (but see Schrama et al., 2012). There is a need for field experiments that explicitly test the relation between net N mineralization and soil compaction, soil texture and soil moisture and potentially other abiotic variables. In this context, water-filled
Conclusion
In this paper we reconciled the effects of herbivores on N mineralization, by explicitly integrating herbivore-induced changes in plant quality with the impact of herbivores on soil physical properties. We used herbivore effects on soil moisture as an example to evaluate whether soil physical conditions can increase our understanding of N mineralization in grazed ecosystems worldwide. In very wet and dry systems, particularly with a fine soil texture, effects of herbivores on N mineralization
Acknowledgements
We thank Theo Elzenga, Wim van der Putten, Matty Berg for helpful comments on previous versions of this review. We are also grateful to the four anonymous reviewers and the handling editor for their comments and suggestions, which greatly improved the quality of this article. We thank Harm van Wijnen for sharing his data. This is Publication 5389 of the Netherlands Institute of Ecology (NIOO-KNAW).
References (118)
- et al.
Reversal of desertification: the role of physical and chemical soil properties
J. Arid Environ.
(2010) - et al.
The impacts of grazing animals on the quality of soils, vegetation, and surface waters in intensively managed grasslands
Advances in Agronomy
(2007) - et al.
Effects of soil compaction on the relationships between nematodes, grass production, and soil physical properties
Appl. Soil Ecol.
(2000) - et al.
Nitrogen mineralization and microbial biomass as affected by soil compaction
Soil Biol. Biochem.
(1996) - et al.
Revisiting the browsing lawn concept: evolutionary interactions or pruning herbivores?
Perspect. Plant Ecol. Evol. Syst.
(2011) - et al.
Effects of acidity on mineralization: pH-dependence of organic matter mineralization in weakly acidic soils
Soil Biol. Biochem.
(1998) - et al.
Soil compaction in cropping systems – a review of the nature, causes and possible solutions
Soil Till. Res.
(2005) - et al.
Browsing by red deer negatively impacts on soil nitrogen availability in regenerating native forest
Soil Biol. Biochem.
(2004) - et al.
Relationships between habitable pore space, soil biota and mineralization rates in grassland soils
Soil Biol. Biochem.
(1993) - et al.
Changes in soil properties and vegetation following livestock grazing exclusion in degraded arid environments of South Tunisia
Flora
(2010)
Grazing as a measure to reduce nutrient availability and plant productivity in acid dune grasslands and pine forests in The Netherlands
Ecol. Eng.
Bacterial cycling of minerals that affect plant growth in waterlogged soils – a review
Aquat. Bot.
Soil properties behavior on grazed and ungrazed plots of a grassland sodic soil
Soil Technol.
Effects of soil compaction and tillage systems on uptake and losses of nutrients
Soil Till. Res.
Animal treading stimulates denitrification in soil under pasture
Soil Biol. Biochem.
Hydrologic response to cattle grazing in the Ethiopian highlands
Agric. Ecosyst. Environ.
Effects of herbivores on grassland plant diversity
Trends Ecol. Evol.
Cattle grazing drives nitrogen and carbon cycling in a temperate salt marsh
Soil Biol. Biochem.
Abandonment in grazing systems: consequences for vegetation and soil
Agric. Ecosyst. Environ.
Changes in soil properties and vegetation following exclosure and grazing in degraded Alxa desert steppe of Inner Mongolia, China
Agric. Ecosyst. Environ.
The North American long-term soil productivity experiment: findings from the first decade of research
Forest Ecol. Manage.
Legume N mineralization: effect of aeration and size distribution of water-filled pores
Soil Biol. Biochem.
Consequence of grazing pattern and vegetation structure on the spatial variations of net N mineralisation in a wet grassland
Appl. Soil Ecol.
Seasonally dependent impacts of grazing on soil nitrogen mineralization and linkages to ecosystem functioning in Inner Mongolia grassland
Soil Biol. Biochem.
Temperature and soil moisture dependence of N mineralization in intact soil cores
Soil Biol. Biochem.
Do ungulates accelerate or decelerate nitrogen cycling?
Forest Ecol. Manage.
Functional traits of graminoids in semi-arid steppes: a test of grazing histories
J. Appl. Ecol.
Rainfall and soils modify plant community response to grazing in Serengeti National Park
Ecology
Grazing systems, ecosystem responses, and global change
Annu. Rev. Environ. Resour.
Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance
J. Wildl. Manage.
Feedbacks between soil nutrients and large herbivores in a managed savanna ecosystem
Ecol. Appl.
Interactive effects of ungulate herbivores, soil fertility, and variable rainfall on ecosystem processes in a semi-arid savanna
Ecosystems
Herbivore effects on above- and belowground plant production and soil nitrogen availability in the Trans-Himalayan shrub-steppes
Oecologia
Cross-site comparison of herbivore impact on nitrogen availability in grasslands: the role of plant nitrogen concentration
Oikos
Impact of herbivores on nitrogen cycling: contrasting effects of small and large species
Oecologia
Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size
Ecol. Lett.
Nature Management by Grazing and Cutting
Herbivore-mediated linkages between aboveground and belowground communities
Ecology
Aboveground–Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change
Changes in plant functional groups, litter quality, and soil carbon and nitrogen mineralization with sheep grazing in an Inner Mongolian grassland
Rangeland Ecol. Manag.
Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil
Oikos
Grazing intensity and ecosystem processes in a northern mixed-grass prairie, USA
Ecol. Appl.
Vegetation loss alters soil nitrogen dynamics in an Arctic salt marsh
J. Ecol.
Soil nutrients and salinity after long-term grazing exclusion in a Flooding Pampa grassland
J. Range Manage.
Principles of Terrestrial Ecosystem Ecology
Do grazers alter nitrogen dynamics on grazing lawns in a South African savannah?
Afr. J. Ecol.
Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots
Plant Cell Environ.
An experimental comparison of leaf decomposition rates in a wide range of temperate plant species and types
J. Ecol.
Global negative vegetation feedback to climate warming responses of leaf litter decomposition rates in cold biomes
Ecol. Lett.
Plant species traits are the predominant control on litter decomposition rates within biomes worldwide
Ecol. Lett.
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These authors contributed equally to the work.