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An integrated perspective to explain nitrogen mineralization in grazed ecosystems

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Abstract

Large herbivores are key drivers of nutrient cycling in ecosystems worldwide, and hence they have an important influence on the productivity and species composition in plant communities. Classical theories describe that large herbivores can accelerate or decelerate nitrogen (N) mineralization by altering the quality and quantity of resource input (e.g. dung, urine, plant litter) into the soil food web. However, in many situations the impact of herbivores on N mineralization cannot be explained by changes in resource quality and quantity.

In this paper, we aim to reconcile observations of herbivores on N mineralization that were previously regarded as contradictory. We conceptually integrate alternative pathways via which herbivores can alter N mineralization. We illustrate our new integrated perspective by using herbivore-induced soil compaction and subsequent changes in soil moisture and soil aeration as an example.

We show that the net effect of herbivores on mineralization depends on the balance between herbivore-induced changes in soil physical properties and changes in the quality and quantity of resource input into the soil food web. For example, soil compaction by herbivores can limit oxygen or water availability in wet and dry soils respectively, particularly those with a fine texture. This can result in a reduction in N mineralization regardless of changes in resource quality or quantity. In such systems the plant community will shift towards species that are adapted to waterlogging (anoxia) or drought, respectively. In contrast, soils with intermediate moisture levels are less sensitive to compaction. In these soils, N mineralization rates are primarily associated with changes in resource quality and quantity.

We conclude that our integrated perspective will help us to better understand when herbivores accelerate or decelerate soil nutrient cycling and improve our understanding of the functioning of 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).

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