Effects of fine-scale simulation of deer browsing on soil micro-foodweb structure and N mineralization rate in a temperate forest

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Abstract

The effects of low densities of native browsing mammals on nutrient cycling are not fully understood. Weak browsing may improve nitrogen (N) mineralization in soil and positively affect plant regrowth at the forest floor. To investigate the effects of weak browsing by sika deer (Cervus nippon) on soil subsystems, we defoliated a dwarf bamboo (Sasa nipponica)-dominated understory layer in a natural forest at different intensities to realistically simulate deer browsing. Defoliation (0–18% leaf removal) was performed three times at approximately 1-week intervals in summer. We measured water-soluble carbon (C) concentration, phospholipid fatty acid (PLFA) profiles as indicators of microbial community structure, a PLFA of 20:4 as an indicator of protozoan abundance, nematode community structure at the family level, and the N mineralization rate in 28 days of incubation. The effects of defoliation on each soil parameter were determined by comparing before and after defoliation values. The N mineralization rate in the first 10 days of incubation showed a unimodal response to defoliation intensity, with a peak mineralization rate at a defoliation rate (number of removed leaves/total leaves) of 7.6%, correlating with protozoan PLFA and the abundance of Plectidae (the most dominant family of bacterivorous nematodes). In contrast, the N mineralization rate during the following 18 days of incubation decreased monotonically with increasing defoliation intensity, correlating with the water-soluble C concentration in the soil and the C content of new leaves. These results suggest that removing <15% of leaves may have induced a pulse-like release of labile organic matter from roots that lasted for less than 1 week and stimulated N mineralization through microbial loop in soil in the short term (in the first 1–2 weeks after defoliation). N mineralization, however, was reduced with increase of defoliation intensity in the longer term (3–5 weeks after defoliation), possibly because of the reduction in labile organic matter supply from roots 1 week after defoliation. As a result, N mineralization rates over the 28-day incubation period responded to defoliation intensity in a unimodal pattern with a small peak (at a defoliation rate of 4.9%) and were negatively affected by high defoliation rates (>10%). This study suggests that browsing on forest floor plants has positive or negative effects on soil N mineralization potential depending on browsing intensity level.

Introduction

Aboveground herbivory by large mammals can modify the structure and functioning [e.g., nitrogen (N) mineralization] of belowground system due to alteration of quality and quantity of organic matter input, and affect nutrient cycling in the terrestrial ecosystem (Bardgett and Wardle, 2003). In forest ecosystems, intense browsing by dense ungulate populations alters plant community structure and affects nutrient cycling in forests by changing plant litter quality (Pastor et al., 1993). However, in natural forests, it is uncertain how native browsing mammals, which are often originally present at low densities, affect nutrient cycling. Nutrient cycling may be gradually modified by increasing population densities of browsing mammals, even if the vegetation has not been greatly affected.

In grassland ecosystems, aboveground herbivory by insects or artificial defoliation is likely to alter the resource allocation patterns of plants to increase root exudates (Holland et al., 1996; Paterson and Sim, 1999), and consequently, soil microbial biomass (Mawdsley and Bardgett, 1997; Guitian and Bardgett, 2000) and abundance of microbivores (nematodes, rotifers, enchytraeids; Mikola et al., 2001, Mikola et al., 2005). Furthermore, Hamilton and Frank (2001) found that aboveground herbivory also enhances N mineralization, and thus positively affects the regrowth of defoliated plants. Although labile organic carbon (C) supply causes N immobilization by microorganisms, it is considered to stimulate N mineralization through the release of immobilized microbial N by microfaunal grazing (Clarholm, 1985; Ingham et al., 1985). However, some other studies found that defoliation had no or even negative effects on C partitioning to root exudation (Mikola and Kytöviita, 2002; Dilkes et al., 2004). These inconsistent responses of plants to defoliation may be partly attributed to the difference in plant species (Guitian and Bardgett, 2000), defoliation intensity (Holland, 1995), or elapsed time since defoliation (Macdonald et al., 2004). The responses of forest floor plant species to defoliation and the consequences for soil subsystem are undetermined.

How the responses of plants and soil subsystems vary with browsing intensity needs to be investigated to determine the effects of browser mammal population density on nutrient cycling in forest ecosystems. Several studies reported that browsing-tolerant grass exhibit monotonous increase of root-derived organic matter input to soil with increase of defoliation intensity (Bokhari and Singh, 1974; Guitian and Bardgett, 2000), while the intensification of defoliation could monotonically decrease root production and reduce organic matter input from roots in long-term defoliation experiment (Mikola et al., 2001). Some other studies suggests that maize (Zea mays) show a unimodal increase of organic matter input from roots with aboveground herbivory increase. Weak herbivory by grasshoppers was found to increase maize resource allocation to root exudates (Holland et al., 1996), soil microbial biomass (Holland, 1995), and microbial-feeding nematode abundance (Fu et al., 2001). However, more intensive herbivory did not cause an increase in microbial biomass (Holland, 1995). Increased root-derived organic matter input can be considered as an adaptive response for herbaceous species with a high tolerance to browsing and a rapid growth rate (Bardgett and Wardle, 2003) because it leads to enhanced N mineralization in the rhizosphere and potentially supports plant regrowth (Hamilton and Frank, 2001). However, stimulating N mineralization by releasing photosynthates from roots may be costly but offer little advantage to the less tolerant plants (e.g., maize) which were browsed severely, because it is difficult for them to restore photosynthetic ability by regrowth.

Sika deer (Cervus nippon Temminck) populations have been expanding in forests across Japan in the past two decades. Although alterations to forest vegetation resulting from the heavy browsing pressure of the deer have become a serious problem (Takatsuki and Gorai, 1994; Yokoyama et al., 2001; Tsujino and Yumoto, 2004), little is known about the effects of the deer on the structure and the N mineralization functioning of soil subsystems. Sasa nipponica Makino et Shibata (Poaceae: Bambusioideae), an evergreen perennial semiwoody plant, often forming dense understory vegetation in cool-temperate forests in Japan (Oshima, 1961; Agata and Kamata, 1979), is the major food of sika deer in many habitats (Takatsuki, 1983; Yokoyama et al., 1996). Because S. nipponica does not have as much tolerance to browsing as pasture plants, in forests with high deer population densities, understory stands consisting mainly of S. nipponica have declined or disappeared because of high browsing pressure (Yokoyama and Shibata, 1998; Terai and Shibata, 2002). S. nipponica may exhibit a unimodal response of labile organic matter release from roots to defoliation intensity as maize is expected to do, although whether C allocation to rhizodeposition changes when S. nipponica is browsed by deer has not been determined.

We investigated the effects on soil subsystems of sika deer browsing on S. nipponica under conditions similar to those of natural habitats with low deer densities by defoliating S. nipponica, realistically simulating the behavior and intensity of deer browsing. The following hypotheses were tested: the labile organic C supply from roots responds to defoliation intensity in a unimodal pattern (i.e., increasing at low intensity, and decreasing at high intensity); the biomass or the abundance of soil micro-foodweb constituents (bacteria, fungi, protozoa, and nematodes) is increased by moderate defoliation, reflecting the labile organic C supply from roots; the N mineralization rate is affected by changes in the soil micro-foodweb structure; and the N content of S. nipponica leaves is positively correlated with the N mineralization rate.

Section snippets

Site description

The experiment was conducted in a broad-leaved deciduous forest in the northern part of Ibaraki Prefecture, Japan (36°47′N, 140°32′E; 770 m altitude), from July to August 2005. The mean temperature and annual precipitation in 2002–2003 at the study site were 9.1 °C and 1942 mm, respectively (Nomiya et al., unpublished data). The soil was a typical Andosol, which is a highly porous soil developed from volcanic parent material, such as volcanic ash. The A layer at this site was >50 cm thick, and the

Results

The mean value of each measure of leaf and soil properties and PLFA for all plots at pre- and post-browsing is shown in Table 1, and that of each nematode measure is shown in Table 2. All the significant relationships found in the regression analysis are shown in Fig. 1.

Discussion

Changes in protozoa and plectid nematode abundance suggest that a moderate intensity of defoliation (i.e., a defoliation rate <15%) stimulated rhizodeposition of C (Paterson and Sim, 1999) and N (Ayres et al., 2007) and enhanced bacterial biomass growth (Fig. 1c, d). The lack of increase in water-soluble C and bacterial PLFAs by moderate defoliation was probably a result of the high degradability of root-derived soluble organic matter, such as root exudates, which consist mainly of sugars (

Conclusions

We revealed that simulated browsing of S. nipponica by a low-density population of sika deer in summer modifies the soil micro-foodweb structure, and consequently the N mineralization potential under field conditions similar to those of natural deer habitats with C-rich soil. And these defoliation effects changed highly depending on defoliation intensity and elapsed time since defoliation. To understand the impacts of browsing by large mammals on soil subsystem in real forests, their population

Acknowledgments

We thank Shin-Ichi Horino and Haruto Nomiya (Forestry and Forest Products Research Institute) for use of the experimental site and unpublished data and for supporting our fieldwork. We also thank Dr. Shigeki Masunaga (Yokohama National University) for use of the organic carbon analyzer, Dr. Hirosuke Oba (National Institute for Agro-Environmental Sciences) for technical guidance on PLFA analysis, and Dr. Reiji Fujimaki (Yokohama National University) for assistance in measuring inorganic

References (44)

  • S. Yokoyama et al.

    Impact of bark stripping by sika deer, Cervus nippon, on subalpine coniferous forests in central Japan

    Forest Ecology and Management

    (2001)
  • W. Agata et al.

    Ecological characteristics and dry matter production of some native grasses in Japan I. Annual growth pattern of Sasa nipponica community (in Japanese with English abstract)

    Journal of Japanese Society of Grassland Science

    (1979)
  • E. Ayres et al.

    The influence of below-ground herbivory and defoliation of a legume on nitrogen transfer to neighbouring plants

    Functional Ecology

    (2007)
  • R.D. Bardgett et al.

    Herbivore-mediated linkages between aboveground and belowground communities

    Ecology

    (2003)
  • U.G. Bokhari et al.

    Effects of temperature and clipping on growth, carbohydrates reserves, and root exudation of western wheatgrass in hydroponic culture

    Crop Science

    (1974)
  • D.D. Briske et al.

    Contribution of flexible allocation priorities to herbivory tolerance in C4 perennial grasses: an evaluation with 13C labeling

    Oecologia

    (1996)
  • N.B. Dilkes et al.

    Temporal dynamics of carbon partitioning and rhizodeposition in wheat

    Plant Physiology

    (2004)
  • Å. Frostegård et al.

    The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil

    Biology and Fertility of Soils

    (1996)
  • Å. Frostegård et al.

    Dynamics of a microbial community associated with manure hot spot as revealed by phospholipid fatty acid analyses

    Applied and Environmental Microbiology

    (1997)
  • R. Guitian et al.

    Plant and soil microbial responses to defoliation in temperate semi-natural grassland

    Plant and Soil

    (2000)
  • E.W. Hamilton et al.

    Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass

    Ecology

    (2001)
  • J.N. Holland

    Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems

    Applied Soil Ecology

    (1995)
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