Wild boar grubbing causes organic carbon loss from both top- and sub-soil in an oak forest in central China

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Highlights

Abstract

Soil disturbances by large animals are known to affect soil carbon (C) storage and thus have the potential to change ecosystem functioning in forests. However, little is known about the effects of wild boar grubbing on soil CO2 emission in forest ecosystems. Here we investigated soil respiration and soil physico-chemical properties of top- (0–10 cm) and sub-soil (10–20 cm) on the paired grubbed and non-grubbed plots in an oak forest for a 2-year period. Wild boar grubbing substantially increased soil respiration by 69.5% in 2015 and 32.9% in 2016, respectively. Wild boar disturbance considerably elevated soil basal respiration but showed no effect on its temperature sensitivity. In addition, we found that the grubbing-induced increases in soil organic carbon and microbial biomass activity from both top- and sub-soil contributed to the stimulated soil respiration after the disturbance. Our 2-year experiment indicates that soil bioturbation could lead to a strong positive effect on soil CO2 emission in oak forest ecosystems, but the stimulation tends to reduce with recovery time. The finding also highlights the importance of soil depth and time effect while quantifying the effect of wild boar grubbing on soil C storage in forest ecosystems.

Introduction

Soils store large quantities of organic carbon (C) and the CO2 released from the soil is one of the largest fluxes in the global C cycling (Xie et al., 2014, Wan et al., 2015, Crowther et al., 2016). Both soil C storage and soil respiration have been shown to be a function of many soil characteristics such as microclimate (Davidson and Janssens, 2006, Chen et al., 2017, Liu et al., 2019a), physico-chemical properties (Ding et al., 2016, Miao et al., 2019, Wang et al., 2019), and biological factors (Karhu et al., 2014, Prescott et al., 2017, Liu et al., 2019b). Therefore, any changes in one or several of those factors can elevate or reduce organic matter decomposition and soil respiration, thus have substantial impact on the terrestrial C cycling.

Wild boar (Sus scrofa L.), native to Eurasia, is now one of the globally most widely distributed invasive ungulates (Long, 2003, Barrios-Garcia and Ballari, 2012). In China, wild boars occur across all regions except the Tibetan Plateau and Gobi Desert. Population of wild boar has increased rapidly in recent decades, reaching approximately 2 million across China (National Forestry Administration, 2009), probably due to the following reasons. First, folk hunting was completely forbidden and hunting of wildlife has been banned since 1994 in China. Second, wild boar has been added to the State Terrestrial Wildlife Protection Directory since 2000, which regulates that hunting any wildlife with beneficial or important economic or scientific values to humans is illegal. In addition, lack of predator is another important reason for the continuous increase in wild boar population.

The impacts of wild boar as an invasive species are well known around the world, not only for its destruction on crop production in agricultural ecosystems (Slg et al., 2009, Frauendorf et al., 2016), but also for its extensive influences on aboveground plant growth and regeneration (Dovrat et al., 2014, Burrascano et al., 2015, Bongi et al., 2017), as well as belowground soil physico-chemical properties (e.g. soil organic C (SOC) and total nitrogen (TN)) (Mohr et al., 2005, Bueno et al., 2013) in forest ecosystems. Wild boar gains most of its food by rooting (grubbing) activity in the soil searching for plant seeds, roots, and invertebrate and vertebrate animals (Baber and Coblentz, 1987, Wirthner et al., 2011). Compared to the sub-soil, wild boar would prefer to overturn the top-soil due to the greater probability in the occurrence of plant seeds and soil micro-animals (Wang et al., 2019). Although wild boar rooting activity was believed to have substantial impact on soil C cycling (Mitchell et al., 2007), surprisingly little research has focused on how wild boar foraging affect soil CO2 emission and subsequent soil C storage (Moody and Jones, 2000, Mohr et al., 2005).

In central China, natural forest resources are mainly distributed in the Dabie Mountains and Funiu Mountains, both of which are mainly dominated by broadleaf tree species. Broadleaf forest, especially oak forest, has been reported more suitable for wild boars compared with coniferous forest because of the high production of acorn (Fernández-Llario, 2004, Torres-Porras et al., 2015). Therefore, wild boar number has increased rapidly due to its vigorous reproduction and the suitable environmental condition in past several years in central China. Physical disturbance of introduced wild boars on soils can alter soil biogeochemical properties, and thus further affect soil C storage.

The aim of this study is to determine the influences of wild boar grubbing on soil C cycle in deciduous forest in central China, by comparing soil respiration, SOC, and microbial activity within and outside areas disturbed by wild boars. The objectives of this study were to (1) estimate the effects of grubbing disturbance of wild boars on soil respiration and its temperature sensitivity, and (2) quantify the influences of boar disturbance on SOC and microbial biomass across 2-year investigation.

Section snippets

Study site

The study site is located within the Jigong Mountains National Nature Reserve (31°46′-31 °50′N, 114 °01′-114 °06′), Henan province, central China, within a transitional zone from subtropical climate to warm temperate climate (Hu and Wan, 2019, Xia et al., 2019). The altitude ranges from 110 m to 810 m a.s.l.. Long-term mean annual precipitation (1968–2018) is 1068 mm with 60% occurring from May to September. Mean annual temperature is 15.7 °C with monthly mean temperature ranging from 2.1 °C in

Soil temperature and moisture

The seasonal dynamics of soil temperature displayed a monotonic peak in the mid-growth season in both 2015 and 2016 (T: P < 0.01, Table 1; Fig. 2a, b). On average, the soil temperature was significantly higher by 0.72 °C in 2015 and 0.69 °C in 2016 in the grubbed plots than in the non-grubbed plots (G: P < 0.05, Table 1; Fig. 2a, b). Soil moisture varied with month in both 2015 and 2016 (T: P < 0.05, Table 1). However, soil moisture showed no differences between the grubbed and non-grubbed

Grubbing effect on soil respiration

Our study exhibited that grubbing disturbance had a strong positive effects on soil respiration as we found significantly greater emission rates on the grubbed plots compared with the non-grubbed plots across our 2-year experiment. In accordance with our results, Risch et al. (2010) found an average 23.1% more CO2 was released from grubbed plots during 2-year measurement in hardwood forests in Switzerland. However, in the Monte Desert, Cuevas et al. (2012) reported a negative effect of wild

Conclusions

This study documented that disturbance of wild boars in temperate oak forest influences a suite of variables related to soil C cycling, with an overall increase in soil respiration and soil organic C. Specifically, results showed that grubbing activity by boars continuously stimulated soil respiration across our two-year experiment period. However, SOC and TN were only enhanced in the first year after disturbance of wild boars probably due to the decreased soil substrate availability during the

CRediT authorship contribution statement

Yanchun Liu: Conceptualization, Investigation, Writing - original draft, Funding acquisition. Xiaojing Liu: Methodology, Software. Zhongling Yang: Validation, Formal analysis. Guoyong Li: Visualization, Data curation. Shirong Liu: Writing - review & editing, Supervision, Funding acquisition.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was supported by the China National Science Foundation (No. 31971454, 31930078), Chinese Postdoctoral Science Foundation (2018T110722 and 01702050), and Scientific Research Fund Project of Henan University, China (yqpy20170053). We are grateful to anonymous reviewers who provided us with important suggestions for improving this manuscript. We thank Yixi Ju and Guangwei Jing of Jigong Mountain Natural Reserve Administration for their field support during the experiment.

References (54)

  • G.Y. Moinet et al.

    Estimates of rhizosphere priming effects are affected by soil disturbance

    Geoderma

    (2018)
  • A. Moody et al.

    Soil response to canopy position and feral pig disturbance beneath Quercus agrifolia on Santa Cruz Island

    California. Appl. Soil. Ecol.

    (2000)
  • C.E. Prescott et al.

    Rehabilitating forest soils after disturbance. In

    Dev. Soil Sci.

    (2019)
  • E. Vance et al.

    An extraction method for measuring soil microbial biomass C

    Soil Biol. Biochem.

    (1987)
  • X. Wang et al.

    Forest soil profile inversion and mixing change the vertical stratification of soil CO2 concentration without altering soil surface CO2 flux

    Forests

    (2019)
  • S. Wirthner et al.

    Effects of wild boar (Sus scrofa L.) rooting on the bacterial community structure in mixed-hardwood forest soils in Switzerland

    Europ. J. Soil Biol.

    (2011)
  • J. Xie et al.

    Long-term variability and environmental control of the carbon cycle in an oak-dominated temperate forest

    For. Eco. Manag.

    (2014)
  • C. Yu et al.

    Soil nutrient changes induced by the presence and intensity of plateau pika (Ochotona curzoniae) disturbances in the Qinghai-Tibet Plateau

    China. Ecol. Eng.

    (2017)
  • D.W. Baber et al.

    Diet, nutrition, and conception in feral pigs on Santa Catalina Island

    J. Wildlife Manag.

    (1987)
  • M.N. Barrios-Garcia et al.

    Impact of wild boar (Sus scrofa) in its introduced and native range: a review

    Biol. Invasions

    (2012)
  • J. Bremner et al.

    Nitrogen-total

  • C.G. Bueno et al.

    Occurrence and intensity of wild boar disturbances, effects on the physical and chemical soil properties of alpine grasslands

    Plant Soil

    (2013)
  • S. Burrascano et al.

    Wild boar rooting intensity determines shifts in understorey composition and functional traits

    Commun. Ecol.

    (2015)
  • T.W. Crowther et al.

    Quantifying global soil carbon losses in response to warming

    Nature

    (2016)
  • E.A. Davidson et al.

    Temperature sensitivity of soil carbon decomposition and feedbacks to climate change

    Nature

    (2006)
  • J. Ding et al.

    Linking temperature sensitivity of soil CO2 release to substrate, environmental, and microbial properties across alpine ecosystems

    Glob. Biogeochem. Cycle

    (2016)
  • Don, A., Hagen, C., Grüneberg, E., Vos, C., 2019. Bioturbation by wild boar increases the stability of forest soil...
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