Plateau pika offsets the positive effects of warming on soil organic carbon in an alpine swamp meadow on the Tibetan Plateau

Highlights

• Warming and plateau pika have interactive effects on SOC in an alpine swamp meadow.

• Without pika, warming increases SOC by 22% because inputs outweigh decomposition.

• With pika, warming does not alter SOC because decomposition counteracts inputs.

• Microbial community structure is sensitive to pika disturbance but not warming.

• Pika offsets the positive effect of warming on soil carbon in the swamp meadow.

Abstract

Both climate warming and plateau pika (Ochotona curzoniae) exert considerable impacts on carbon cycling in alpine ecosystems on the Tibetan Plateau. However, the interaction of warming and pika disturbance on soil organic carbon (SOC) dynamics in alpine ecosystems remains largely unknown. Here, we measured plant, soil and microbial properties after four-year warming in a swamp meadow (with or without pika disturbance) on the Tibetan Plateau. Our results showed that in non-pika plots, warming not only increased plant belowground biomass (48%), but also enhanced microbial biomass, hydrolytic enzyme activities, and bacterial functional genes (41–46%). More plant inputs likely outweighed faster microbial decomposition, leading to the accumulation of fast-cycling particulate organic carbon (POC, 49%) and bulk SOC (22%), but not slow-cycling mineral-associated organic carbon (MAOC). In pika-disturbed plots, however, warming did not significantly change plant belowground biomass (which dominates total plant biomass), microbial biomass and hydrolytic enzyme activities. Although bacterial functional genes were suppressed (−40%) and plant aboveground biomass was increased (118%), oxidative enzymes were significantly stimulated (17%), which likely counteracted the higher aboveground plant inputs and led to minor changes in soil carbon pools (SOC, POC and MAOC) with warming. Moreover, bacterial and fungal community structure were significantly altered by pika disturbance, but not warming. Overall, these findings demonstrated that pika disturbance could offset the short-term positive effect of warming on soil organic carbon in the alpine swamp meadow ecosystem.

Introduction

Known as the Earth’s third pole, the Tibetan Plateau is the highest and most extensive highland in the world (Yang et al., 2008, Kang et al., 2010). Due to large soil organic carbon (SOC) storage and rich biodiversity, it plays an important role in regulating the balance of global carbon cycling (Yang et al., 2008, Piao et al., 2019). Yet, over the past several decades, rapid climate change and extensive human activities have considerably influenced ecosystem processes and functions on the Tibetan Plateau (He et al., 2021). For instance, climate warming enhanced plant production and soil respiration (Chen et al., 2020), and increased old C emission from permafrost deposits (Chang et al., 2021). Besides, plateau pika, as a widespread small mammal, caused extensive disturbance on alpine ecosystems, such as increasing plant species diversity (Pang et al., 2020) and affecting soil nutrient availability (Wei et al., 2019). However, most studies mainly focused on the impacts of climate change or biotic disturbance in isolation, while climate warming and pika disturbance actually co-occur in some regions of the Tibetan Plateau. Until now, it remains unclear how the interaction of warming and pika disturbance affects SOC storage and dynamics on the Tibetan Plateau and what are the regulatory mechanisms.

The mean annual air temperature on the Tibetan Plateau has increased ~0.40 °C per decade from 1971 to 2019, which is much higher than that of the global average (He et al., 2021). Climate warming exerted multiple effects on above- and belowground communities and soil C dynamics of the Plateau (Chen et al., 2020). Increasing temperature could directly increase plant metabolic rates and productivity (Walther, 2003), especially in colder ecosystems (Rustad et al., 2001). Belowground microbial activities also could be profoundly altered by warming, further influencing soil C decomposition or transformation (Chen et al., 2015). For example, warming stimulated soil C cycling through increased soil respiration on the Tibetan Plateau (Chen et al., 2020), or reduced soil C loss due to warming-induced soil moisture limitation (Kirschbaum, 2000). However, it remains uncertain whether the soil C of alpine ecosystems increases or decreases in the past decades on the Tibetan Plateau (Chen et al., 2017, Ding et al., 2017). In any case, changes in the SOC represent the balance of gains and losses (Lal, 2004), closely relating to the responses of plants and microorganisms under warming or external disturbance.

The plateau pika (Ochotona curzoniae) is a common small mammal that inhabits on the Tibetan Plateau, China (Guo et al., 2012). Given its burrowing and gnawing activities to plants, soils and competition with livestock for food, the plateau pika is often considered as a pest in alpine ecosystems (Smith and Foggin, 1999, Wei et al., 2020). In fact, divergent changes in plant biomass have been detected in pika-disturbed regions. Some studies showed negative effects of pika on plant biomass, due to consuming/gnawing (Liu et al., 2013, Zhao et al., 2019). Neutral and even positive effects of pika on plant biomass were also detected in alpine ecosystems, because the increased plant production with higher nutrient availability compensated for the biomass consumption by pika (Zhang et al., 2016, Pang et al., 2020). In contrast, there have been very few studies on the effects of pika disturbance on belowground microbes and SOC dynamics. For instance, Zhao et al. (2019) reported that SOC and microbial biomass C decreased with reduced plant biomass in pika-disturbed sites. SOC content first increased and then decreased with increasing pika burrow densities in alpine meadows (Yu et al., 2017a), and microbial activity was stimulated by the improvement of soil water availability and aeration by pika (Zhang et al., 2016, Yu et al., 2017b). Yet, there have been no direct measurements of microbial communities and functional genes related to soil C and nutrient cycling together with soil C pools responding to pika disturbance.

A growing number of studies have demonstrated the importance of separating SOC pools in the process of quantifying changes in bulk SOC (Kögel-Knabner, 2002, Poeplau et al., 2018, Yuan et al., 2020). This is because SOC stock is very complex in composition, and small changes in SOC stock might be difficult to discern by traditional approaches (Bradford et al., 2016, Li et al., 2020). In this case, schemes for SOC separation can shed light on understanding and predicting SOC dynamics under global changes (Lavallee et al., 2020). For instance, the fast-cycling, less-protected particulate organic C (POC, using wet sieving method) in agricultural soils decreased with increasing temperature (Qi et al., 2016), while the slow-cycling, mineral-associated organic C (MAOC) may not be altered by short-term warming (Conant et al., 2011). Li et al. (2020) also found that warming affected SOC chemical composition (increasing alkyl C and decreasing aromatic C), despite a minimal effect on SOC stock. Therefore, an integrative analysis of warming and plateau pika influencing SOC stock as well as its distinct components on the Tibetan Plateau is strongly needed.

This study was based on the experimental warming platforms conducted in non-pika and pika-disturbed regions in an alpine swamp ecosystem located on the northeast Tibetan Plateau. We hypothesized that warming and pika disturbance would affect the fast-cycling SOC fraction (POC) but not the bulk SOC content and the slow-cycling SOC fraction (MAOC), following changes in plant inputs and microbial activities. Therefore, we measured plant biomass (aboveground and belowground), soil physical and chemical properties, microbial characteristics (including biomass, enzyme activities, community composition and functional genes), and bulk SOC (including physical fractions and chemical composition) under warming and pika treatments. Specifically, we aimed to answer two questions: 1) how plants and soil microbes respond to warming and pika disturbance? and 2) how warming and pika disturbance affect bulk SOC and its different components, and what are the plant-microbial regulatory mechanisms?