Multitrophic diversity of the biotic community drives ecosystem multifunctionality in alpine grasslands
Hongye Su1,2, Zhen Wang1, Li Ma1, Ruimin Qin1,2, Tao Chang3, Zhonghua Zhang1, Junfei Yao4, Xudong Li4, Shan Li5, Xue Hu1,2, Jingjing Wei5, Fang Yuan1, Haze Adi1,2, Zhengchen Shi1,2, Honglin Li6 and Huakun Zhou1*
1 Qinghai Provincial Key Laboratory of Restoration Ecology in Cold Regions, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China;
2 College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China;
3 College of Grassland Science and Technology, China Agricultural University, Beijing, 100191, China;
4 College of Agriculture and Animal Husbandry, Qinghai University, Xining 810016, China;
5 College of Geographical Science, Qinghai Normal University, Xining, 810008, China;
6 State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China;
* Correspondence: hkzhou@nwipb.cas.cn.
ABSTRACT
1. Biodiversity and ecosystem multifunctionality are currently hot topics in ecological research. However, little is known about the role of multitrophic diversity in regulating various ecosystem functions, which limits our ability to predict the impact of biodiversity loss on human well–being and ecosystem multifunctionality.
2. In this study, multitrophic diversity was divided into three categories: plant, animal, and microbial communities (i.e., plant diversity, rodent diversity, bacterial and fungal diversity). Also, 15 ecosystem functions were divided into four categories–water conservation, soil fertility, nutrient cycling and transformation, and community production–to evaluate the significance of biotic and abiotic variables in maintaining ecosystem multifunctionality.
3. Results indicated that species diversity at multiple trophic levels had a greater positive impact on ecosystem multifunctionality than species diversity at a single trophic level. Notably, the specific nature of this relationship depended on the niche breadths of plants, indicating that plants were key indicators linking above and below ground trophic levels. Abiotic factors such as altitude and pH directly acted on ecosystem multifunctionality and could explain changes in ecosystem functions.
4. Overall, our study offers valuable insights into the critical role of multitrophic species diversity in preserving ecosystem multifunctionality within alpine grassland communities, as well as strong support for the importance of biodiversity protection.
KEYWORDS
biodiversity, multitrophic levels, community, biotic variables, ecosystem functions
1 INTRODUCTION
In the past 20 years, the relationship between biodiversity and ecosystem multifunctionality has been a central issue in applied ecology (Hooper et al., 2005; Lefcheck et al., 2015; Soliveres et al., 2016). There is clear evidence indicating that loss of biodiversity at any particular trophic level can lead to a decline in ecosystem services (e.g., production, maintenance of soil fertility, and water purification) and efficiency of resources capture (Balvanera et al., 2006; Weisser et al., 2017). Nevertheless, existing studies typically concentrated on single trophic groups, especially plant communities, overlooking the fact that biodiversity loss occurs across multiple communities (Allan et al., 2014; Antiqueira et al., 2018; Wang et al., 2019).
Indeed, ecosystems are complex and diverse, with food webs formed by the interactions of species at different trophic levels, thus harmonizing the ecosystem structure and functions (Seibold et al., 2018). Many experiments have shown that focusing solely on a single trophic level group may significantly underestimate the impact of biodiversity on ecosystem functioning. The underlying reason is that functional effects of different trophic groups may complement or counteract each other (Soliveres et al., 2016; Seibold et al., 2018; Luo et al., 2022). For example, enriching plant diversity can increase soil microbial diversity in natural ecosystems and farming systems (Garland et al., 2021), and in agricultural systems microbial diversity can also improve crop yield (Dahlstrom et al., 2020) and quality and facilitate the rate of nutrient acquisition by plants (Jing et al., 2015); the manipulation of plant species has knock-on effects on other groups, such as bacteria and mycorrhiza (Hector and Bagchi, 2007); an increase in plant species diversity promotes beneficial interactions between insects and plants at different trophic levels, leading to significant bottom-up effects that influence ecosystem functions (Wan et al., 2020). Also, the interactions within multitrophic metacommunity can mediate the asynchrony and stability of communities in fluctuating environments (Firkowski et al., 2021). Currently, research on multitrophic interactions primarily focuses on the interactions among primary producers (plants), primary consumers (insects), and decomposers in the soil (bacteria, fungi, and nematodes), as well as their responses to climate change and ecosystem functioning (Granot et al., 2019; Buzhdygan et al., 2023; Wang et al., 2023a), with limited attention given to rodents. Rodents serve as seed consumers and dispersers, and the differences in seed characteristics directly influence their dispersal strategies. Over long-term evolution, this has led to a mutualistic relationship between rodents and plants (Yu et al., 2014). Meanwhile, rodent digging changes soil nutrient distribution, enhances soil permeability and water absorption, and increases grassland soil surface heterogeneity, thereby indirectly impacting the plant growth environment (Laundre and Reynolds, 1993). Therefore, there is an urgent need to fully understand whether changes in trophic level complexity will affect ecosystem functioning.
Studies of multiple trophic levels have relied on measuring the species diversity of habitats to uncover trophic linkages, with species at different trophic levels transferring energy and nutrients through food chains, facilitating interactions and linkages between organisms (Deraison et al., 2015; Li et al., 2020). Trophic richness will mean that a diverse range of organisms will be able to occupy suitable niches within an ecosystem, thus contributing to the maintenance of biodiversity. For a long time, ecologists have been exploring how species diversity is maintained within biological communities. The classical theory of species coexistence suggests that environmental filtering leads to species with similar functional traits occupying similar ecological niches in space, resulting in aggregated distributions (Kraft et al., 2014; Hua et al., 2024). Biological filtering mainly involves niche differentiation and fitness differences among species with similar functional traits in the community due to competition, involving both interspecific competition and intraspecific functional trait variation (Aschehoug et al., 2016).
Plants act as intermediaries connecting consumers and decomposers, providing an energy foundation for the food chain through photosynthesis for primary consumers to utilize, directly or indirectly regulating soil fertility, nutrition cycling and transformation, community productivity, and so on (Cosme, 2023), maintaining a beneficial cycle within the ecosystem. The ecological niche differentiation among plant species can reduce the intensity of interspecific competition. In communities with stronger competition, species tend to exhibit a preference for different niches to reduce overlap and interspecific competition, leading to an increase in biodiversity (Zuppinger-Dingley et al., 2014). Many studies have revealed that species richness influences biomass size, with higher predator and prey diversity increasing plant species diversity (Brose, 2008; Katano et al., 2015) and primary consumers may be more inclined to select more energetically efficient plant species (Schneider et al., 2016). The above indicates that we cannot ignore the important role of plant ecological niche indicators in multitrophic level studies.
In addition to considering biotic factors, the impact of abiotic factors on ecosystem functioning should not be overlooked. Elevation influences the developmental diversity and species richness of plant systems through environmental filtering (Galván-Cisneros et al., 2023), regulating changes in various ecosystem functions (Fu et al., 2020). The diversity of microbial communities, the complexity of co-occurrence networks, and the multifunctionality of ecosystems all significantly decrease with increasing elevation (Chen et al., 2022). Soil pH, as a dominant factor in explaining multifunctionality and functional group changes, inhibits ecosystem functions and multifunctionality due to soil acidification (Wei et al., 2022), and it also significantly impacts soil biodiversity, thereby affecting ecosystem stability (Chen et al., 2021).
The interactions among biotic factors across multiple trophic levels, as well as abiotic factors, have been shown to influence ecosystem functioning. However, alpine grasslands as the most important ecosystem and natural resource on the Qinghai-Tibet Plateau, covering over 60% of the region (Zuo et al., 2022), it remains unclear how the diversity of trophic levels and abiotic factors impact the ecosystem multifunctionality of alpine grasslands. To fill these critical knowledge gaps, our study aimed to reveal how multitrophic diversity (including plant diversity, microbial diversity, and rodent diversity) and abiotic variables (including altitude and pH) and their interactions influence ecosystem multifunctionality by investigating the vegetation and soil characteristics of different grassland types in Qinghai–Tibet Plateau alpine grassland. We propose the following hypotheses: (1) the multitrophic diversity of the biotic community will enhance ecosystem multifunctionality more than any single trophic level; (2) the differentiation of plant niche breath is influenced by abiotic factors and ecosystem functioning, thereby affecting the construction of multitrophic level communities; and (3) abiotic factors, particularly altitude and pH, can directly affect ecosystem multifunctionality.