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.