Andean grassland stability across spatial scales increases with camelid grazing intensity despite biotic homogenization

Abstract

1 INTRODUCTION

Grazing by herbivores is a key factor shaping the biodiversity, functioning and stability of grassland ecosystems worldwide (Eskelinen et al., 2022; Olff & Ritchie, 1998; Wang et al., 2019). Earlier research has demonstrated that while grazing may lead to either increases (Eskelinen et al., 2022) or decreases (Sandoval-Calderon et al., 2024) in local plant diversity, contingent upon the nature and extent of grazing pressure, it usually leads to a reduction in plant biomass (Milchunas et al., 1988). Additionally, these changes can arise via indirect effects of herbivores on the amount and distribution of soil nutrients via litter, dung and urine, as well as influencing soil compaction, erosion, organic matter redistribution, pH and hydrological processes (Eldridge & Delgado-Baquerizo, 2017; Eskelinen et al., 2022). Consequently, both plant diversity and biomass undergo dynamic changes with increasing grazing intensities, potentially influencing the temporal stability of these ecosystems (Ganjurjav et al., 2016; Hautier et al., 2015; Liang et al., 2021; Qin et al., 2016).

The temporal stability of productivity, measured as the temporal mean of productivity divided by its standard deviation, has been the centre of ecological research in the last decades (Hautier et al., 2014; Hautier & van der Plas, 2022; Hector et al., 2010; Tilman et al., 2006). It indicates an ecosystem's capacity to sustain consistent biomass production across different years despite environmental fluctuations (Wilcox et al., 2017). Recently, a mounting body of studies has explored the influence of grazing on the stability of grassland communities (Chen et al., 2022; Liang et al., 2021; Qin et al., 2019; Song et al., 2020). Results from these studies are mixed, with evidence of positive (e.g. Hallett et al., 2017), neutral (e.g. Bluthgen et al., 2016) or negative (e.g. Qin et al., 2019) impacts. A recent study proposes that these seemingly contradictory results can be explained by the impact of grazing on plant diversity (Liang et al., 2021). That is, in line with numerous studies demonstrating that biodiversity enhances temporal stability (Hautier et al., 2015, 2020; Isbell et al., 2015; Tilman et al., 2006), grazing should decrease stability when it decreases plant diversity and vice versa.

However, these studies have traditionally been based on experimental manipulation of herbivores, focusing on plant responses at the local scale. While these experiments allow establishing the causal effects of herbivores on plant diversity and functional stability, the transferability of these results to the management of real-world ecosystems has been recently questioned (Manning et al., 2019). There is therefore an urgent need to understand whether the responses of natural grasslands to herbivores at local scales are transferable to larger spatial scales most relevant for ecosystem management (Gonzalez et al., 2020; Isbell et al., 2017). The difficulty lies in the fact that grazing effects on diversity and stability are potentially scale-dependent and that results from small, local scales may not be directly transferable to larger spatial scales. For instance, via selective foraging, trampling and defecation, large herbivores have the potential to diminish spatial heterogeneity in soil nutrients and plant species composition at the local spatial scale, while increasing it at larger spatial scales (Adler et al., 2001; Schrama et al., 2013). Additionally, in productive ecosystems, low to moderate grazing can increase local plant diversity by reducing competition for light and allowing species coexistence (Borer et al., 2014; Eskelinen et al., 2022; Hautier et al., 2009). In contrast, in both productive and unproductive ecosystems, intensive grazing can increase soil mineralization through trampling (Li et al., 2021; McNaughton et al., 1997), which can reduce grassland diversity at both the local and large spatial scale (Liang et al., 2021). However, direct pressures from herbivores, such as physical disturbance and selective foraging, are expected to override indirect effects associated with changes in soil nutrients.

In addition to grazing, both diversity and stability can respond to abiotic factors along natural gradients. For example, aridity has been linked to reductions in local plant species richness and ecosystem stability (Hautier et al., 2015; Huang et al., 2023; Song et al., 2023). Moreover, nitrogen addition is known to reduce the temporal stability of primary productivity (Hautier et al., 2014; Zhang et al., 2019; Zhou et al., 2020). This effect potentially arises because nitrogen reduces plant diversity via increased competition for light (DeMalach et al., 2017; Eskelinen et al., 2022; Hautier et al., 2009), thereby diminishing the positive impact of plant diversity on stability at multiple spatial scales (Hautier et al., 2020). Nitrogen addition can also cause soil acidification (Bobbink et al., 2010; Galloway et al., 2008), which in turn may lower species richness and diversity (Crawley et al., 2005; Silvertown et al., 2006). Additionally, soil acidification can lower temporal stability via its negative impact on plant diversity (Verma & Sagar, 2021).

The development of a theoretical framework employing a hierarchical approach represents a significant step towards understanding ecosystem stability across spatial scales (Wang & Loreau, 2014, 2016). This framework allows testing whether the influence of grazing on plant diversity and stability is scale dependent. Higher stability at the larger spatial scale (gamma stability) can result from two main processes. First, higher local scale stability of community productivity (alpha stability) can increase stability among neighbouring local communities due to lower variation in the productivity of individual communities from year to year. Second, more asynchronous temporal dynamics of productivity across local communities (spatial asynchrony) can increase gamma stability because declines in the productivity of some communities through time are compensated for by increases in other communities. These two processes can act simultaneously. Higher alpha stability can result from greater local, plot-level species diversity (alpha diversity), while higher spatial asynchrony can result from greater compositional differences among local communities (beta diversity).

To the best of our knowledge, only a few studies have explored the scale dependence of grazing on stability and whether this effect is mediated by changes in plant diversity. These studies generally showed that increasing grazing intensity reduces both alpha and beta diversity and their positive contributions to alpha stability, spatial asynchrony and gamma stability (Liang et al., 2021; Zhu et al., 2024; Zuo et al., 2023). Grazing can affect alpha stability by influencing local plant diversity and the functional redundancy of species within a community. As grazing reduces alpha diversity, it can also reduce the capacity of communities to buffer environmental variability, thereby decreasing alpha stability. Additionally, grazing can influence spatial asynchrony by altering the extent to which different communities respond independently to environmental fluctuations. A reduction in beta diversity due to grazing-induced biotic homogenization may decrease spatial asynchrony, which is critical for stabilizing ecosystem functions at larger spatial scales (gamma stability). This cascade of effects implies that grazing has the potential to modulate biodiversity–stability relationships across spatial scales through complex and interdependent mechanisms. Additionally, relatively few studies have delved into the relationship between beta diversity and spatial asynchrony in grasslands (Liang et al., 2021, 2022; Wang et al., 2021; Wilcox et al., 2017; Zuo et al., 2023). These studies usually found that beta diversity provides higher spatial insurance effects, thereby enhancing stability at larger spatial scales (but see Wilcox et al., 2017). However, these studies focused on temperate high-productive grasslands. To the best of our knowledge, no study has investigated the influence of grazing on stability in tropical mountainous grasslands. Since these grasslands are normally lower in productivity and have a long history of grazing, the biodiversity–stability dynamics under grazing pressure can differ from previous studies. Tropical grasslands in South America are vital for sustaining the livelihoods of indigenous communities, particularly in the central Andes where camelid herding has been a primary socio-economic activity for centuries (Duchicela et al., 2019; Postigo et al., 2008).

Here, we investigate the relationship between community stability and biodiversity, exploring the scale-dependent impact of grazing on stability across a natural gradient of biodiversity, grazing intensity and abiotic factors within the tropical grasslands of the National Park Apolobamba in northwestern Bolivia. Previous analyses of diversity responses utilizing the same dataset (Sandoval-Calderon et al., 2024) indicate a neutral relationship between grazing and alpha diversity, a marginally negative relationship between grazing and beta diversity, and a positive relationship between pH and alpha diversity. Consequently, we hypothesize that increased grazing intensity in this ecosystem modulates stability across spatial scales through biotic homogenization and spatial asynchrony among ecological communities but not through the loss of local plant diversity. Additionally, we hypothesized that soil acidification reduces local stability by reducing local plant diversity.