Plant nutrient-acquisition strategies contribute to species replacement during primary succession

Abstract

1 INTRODUCTION

Understanding species replacement is crucial to unravel the mechanisms underlying plant community succession (Buma et al., 2017; Cantera et al., 2024), which has been a challenge in ecology for decades. Plant species replacement during primary succession can be related to ecological processes, such as light competition (Buma et al., 2019), accumulation of plant-specific soil pathogens (Van der Putten et al., 1993), allelopathy (Chapin et al., 1994) and discrepancies in responding to varying nutrient availability (Tilman, 1985). Nitrogen (N) and phosphorus (P) limitation commonly occur in terrestrial ecosystems (Oldroyd & Leyser, 2020). Plants have evolved an array of nutrient-acquisition strategies (NAS) responding to varying availability and forms of soil nutrients along chronosequences (Lambers et al., 2008; Zemunik et al., 2015). Although plant NAS change with soil nutrient availability and affect plant community composition (Johnson et al., 2023; Lambers et al., 2008; Li et al., 2021; Zemunik et al., 2015), their roles in affecting plant species replacement during primary succession still remain unclear.

Plant NAS can be classified into different groups according to their ability to acquire different nutrient forms, that is scavenging, mining and N₂-fixing strategies (Lambers et al., 2008). Scavenging strategies acquire plant-available nutrients from soil by adjusting fine root morphology and symbioses associated with arbuscular mycorrhizal (AM), ericoid and ectomycorrhizal (ECM) fungi. In contrast, mining strategies involve mobilizing and taking up unavailable nutrients, including sparingly soluble phosphate (e.g., calcium phosphate) by releasing carboxylates and protons and organic N and P by exuding hydrolytic enzymes. N₂-fixing strategies involve fixing atmospheric N₂ via symbiotic nodules and rhizothamnia. Actinorhizal plants are generally able to mine soil P via cluster roots and acquire N by rhizothamnia (Shane & Lambers, 2005). Ectomycorrhizal plants may simultaneously employ both strategies, as ECM fungi extend hyphae to scavenge soil nutrients while also mining nutrients through the secretion of carboxylates and enzymes by ECM fungi or associated bacteria (Landeweert et al., 2001; Yuan et al., 2024). The trade-offs among these strategies are contingent upon soil nutrient availability (Cao et al., 2024).

Previous studies on the relationship between plant NAS and species replacement were mainly conducted along chronosequences spanning thousands to hundreds of thousands of years (Holdaway et al., 2011; Zemunik et al., 2015). For example, the diversity of plant NAS is considered to play a critical role in plant community assembly as P availability declines during long-term ecosystem development along a 2 million-year chronosequence in southwest Australia (Zemunik et al., 2015). However, knowledge about plant NAS contributing to species replacement over a long time cannot necessarily be transferred to the rapid and short-time changes over decades. The difference lies in the distinct temporal patterns of soil nutrient dynamics between short- and long-term chronosequences. Soil N and P availability typically decline while recalcitrant organic nutrients accumulate with increasing soil age during long-term pedogenesis (Turner & Condron, 2013). In contrast, during the early stages of succession—from bare land to the establishment of pioneer communities—soil P availability and total N content increase significantly within decades, driven by shifts in soil P forms and atmospheric N₂ fixation (Zhou et al., 2013). These different nutrient availability gradients and distinct P compositions between short- and long-term chronosequences may result in varying contributions of plant NAS to species replacement during succession. However, the role of plant NAS in species replacement during the early stage of pedogenesis has largely been ignored.

The absence of N in soil during the early stages of soil development has been widely recognized in postglacial, coastal sand dune and volcanic chronosequences (Laliberté et al., 2012; Lawrence et al., 1967; Vitousek et al., 1993). Although young soils contain abundant total P and old ones do not, due to weathering during prolonged soil development (Walker & Syers, 1976), P is recently being considered also as a limiting factor to plant growth at this early stage (Darcy et al., 2018), since insoluble apatite-P dominates total soil P and the plant-available P concentration is very low (Zhou et al., 2018). Due to the strong ability of mining and N₂-fixing strategies to acquire sparingly available nutrients in infertile environments (Lambers, 2022; Reichert et al., 2022), it is presumed that plant species with N₂-fixing and carboxylate-releasing strategies have an advantage over those relying solely on scavenging strategies. As a result, species with mining or N₂-fixing strategies frequently dominate in communities on very ‘young’ soils across various climates and parent materials (Chapin et al., 1994; Li et al., 2021; Vitousek et al., 1993; Zemunik et al., 2015; Zhou et al., 2013). Ectomycorrhizal fungi may release more carboxylates for P mining and rely less on a scavenging strategy with far-extending hyphae at this stage. Such responses to soil nutrient availability may favour host plant species over plants that heavily rely on a scavenging strategy. In contrast, plant species with fine roots and AM fungi are less capable of acquiring sufficient plant-available nutrients.

The performance of plants with mining strategies may decline as the concentrations of plant-available soil nutrients increase during the initial to middle stages of primary succession during the early stage of pedogenesis. In nutrient-rich soils, scavenging strategies are more efficient, as they require less carbon investment compared with mining strategies (Raven et al., 2018; Wang et al., 2022). As a result, plants utilizing scavenging strategies can more efficiently acquire plant-available nutrients and gain a competitive advantage (Lambers et al., 2008). For example, mycorrhizal plant species can acquire P more economically and therefore dominate in P-rich soil compared with those exhibiting a P-mining strategy by releasing carboxylates (Zemunik et al., 2015). In addition, the acquisition of limited nutrients is associated with the allocation of plant photosynthates both aboveground and belowground (Qiu et al., 2021). Plants that allocate fewer photosynthates belowground for nutrient acquisition will be favoured in nutrient-rich soil (Tilman, 1985). Consequently, the dramatic changes in plant competitiveness related to different NAS and soil nutrient statuses may contribute to the shift in dominant species during primary succession. However, empirical evidence supporting this contention is scarce.

To address this knowledge gap, we conducted a study along a ‘young’ chronosequence (~130 years) with primary vegetation succession at the Hailuogou Glacier foreland on the eastern edge of the Tibetan Plateau, southwest China (Figure S1). During the first three stages of succession, Hippophae tibetana (Elaeagnaceae) is initially dominant compared with Populus purdomii (Salicaceae, stage 1). Then both species co-dominate at the second stage. Following that, P. purdomii gradually replaces H. tibetana and becomes the dominant species at the third stage (Li & Xiong, 1995). Soil N concentration increases from nearly undetectable levels to a relatively high level (Zhou et al., 2013). Almost all P is present in apatite or in granite at the first stage (Zhou et al., 2018). Then plant-available and organic P concentrations gradually increase with rapid weathering of the apatite and increasing soil age (Zhou et al., 2018, 2019). Hippophae species, an actinorhizal plant group, have the potential to form rhizothamnia, cluster roots and an AM symbiosis (Oremus & Otten, 1980, 1981; Shah et al., 2015). Accordingly, species within the Hippophae genus can fix N₂, mobilize insoluble P by releasing carboxylates and protons, hydrolyse organic P by exuding phosphatases, and scavenge plant-available N and P from the soil depending on AM fungal hyphae (Lambers et al., 2019). On the other hand, species within the Populus genus exhibit scavenging strategies dependent on extraradical mycelium and mining strategies by hydrolysing organic N and P in soil with a utilization of enzymes secreted by symbiotic fungi or associated bacteria (Phillips & Fahey, 2006; Yuan et al., 2024). Given the effectiveness of N-fixing and carboxylate-releasing strategies in acquiring N and P, we hypothesized that the dominance of H. tibetana at the beginning of the primary succession is attributed to its stronger ability to acquire N and P than that of P. purdomii due to its N₂-fixing and P-mining strategies. However, the absorption of nutrients by scavenging strategies including fine roots and mycorrhizas may become effective with increasing plant-available soil nutrients. Therefore, the replacement of H. tibetana by P. purdomii during the succession could be related to the latter's more efficient scavenging strategies than H. tibetana's N₂-fixing and mining strategies in a nutrient-rich stage. Specifically, we aimed to (1) investigate the differences and changes in the NAS of the two species and (2) reveal the role of plant NAS in species replacement during primary succession.