Community-level plant functional strategies explain ecosystem carbon storage across a tropical elevational gradient

Abstract

1 INTRODUCTION

Plant species differ in their allocation of resources to growth, reproduction, and survival, resulting in trait combinations that represent adaptation strategies to various environmental conditions (Chapin III et al., 1993; Reich, 2014; Wright et al., 2004). Global variation in above-ground traits is described in the global spectrum of form and function, which differentiates two principal axes of trait variation. The first contrasts fast, resource-acquisitive strategies with slow, resource-conserving strategies (Wright et al., 2004), and the second is related to plant and seed size (Díaz et al., 2016; Reich, 2014). Additional strategy axes have also been described for below-ground traits, with the collaboration axis describing a gradient of strategies for acquiring soil resources. This ranges from plants with a do-it-yourself strategy that acquire resources via direct root uptake to species outsourcing resource acquisition by forming relationships with mycorrhizal fungi (Bergmann et al., 2020; Weigelt et al., 2021).

There is evidence that the major axes of functional strategy variation, initially described for individual species, can also manifest at the community level. This is due to habitat filtering selecting for consistent traits across multiple species of a community (Bruelheide et al., 2018). These community-level trait responses are often described using abundance-weighted mean trait values (CWMs). CWMs have been shown to vary in response to environmental gradients across scales. For instance, at a global level, CWMs of plant traits related to a conservative strategy are closely correlated with precipitation gradients, while traits associated with plant size and nutrient acquisition are strongly linked to temperature (Bouchard et al., 2024; Joswig et al., 2022; Moles et al., 2014; Xu et al., 2023). Additionally, at the regional scale, Li et al. (2017) observed strong associations between precipitation and CWM root traits related to mycorrhizal colonization, whereas at the local scale, Schellenberger Costa et al. (2017) observed a positive relationship between resource-acquisitive traits and precipitation.

As plant traits can affect the rate of biogeochemical processes (Chacón-Labella et al., 2023), both climate and variation in community-level strategies can influence ecosystem functioning (Freschet et al., 2010; Neyret et al., 2024; Reich, 2014). For instance, Manning et al. (2015) found significant effects of both mean annual temperature and CWM leaf nitrogen content on soil carbon, and Huxley et al. (2023) found significant direct and indirect trait-mediated effects of climate on above-ground net primary productivity. Yet, most of these studies focus only on a few individual traits, often leaf traits, rather than whole-plant strategy variation, and most of these studies do not incorporate root traits (Carmona et al., 2021; Cebrián-Piqueras et al., 2021; Freschet et al., 2010). This is likely due to technical difficulties in root trait measurement and a corresponding lack of data, especially in understudied regions (De Deyn et al., 2008; Iversen et al., 2017; Laliberté, 2017). As a result, there are still major gaps in understanding the relative importance of direct and indirect, trait-mediated climate effects in driving ecosystem functioning, especially the relative roles of both above- and below-ground plant functional traits.

Here, we focus on one aspect of ecosystem functioning, carbon storage, which plays a crucial role in climate change mitigation (Houghton, 2007; Lewis et al., 2004). Growing evidence indicates that community-level (CWM) trait variation influences carbon storage (Conti & Díaz, 2013; Freschet et al., 2012; Vargas-Larreta et al., 2021). Specifically, the amount of wood and its carbon content are primary drivers of both above- and below-ground carbon storage (Conti & Díaz, 2013). Accordingly, traits linked to biomass production and increased structural investment per unit biomass are expected to directly impact carbon storage (Baker et al., 2004; Moles et al., 2009). Several studies have reported associations between above-ground CWM traits and carbon, including that between taller vegetation with higher leaf carbon concentrations and higher carbon stocks (Shen, Gilbert, et al., 2019; Yang et al., 2019). Additionally, root traits can also influence both above-ground and soil carbon storage through their contribution to the slow-fast or collaboration strategy axes. Root traits related to the conservation and outsourcing axes (like high dry matter content and lifespan) have been associated with high carbon storage, while those related to do-it-yourself and fast strategy axis (like specific root length and root nitrogen concentration) have been associated with high-resource turnover and low carbon storage (Lachaise et al., 2022; Wen et al., 2022). However, while only a few studies have assessed root trait-carbon storage relationships, even fewer have incorporated both above-ground and below-ground traits (but see Chanteloup & Bonis, 2013; Craine et al., 2002; Orwin et al., 2010).

While many trait–carbon relationships have been described, these are not universally consistent (Feng & Dietze, 2013). This may be due to scaling issues, but also because the drivers of carbon storage vary across ecosystem types, with land management and with climatic contexts (Peters et al., 2019; Van der Plas et al., 2020). In addition to well-known trait responses to climatic conditions, land use can also drive variation in plant functional strategies (Allan et al., 2015). Intensive land use, including agricultural and grazing activities, often causes a shift towards species with rapid growth and high reproductive output at the expense of species with conservative traits and longer lifespans (Flynn et al., 2011; Laliberte et al., 2010; Schellenberger Costa et al., 2017). This shift can reduce carbon storage as these fast-growing species typically have lower wood density and shorter root lifespans, leading to faster carbon pool turnover (Garnier et al., 2004). Moreover, changes in land use can disrupt relationships between plants and soil symbionts (De Deyn et al., 2008), and can alter nutrient availability, soil chemistry, and microbial activity. These soil characteristics may also play an important role in carbon cycling, both directly and by influencing plant community functional trait composition (Joswig et al., 2022) and mediating the effects of climate and land use (de Castilho et al., 2006; Hartley et al., 2021; Manning et al., 2015).

Trait-carbon relationships may also differ between biomes (De Deyn et al., 2008). For instance, while above-ground traits may explain carbon storage in above-ground stocks in forests, below-ground traits might better explain carbon stocks in systems where below-ground biomass and resource allocation are high, such as grasslands (Ottaviani et al., 2020). This may mean that relationships described in temperate systems cannot be transferred to other biomes, such as tropical ecosystems, which play a major role in carbon storage worldwide. Yet evidence for trait-functioning relationships from these systems is scarce (Finegan et al., 2015). Therefore, there is a need for greater understanding of how plant functional strategies interact with land-use intensity and climatic conditions to influence carbon storage in tropical ecosystems.

Here, we assessed variation in trait composition at the community level and its relationship with above- and below-ground organic carbon storage along the large tropical elevational gradient of Mount Kilimanjaro, which ranges from savanna through forest to alpine ecosystems. This gradient also encompasses variations in land use, as ecosystems at low to mid-elevation have experienced habitat disturbances and land-use transformation (Misana, 2012). We hypothesised that coordination of below-ground and above-ground plant traits exists at the community level along the climatic gradients of Kilimanjaro, with communities with acquisitive strategies found in ecosystems with high precipitation, high land-use intensity, and moderate temperature, and communities with conservative strategies found in ecosystems with low precipitation and more extreme temperatures (Hypothesis 1).

Furthermore, we investigated whether the interplay between climate variables and plant functional strategies was related to patterns of ecosystem carbon storage using structural equation models (Figure 1, where the model structure is also justified). Here we hypothesised that climate influences carbon storage mostly via indirect pathways, mediated by land use and trait effects, with the highest carbon storage being in communities of tall, conservative plants (Hypothesis 2). The hypotheses were tested using vegetation and soil data from 60 plots located along the elevational gradients of Mount Kilimanjaro.

FIGURE 1

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Conceptual model illustrating the plant functional strategies-carbon relationship. Arrows marked I represent direct influences of local climate on carbon storage, arrows marked II represent direct effects of climate on land-use intensity, as on Kilimanjaro, intensive land uses are located at low- to mid-elevation (i.e. warmer plots; Alemayehu et al., 2023). Arrow III represents indirect effects of climate on plant functional strategies via land use (Stampfli et al., 2018), arrow IV shows the direct of influence of climate on plant strategies (Shen et al., 2016), arrow V represents the direct effect of land use on carbon storage (Ensslin et al., 2015), and arrow VI represents the influence of functional strategies on carbon storage (Chave et al., 2009). Additional models employed a modified version of the structure shown here to investigate the potential role of soil covariates in mediating these relationships (see Supporting Information: Note 3).