Positive and negative feedbacks drive aboveground traits in rare plant species

Abstract

Microbially mediated plant-soil feedbacks drive patterns of plant growth, competitive ability, succession, and community composition. Although rare plant species maintain unique functional traits that often facilitate negative feedbacks, there is not a consensus on the belowground drivers nor the effects of phylogenetic origin of previously plant-conditioned soil on aboveground traits associated with rare species. Using a common garden, we connect belowground fungal colonization to aboveground traits in species varying in rarity, and soil conditions varying in the phylogenetic relatedness of conditioning plant species, to demonstrate the mechanistic relationship between belowground ectomycorrhizal fungal (ECM) colonization and aboveground total plant biomass in 14 Eucalyptus species varying in their rarity status. Specifically, we found that while the rarest species displayed 88% less total biomass than common species, the rarest species also maintained 62% greater ECM colonization than common counterparts. Further, negative feedbacks resulted in reduced biomass coupled with positive feedbacks that resulted in increased ECM colonization that varied on the basis of phylogenetic relatedness. The rarest species decreased by 71% - 94% in total biomass but increased by 96% - 114% in ECM colonization in phylogenetically similar and distant soil compared to conspecific soil conditions. The effect size of ECM colonization directly affected the effect size of total biomass in phylogenetically distant conditions with a significant negative correlation (r^2 = -0.83) to show that biomass may be a function of ECM colonization acting differently among species varying in rarity. Consequently, rare plant species may utilize stronger associations with belowground mycorrhizal mutualists than common plant species, to facilitate geographic, competitive, and functional persistence, even while maintaining lower biomass.

Introduction

Plant-soil feedbacks are major drivers of plant growth, long-term survival, and patterns of biodiversity in plant communities, that are especially important in an era of global change (van der Putten et al. 2013, Van Nuland et al. 2017, Semchenko et al. 2022). Through unique alterations in the biological and chemical properties of soil due to plant traits and inputs that lead to changes to the microbial community composition and function, the conditioning effects of plant communities drive patterns of productivity, composition, and succession in future plant communities through soil legacy effects (Li et al. 2023; Lu et al. 2023; Qu et al. 2023). Although plant-soil feedbacks can range from facilitative to inhibitory, microbially mediated legacy effects can persist in the soil for long periods of time after the conditioning plant species have disappeared (Kulmatiski & Beard 2011; Schmid et al. 2021). Therefore, patterns of plant growth, reproduction, and competitive ability in current plant communities may be driven by soil-microbial changes induced by previous species no longer present or prevalent (Bever 2003, van der Putten et al. 2013). Specifically, mutualistic ectomycorrhizal (ECM) fungi play an integral role in mediating the productivity and diversity of aboveground plant communities through facilitating shifts in nutrient availability as well as soil structure and stability across early, mid-, and late successional stages (Kałucka & Jagodziński 2017; McMahen et al. 2022; Zhao et al. 2023 Wang et al. 2023). For example, Hannula et al. (2021) found that while bacterial communities quickly respond to alterations in plant community composition, microbially mediated soil legacy effects remain after five months of succession. Similarly, McMahen et al. (2022) found that plant succession is highly influenced by mycorrhizal dependence, with ECM plant hosts demonstrating higher seedling survival and biomass in early succession. Additionally, other belowground root-colonizing fungi such as dark septate endophytes (DSE) can enhance aboveground plant growth through increased nitrogen (N) and phosphorus (P) root absorption as well as increased root surface area (He et al. 2019; Xie et al. 2021). However, Reininger & Sieber (2012) suggests that a trade-off exists between DSE and ECM communities, such that increased allocation to ECM fungi can create physiological barriers preventing the colonization of beneficial DSE with extended effects on future plant community dynamics. Furthermore, plant community composition and variation in plant functional groups can also drive unique changes in soil-legacy effects not seen in species-specific monocultures (Schmid et al. 2021). While species-specific legacy effects exist in grasslands, Heinen et al. (2020) demonstrated that a marked dominance in functional group (grasses versus forbs) within a conditioning community leads to negative feedbacks on the same functional group in future plant communities. Moreover, these community-driven legacy effects often exhibit subsequent effects on plant-herbivory, plant-pollinator, and plant-plant interactions, all of which can determine changes to ecosystem function (Wurst & Ohgushi 2015; Heinen et al. 2018; Li et al. 2023).
Although legacy effects work in tandem with other ecological and evolutionary processes shaping communities, the conditioning effects of previous plant communities in soil are often recognized as major determinants of above- and belowground plant success in widespread grassland communities consisting of common species (Kulmatiski et al. 2008; van de Voorde et al. 2011; Cortois et al. 2016). For example, Kulmatiski et al. (2008) found that 83% of the 315 experiments at that time were focused on grassland systems that informed patterns in plant-soil feedback strength and direction. Patterns in grasslands, however, may not be applicable to other systems varying in growth form, habitat, or rarity such as trees, forests, or plants with rare status (Rabinowitz 1981). However, the consideration of plant-soil feedbacks is paramount to understanding rare species persistence in community mixtures due to unique and wide variation of specialized functional traits in rare species, such as specific leaf structures, root systems, growth forms and rates, and microbial mutualisms, often not seen in common species (Dee et al. 2019; Xi et al. 2021; Zhang et al. 2022). For example, rare species have been found to exhibit low biomass (Kempel et al. 2018; Vincent et al. 2020), high specific root length (SRL) (Poot & Lambers 2003), and increased phenotypic plasticity (Munson & Sher 2015; Boyd et al. 2022). Although ecological studies of rare plant species are often focused on the geography and population traits of rare species, rather than the context of growing conditions, studies have demonstrated the role of plant-soil feedbacks in driving patterns of rarity and commonness in plant communities on the landscape (Klironomos 2002; Maron et al. 2016; Kempel et al. 2018). For example, Maron et al. (2016) suggested that abundant common species may suffer from increasingly negative plant-soil feedbacks, while rare species may persist in a geographically limited space due to positive plant-soil feedbacks. Moreover, van der Putten et al. (2013) proposed that rare plant species may have the potential to become invasive outside of their native range due to favorable, positive plant-soil feedbacks in non-native ranges. Further, the relationship between unique plant functional traits and belowground mycorrhizal fungi can range from mutualistic to parasitic dependent on temporal and spatial variation in soil nutrient conditions; however, the expected relationships between plant traits and soil factors, such as N enrichment, are inconsistent and often lack predictability (Treseder 2004; Hoeksema et al. 2010). For example, Treseder (2004) found that mycorrhizal abundance decreased by 15% under N fertilization, while Johnson et al. (2010) suggested that the prominence of mycorrhizal parasitism decreased under nitrogen-limiting conditions. However, Hoeksema et al. (2010) and Wooliver et al. (2018) both demonstrated a marked reduction in mycorrhizal dependence under high N conditions. Taken together, these studies suggest that unique interactions take place between plant functional traits and variation in soil conditions, such that plants either carefully manipulate the allocation of carbon (C) to belowground symbionts or are parasitized by them under higher N conditions. Whether and how N enrichment affects plant host reliance on mycorrhizal fungi on the basis of species rarity to affect the outcome of plant-soil feedbacks in unknown, to our knowledge.
Although plant community composition is crucial to the development of unique plant-soil feedbacks, the phylogenetic relatedness underpinning plant communities provides a mechanistic driver of plant soil feedback strength and direction (Jiang et al. 2022). There is a strong phylogenetic signal to the degree in which plant species share their belowground biotic partners, such that more closely related species have more similar microbiomes (Wandrag et al. 2020). Although some plant species have demonstrated increased growth in phylogenetically similar communities due to the utilization of closely related co-evolved microbial communities (Anacker et al. 2014), others have demonstrated positive feedbacks in plant growth in communities of increasing phylogenetic distance (Kempel et al. 2018; Jiang et al. 2022). The beneficial relationship between phylogenetically distant species and their associated microbial communities may be mediated by species-specific mutualists and negative feedbacks in pathogen colonization (Crawford et al. 2019). For example, Kempel et al. (2018) found that regionally rare plant species demonstrated increased soil biota coupled by decreased biomass in genetically similar mixtures. Similarly, plant-soil feedbacks also drive divergence in community trait optimums on a phylogenetic basis, such that phylogenetic patterns in plant-soil feedbacks can be partially explained by phylogenetic conservatism in plant traits (Senior et al. 2018). Consequently, plant-soil feedbacks can be explained by plant traits, many under selection evolutionarily, and are reflected in phylogenetic patterns of plant co-existence (Kut’áková et al. 2018). For example, Münzbergová & Šurinová (2015) and Fitzpatrick et al. (2017) both demonstrated that the intensity of plant-soil feedbacks were affected by physical plant traits such as height, specific leaf area (SLA), and leaf N and P concentration, as well as temporal traits such as plant life stage. Further, Jiang et al. (2022) suggested that divergent, phylogenetically dependent, plant-soil feedbacks exist among rare versus common species, such that rare species persist in phylogenetically distant communities, while common species perform best in phylogenetically similar communities. These phylogenetically based plant-soil feedbacks are thought to effect spatial and temporal patterns of rare versus common species differently on the basis of functional trait response (Jiang et al. 2022). For example, Reijenga et al. (2021) found that priority effects, which can include plant-soil feedbacks in which early arrival species condition soils in a way that exerts inhibitory or facilitative control on secondary communities (Chappell et al. 2022), can facilitate the persistence of rare species due to improved resistance to competitive displacement through traits promoting longevity operating in rare but not common species (McKinney 1997), leading to higher levels of metacommunity diversity. These results suggest that local plant-soil feedbacks may facilitate the phylogenetically dependent persistence of rare species in community mixtures, even with lower biomass and abundance in a given community (Kempel et al. 2020; Vincent et al. 2020; Nytko et al. in review ). Taken together, the phylogenetic relatedness of a community, as well as species’ rarity must be considered under varying soil nutrient conditions when analyzing the mechanistic drivers and evolutionary processes shaping plant-soil feedbacks across the landscape.
To understand how the evolution of performance traits interacts with the rarity and phylogenetic relatedness of species to drive variation in plant-soil feedbacks, we analyzed the above- and belowground biomass and associated ectomycorrhizal (ECM) and dark septate endophyte (DSE) colonization of 14 species of native Tasmanian Eucalyptus of known evolutionary relatedness under two N treatments (low vs. high) (data from Wooliver et al. 2018). Previous work has demonstrated that rare species have low biomass coupled with high SLA, late onset and short duration of flowering, and high tissue nutrient content (N and P), potentially caused by critically important interactions and trade-offs with mycorrhizal symbionts (Cornwell & Ackerly 2010; Holdaway et al. 2011; Ames et al. 2017; Kempel et al. 2020; Vincent et al. 2020; Lachaise et al. 2021; Nytko et al. in review ). Moreover, common ECM plant hosts demonstrate significant variation in leaf, root, dispersal, and vegetative functional traits such as SLA, specific root length (SRL), seed mass, plant height, and life span (Friesen et al. 2011). Thus, belowground mycorrhizal colonization and aboveground trait expression in rare plant species via plant-soil feedbacks may be connected. By connecting belowground fungal colonization to plant traits associated with species rarity, across soils conditioned by species varying in phylogenetic relatedness, we can utilize evolutionary history within a common garden framework to understand the connection between, and the mechanisms underlying, differing aboveground trait expression and belowground legacy effects in rare versus common species. Understanding the mechanistic role of belowground microbially mediated legacy effects in determining the persistence of rare species is a significant advance because it allows for eco-evolutionary informed predictions of rare species performance not only at a geographic level, but also at a functional level across communities varying in composition and relatedness. We hypothesized that: 1) Total plant biomass, ECM colonization, and DSE colonization vary based on the rarity of plant host; 2) Plant species inoculated by conditioned soil varying in phylogenetic relatedness (conspecific, similar, distant) from phase one, demonstrate differences in total plant biomass, ECM colonization, and DSE colonization. To understand potential mechanistic drivers of hypotheses 1 and 2, we also hypothesized that: 3) The difference between the total plant biomass of species in conspecific soil versus same lineage or opposite lineage soil is related to differing rates of ECM and DSE colonization. Our results not only confirm that rare species maintain lower levels of biomass, but also demonstrate increased ECM colonization in rare versus common species, particularly in low N conditions. These results suggest that ECM fungi may play a mechanistic role in maintaining rare species persistence, even with lower aboveground biomass, across the landscape. Microbial mechanisms underlying differences in plant-soil feedbacks of rare and common species will become increasingly important in a changing world for understanding species persistence, as well as facilitating necessary range expansion and succession.