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.