The problem
A trait is an attribute influencing an organism’s performance within its
environment, encompassing morphological, genetic and physiological
characteristics measured at the individual or population levels
(Salguero-Gómez et al. , 2018; Zhang et al. , 2023a).
Understanding the ecology of species using a trait-based approach can
contribute to a mechanistic explanation of processes mediated by
microbes, including those that affect ecosystem functioning
(Romero-Olivares et al. , 2021). This approach holds particular
significance for arbuscular mycorrhizal (AM) fungi - Phylum
Glomeromycota. As obligate symbionts of plants, where multiple species
colonize both roots and soils in a network, predicting the functional
outcomes (e.g., host growth, plant community diversity, soil
characteristics) of individual AM fungal genotypes and communities
within ecosystems remains challenging, despite major developments in
molecular methods in the last two decades (Tisserant et al. ,
2013; Montoliu-Nerin et al. , 2021). Indeed, establishing
connections between AM fungal taxa and/or genotypes (e.g., within
species) and their functional roles is a laborious process, which is
expected to continue in the foreseeable future (Serghi et al. ,
2021; Manley et al. , 2023). This is needed due to the complex
links between AM fungi and functional outcomes for both hosts
(e.g. , plant growth and fitness, nutrient uptake and stress
tolerance) and soil functions/properties (e.g. , carbon storage,
aggregate stability, biotic diversity), which appear to be highly
context dependent and relatively poorly predicted by taxonomy alone
(Munkvold et al. , 2004; Koch et al. , 2017; Yang et
al. , 2017; Qiu et al. , 2021). However, this effort is also
required because AM fungal traits have not been systematically assessed
alongside with hypotheses of adaptation or with specific mechanisms in
mind. For example, small-spored AM fungi may be dispersed longer
distances by wind than large-spored AM fungi. It is then a reasonable
hypothesis that small spore size is an adaptation for wind dispersal.
One could empirically observe that small-spored AM fungi are
geographically more widespread than large-spored fungi and this
potential result could be viewed as evidence in support of this
hypothesis. However, this finding would not necessarily prove that such
dispersal difference has “functional” or “adaptive” value.
Alternatively, producing small spores is a correlated response to
producing many spores quickly, which itself could be an adaptive
response to the likelihood of unpredictable soil disturbance such as
from tillage. In this scenario, the adaptation and/or function is the
production of many spores quickly to confer resistance to disturbance
and then, after soil disturbance with wind erosion, small spores may
also be blown farther (which may or may not improve fitness). Another
example, variation in rooting depth among plants in a community may
contribute to resource partitioning. But the mechanism (differential
resource depletion with depth) still needs to be demonstrated separately
from the trait evidence. AM fungi could contribute to equalize resource
partitioning if plants with short roots associate with AM fungi that
form more extensive extra-radical mycelium and vice-versa. Given these
complexities, we consider the development of a robust, universally
applicable trait-based framework for predicting key AM fungal functional
outcomes a priority. To achieve this objective, first we must identify
AM fungal traits that can be measured at morphological, physiological,
and genetic levels. Second, considering the important roles of AM fungi
in ecosystems, affecting host plants, soil, and the AM fungi themselves,
we need to discern/hypothesize how measuring AM fungal traits impacts
each of these components. For the host plant, it is crucial to consider
nutrition, biomass, fitness, and survival in face of pathogens, heavy
metals, salinity, drought, etc. (Delavaux et al. , 2017; Wehneret al. ). Within the soil environment, AM fungal effects on soil
structure (Rillig & Mummey, 2006), nutrient cycling, carbon storage,
and other members of the soil food-web are paramount (Antunes & Koyama,
2016; Frew et al. , 2021; Horsch et al. , 2023a). Regarding
the fungal organism, we should focus on key aspects of their
life-history strategies; reproduction and fitness, survival, dispersal,
competitive ability, infectivity and abundance both within the host and
soil environments (Aguilar-Trigueros et al. , 2019; Chaudharyet al. , 2020; Deveautour et al. , 2020). This requires
identifying relevant proxies (sometimes termed “soft traits” in the
plant ecophysiology literature) to provide easy-to-measure quantitative
metrics for such complex facets of fungal life-history that can be
measured across several species. Third, we need to evaluate existing
standardized methods and experimental designs, or develop new ones, to
measure such relevant (soft) traits, as has been done in plant
ecophysiology (Pérez-Harguindeguy et al. , 2013). Measurement
standardization and relevant metadata for hypothesis-driven analysis and
interpretation is essential if we are to aggregate trait information
from different studies into a public database, facilitating their
incorporation into earth system models (e.g., (Fry et al. , 2019)
and enhancing the predictability of functional processes and/or
adaptations associated with AM fungi. Analogous libraries on plant
traits (Kattge et al. , 2020) have proved useful to better
understand trait variation along global climatic gradients (Butleret al. , 2017). Here, we aim to:
- To comprehensively catalog and define AM fungal functional traits
(morphological, physiological/phenological, and genetic) while
avoiding redundancy.
- To elucidate the relationships between these traits and their
functional outcomes for host plants, soil environments, and the AM
fungi themselves.
- To critically review the historical methods and experimental designs
employed in measuring AM fungal traits, highlighting their strengths
and limitations.
- To propose standardized methodologies and protocols for measuring AM
fungal traits.
- To explore the integration of AM fungal trait information into
ecological models to enhance ecosystem processes’ predictability.