Discussion
Using an isotopic ingrowth core technique, we quantified root-derived
soil C accumulation (in the bulk soil and MAOM fraction) and root
production across gradients of ECM-associated tree dominance in six
temperate forests. We found that root-derived C accumulation does not
mirror root production patterns, with greater root-derived C in
AM-dominated plots yet greater root production in ECM-dominated plots
(Fig. 2). We also recovered more root-derived inputs in the MAOM
fraction in AM compared to ECM plots (Fig. 4). Finally, our results
highlight the impressive magnitude of root-derived C inputs (199.5 ±
14.7 g C m-2 y-1), emphasizing the
importance of adequately characterizing this plant-to-soil C flux in
order to understand how tree community composition influences ecosystem
C cycling (Fig. 3).
Given that root production did not predict root-derived soil C in our
study, and that fungal production is typically greater in ECM plots
(Clemmensen et al. 2013; Cheeke et al. 2017), greater root
and/or fungal production most likely do not explain the greater
root-derived C accumulation in AM plots. Importantly, our measure of
root-derived soil C accounts for all root and fungal inputs plus
rhizodeposition that persisted in soil after two years. Data quantifying
rhizodeposition are less abundant, but previous work has found this flux
can be greater in ECM stands (Yin et al. 2014) or similar between
mycorrhizal types (Keller & Phillips 2019b). Finally, our two-pool
mixing model accounts for changes in soil C within each core. This
minimizes the effects of mycorrhizal type differences in priming on our
estimates of root-derived C. Thus, it is unlikely that the observed
variation in root-derived soil C accumulation across the mycorrhizal
gradient is principally driven by mycorrhizal type differences in root
production or rhizodeposition.
Instead, mycorrhizal type differences in root and fungal turnover
between AM and ECM trees may contribute to the greater root-derived C in
AM plots. AM plant tissues tend to decay more quickly than those of ECM
plants (Keller & Phillips 2019a; See et al. 2019), and faster
turnover rates of these tissues could result in greater total
root-derived C inputs in AM plots when measured over multiple
phenological cycles. Mycorrhizal type differences in root turnover may
also explain, to some degree, the lack of relationship between
root-derived C accumulation and root production (quantified in this
study as root biomass recovered from ingrowth cores after two growing
seasons). Likewise, turnover of AM fungi can exceed that of ECM fungi by
an order of magnitude (Staddon et al. 2003; Tedersoo & Bahram
2019). Differences in fungal turnover rates between mycorrhizal types
may be particularly important in driving root-derived soil C
accumulation as fungal inputs to soil C have been shown to exceed that
of both leaf and root litter (Godbold et al. 2006).
The greater recovery of root-derived C in AM soils also reflects
mycorrhizal-associated differences in soil organic matter formation
pathways. Whereas plant inputs to ECM soils tend to accumulate in
organic horizons or particulate C pools, there is increasing evidence
that AM systems transfer greater amounts of plant-derived C into
mineral-associated forms (Cotrufo et al. 2019) and our results
support this idea (Fig. 4). Faster decomposition of AM inputs leads to
more microbial products which are important MAOM precursors (Cotrufoet al. 2013). To the extent that MAOM cycles slowly and protects
C from microbial decomposers (Grandy and Neff 2008, Bradford et al.
2013, but see Jilling et al. 2018), this could explain the greater
root-derived C accumulation in both the bulk soil and MAOM fraction in
AM compared to ECM soils. Our ingrowth core method did control for
edaphic differences (cores were filled with a uniform soil matrix across
all plots and sites) and thus differences in microbial and soil C
cycling dynamics driven by edaphic factors were minimized. However, soil
C cycling is also driven by distinct plant and microbial traits which
can promote (or reduce) soil C aggregation and stabilization (Cheng &
Kuzyakov 2005; Schmidt et al. 2011). For example, AM fungi are
known to produce an aggregate-promoting glycoprotein (Rillig 2004),
while ECM fungi have greater oxidative enzyme capacity to destabilize
organic matter (Shah et al. 2016). In this way, the observed
inverse relationship between root-derived soil C and ECM dominance (Fig.
1a) may reflect differences between mycorrhizal types in their input
chemistry, and in their capacity to destabilize soil organic matter to
acquire nutrients.
While root-derived soil C accumulation in forests has been poorly
quantified to date, our estimates are similar in magnitude to previous
studies using the isotopic ingrowth core technique. Across all plots in
our study, root-derived soil C averaged 199 g m-2y-1 (ranging from 59 to 500 g m-2y-1). In an ECM-dominated 130-year old forest,
Martinez et al. (2016) estimated root-derived C inputs to be 303 g
m-2 y-1, and Panzacchi et al. (2016)
reported a similar rate (309 g m-2y-1) in a young mixed hardwood plantation. Moreover,
mean root-derived C inputs were estimated to be ~40%
and ~70% of ANPP at these sites, respectively. Across
our six temperate forest sites, we found root-derived C to range from
74% (HF) to 157% (SERC) of ANPP. While our ANPP estimates (SI Fig. 1)
may be conservative given that we excluded both small, understory trees
(i.e. < 10 cm diameter, including individuals that grew into
the >10 cm diameter class between measurement periods) and
trees that died between measurement periods, annual root-derived C
accumulation is still larger on average than leaf litter flux (Fig. 3;
SI Fig. 2). This highlights the relative importance of belowground C
inputs to soils and suggests that models that presume the primacy of
leaf litter fluxes are drivers of soil C dynamics may be underestimating
the importance of root dynamics.
Overall, our results suggest the magnitude of root-derived soil C inputs
is large and can vary significantly across sites and mycorrhizal types.
Importantly, we show direct evidence of distinct plant mycorrhizal type
effects on soil C formation. Accurate predictions of ecosystem C cycling
in ecosystem and land surface models depend on improved quantification
of the belowground C flux from plants to soil C pools, and improved
understanding of the factors that control soil C stabilization. Our
results suggest that better estimates of root and fungal contributions
to stable soil organic matter pools are clearly needed in order to
better understand how plant species shifts affect ecosystem C cycling
now and in the future.