Discussion
To the best of our knowledge, our meta-analysis has provided the first
global evidence that belowground fine-root attributes could be modified
to meet elevated resource demands in species-rich plant communities. We
demonstrated that species mixtures increased fine root biomass, with
more pronounced increases observed in older stands and deeper soil
layers. Although on average, plant mixtures did not alter other fine
root traits, the effects of species mixtures on specific root length
shifted from negative to positive with stand age, positive in
two-species mixtures to negative in more species-rich mixtures, and
positive to negative with soil depth. The effects of plant mixtures on
root length density shifted from positive to negative, mostly in
croplands, with increasing mean annual temperature. Plant mixtures had
no effects on weighted rooting depth in grasslands or planted forests
but had a positive effect under cold and moist climates, and a negative
effect under warm and dry climates in natural forests.
Unsurprisingly, we found that species mixtures, on average, increased
fine root biomass, and the positive mixture effects increased with
species richness and soil depth with more pronounced species richness
effects in both older stands and deeper soil layers. Our results
extended the aboveground overyielding to belowground
(Cardinale et al. 2007;
Zhang et al. 2012;
Liang et al. 2016), particularly,
the pronounced diversity effects in more species-rich and older stands
and in deep soils (Ma & Chen 2016). This
result supported the notion that complementary effects increase with
species richness in mixtures (Barryet al. 2019), and functional redundancy decreases with stand
age, while interspecific facilitation increases with soil depths
(Jobbágy & Jackson 2001;
Makita et al. 2010;
Reich 2012;
Forrester & Bauhus 2016). This finding
suggests elevated water and nutrient demands in species-rich and old
mixtures, leading to deeper soil exploration. Moreover, the mixture
effects on root biomass were significantly different between ecosystem
types, which might have resulted from differences in the average species
richness of mixtures between ecosystem types (Table S3).
However, contrary to the prediction of the stress gradient hypothesis,
we found that the mixture effects on root biomass increased with mean
annual precipitation, particularly in species-rich mixtures. Although
interspecific facilitation may be enhanced through resource limitations
(Maestre et al. 2009;
Forrester & Bauhus 2016), it is possible
that increased water and nutrient availability augmented niche
differentiation, which consequently leads to stronger diversity effects
on productivity (Searle & Chen 2019).
Further, in dry climates, species mixtures can increase soil moisture
content, which alleviates heightened water requirements for roots
(Lange et al. 2014). The enhanced
mixture effects on root biomass with water availability in more diverse
communities might be attributable to stronger positive resource
partitioning in species-rich mixtures
(Barry et al. 2019).
On average, root functional traits, including the root:shoot ratio,
community weighted-mean rooting depth, root length density, specific
root length, mean root diameter, and root nitrogen content, did not
differ between species mixtures and the mean of corresponding
monocultures. The lack of a mixture effect on the root:shoot ratio
suggested that fine root overyielding was of the same magnitude as its
aboveground counterpart on a global scale. Furthermore, the variations
of mixture effects on root biomass were synchronous with those of root
length density and specific root length (Fig. S2). The neutral mixture
effects may have been attributable to the fact that the majority of the
original studies consisted of two species mixtures with short
experimental durations, in which mixture effects are expected to be
minimal due to limited interspecific interactions between individual
plants (Lei et al. 2012;
Beyer et al. 2013;
Siebenkäs & Roscher 2016). Nevertheless,
the mixture effects on several functional traits were highly dependant
on the species richness in mixtures, stand age, soil depth, or
environmental stress.
We found that the effects of species mixtures on root length density
shifted from negative to positive from young to old stands, topsoil to
deep soils, and warm to cold climates. Firstly, the increasing plant
mixture effects on root length density with stand age were anticipated,
since diversity effects should facilitate fine roots to have a high
resource uptake capacity to satisfy the elevated water and nutrient
demands (Cardinale et al. 2007;
Zhang et al. 2012), which could be
achieved by the higher horizontal soil volume utilization of fine roots
in older stands (Brassard et al.2013; Ma & Chen 2017). Secondly,
increased root length density with soil depth implied that fine roots
penetrated deeper into the soil to uptake additional soil resources to
compensate for the overyielding of plant mixtures
(Zhang et al. 2012;
Ma & Chen 2017;
Oram et al. 2018). Lastly, in
colder climates where fine roots are likely to face lower resource
availability due to the slower fine root decay rate
(See et al. 2019), the increased
interspecific facilitation in mixtures
(Forrester & Bauhus 2016) might increase
root length density for an improved resource capacity. The shifted
mixture effects on root length density suggested that the intense
competition for resources overridden interspecific facilitation in young
stands, shallow soil, and colder sites.
We also found that the mixture effects on specific root length shifted
from positive to negative from two to higher numbers of species in
mixtures, topsoil to deep soils, and from negative to positive with
increasing stand age. Firstly, the decreased specific root length with
the species richness in mixtures implied that fine roots reduced
resource uptake efficiency in more diverse communities
(Ostonen et al. 2007), which might
have resulted from more intense resource competition. A recent
meta-analysis demonstrated that the soil organic carbon content
exhibited small variations with increasing species richness globally
(Chen et al. 2019), which
suggested a stable soil nutrient pool regardless of species richness.
Therefore, increased soil nutrient competition leads to a decreased
specific root length for a more conservative strategy with lower carbon
costs (Reich 2014). Secondly, in
alignment with the notion that interspecific facilitation increases with
soil depth (Forrester & Bauhus 2016), we
found that the mixture effect on specific root length decreased in
deeper soils for lower resource availability. To support aboveground
progressive overyielding with species richness
(Liang et al. 2016), the high
diversity effects on specific root length in surface soil might be a
compensating strategy of resource uptake in this root-rich soil layer
(Yuan & Chen 2010). Lastly, the
increased mixture effects on specific root length with stand age were
attributable to elevated water and nutrient demands in older stands,
which resulted in a high resource uptake efficiency. Moreover, we found
that the negative diversity effects on specific root length shifted to
neutral in older stands (> 5 years, Fig. 3b). Due to the
positive mixture effects on soil organic carbon content with stand age
(> 5 years) (Chen et
al. 2019), the intense competition for nutrients in more diverse
communities might be counteracted in older stands.
We found that plant mixture effects on root attributes were highly
dependant on the species richness in mixtures, stand age, soil depth, or
environmental stress. To address the high water and nutrient demands in
the support of greater aboveground productivity in plant species
mixtures, fine roots increased the root biomass and/or root length
density, but decreased the specific root length, in relation to both the
species richness in mixtures and soil depth. We also found that the
plant mixture effects on root biomass, root length density, and specific
root length increased with stand development. Across global climatic
variations, the mixture effects on root biomass increased with the mean
annual precipitation, and the increased trends were more pronounced in
more diverse plant communities, while the mixture effects on root length
density decreased with the mean annual temperature. Our analysis
highlights the need to incorporate the number of species in mixtures,
stand age, and soil depth profiles, toward examining mixture effects on
root attributes. Because of the dominant role of fine roots in soil
resource exploration, our results suggest that increased fine root
biomass with shifts in fine root traits enhanced soil resource uptake to
support high primary production in mixtures.
Table 1 Fine-root traits and resource uptake
strategies.