Introduction
Plant diversity is decreasing due to ongoing land-use intensification
(Newbold et al. 2015), which has
profound negative impacts on a diverse array of ecological functions
that are critical for humanity (Cardinaleet al. 2012). In terrestrial ecosystems, increased aboveground
productivity with plant species diversity is accompanied by greater fine
root biomass and productivity (Zhanget al. 2012; Ma & Chen 2016).
This suggests that plant mixtures with increased aboveground
productivity require more water and nutrients in contrast to
corresponding monocultures. Although high demands for soil resource
uptake might be achieved by increased carbon investment to roots, i.e.,
large fine root biomass (or root mass per unit soil volume)
(Ma & Chen 2016), changes in the
architectural, morphological, and chemical traits of fine-roots may also
augment soil resource uptake (Bardgettet al. 2014; Reich 2014).
However, the global effects of plant diversity on fine root traits
remain uncertain.
Plant mixtures can increase
fine root biomass (Ma & Chen 2016) and
simultaneously alter the multiple fine root traits that influence
resource uptake capacity and efficiency (Table 1). The high demand for
soil resources in plant mixtures was observed to decrease biomass
allocation to roots in experiments conducted under optimal soil
conditions (Bessler et al. 2009;
Martin-Guay et al. 2019), but
increased this allocation to roots in natural forests where water and
nutrients are limiting (Ma et al.2019). In the soil profiles of plant mixtures, more fine root biomass
or length density might be allocated to the organic horizon where soil
nutrient contents are highest, and/or deeper soil layers where few roots
compete for nutrients or more water is available for plants when drought
occurs (Brassard et al. 2013;
Oram et al. 2018). At the
individual root level, specific root length (SRL) may increase in plant
mixtures (Shu et al. 2018) as
higher SRL increases resource uptake efficiency for a given unit of
biomass investment (Ostonen et al.2007). However, other researchers have reported insignificant
(Gould et al. 2016), or even
negative (Salahuddin et al. 2018)
effects of plant diversity on SRL. These divergent findings might have
resulted from multiple mechanisms involved with root trait changes to
meet the resource demands associated with high productivity in plant
mixtures (Table 1), including the level of species diversity in plant
mixtures, resource availability in different soil layers, changes in
resource demands associated with plant development, as well as the
background environment.
The effects of plant mixtures on plant productivity increase with plant
richness in mixtures (Zhang et al.2012). Enhanced plant productivity associated with plant richness in
mixtures shall increase the demand for water and nutrients, which leads
to greater fine root biomass, as well as changes in the traits of fine
roots. Higher species diversity is thought to be associated with a
higher complementarity effect, including resource partitioning and
abiotic facilitation (Barry et al.2019). A higher root length density (RLD) for increased resource uptake
capacity is found in more diverse plant communities
(Gould et al. 2016), which
facilitates access to water and nutrients by fine roots. Alternatively,
the higher resource demands of species-rich communities might be met by
changes in root traits toward higher resource uptake efficiency.
Therefore, we expected that a higher specific root length (SRL) and root
nitrogen content (RN) and thinner root diameter (RD) increase returns
(soil nutrients and water) per carbon investment
(Fitter et al. 1994;
Reich 2014) in species mixtures than
their averages in corresponding monocultures.
The effects of plant mixtures on fine root traits may change with stand
development. Underutilized soil space and other resources in young
stands often lead to an insignificant diversity effect on fine root
biomass and productivity (Ma & Chen
2017). In mature stands, the increasing interspecific complementarity
and decreasing functional redundancy increase the positive effects of
plant mixtures on standing biomass and productivity
(Cardinale et al. 2007;
Reich 2012), and thus increase water and
nutrient demands. Therefore, we expected that the mixture effects on RLD
and SRL would be progressively stronger in mixtures over time, due to
elevated resource demands. Alternatively, with stand development, the
higher fine-root production in mixtures could enhance carbon inputs into
the soil through the high turnover rates of fine roots over time
(Steinbeiss et al. 2008), which
might promote mineralization and increase nutrient availability
(Fornara et al. 2009).
Consequently, the high availability of soil nutrients could counteract
the high demand in older stands, resulting in no changes in species
mixture effects on fine-root traits with stand development.
The mixture effects on fine-root traits may differ between soil layers.
High resource demands in mixtures increase rooting depth to satisfy the
requirements of water and nutrients, leading to a greater rooting depth
(Oram et al. 2018). Meanwhile, the
mixture effects on RLD may increase with soil depth for a higher
resource capacity (Wang et al.2014). However, the positive effects of tree species mixtures on root
traits, such as SRL and RD were consistent across soil layers to capture
soil resources down to 17 meters in tropical plantations
(Germon et al. 2017). Conversely,
high resource demands in mixtures may lead to more fine roots allocated
to the surface soil, since it contains the highest nutrient content and
water holding capacity, due to the highest content of organic matter
(Jobbágy & Jackson 2001;
Makita et al. 2010;
Brassard et al. 2013). Moreover,
soil depth-dependent responses to species mixtures may increase with
stand age, as the positive effects of species mixtures on fine root
biomass in mixtures increase over time
(Steinbeiss et al. 2008;
Ma & Chen 2017). The uncertainty of
fine-root attributes associated with soil depth in mixtures hampers the
appreciation of fine root resource uptake strategy.
Plant mixture effects may be altered through the background environment.
Climatic parameters such as temperature and precipitation are crucial
factors on fine-root attributes (Freschetet al. 2017); however, it remains unclear how the effects of
plant mixtures on root attributes change under variable climates. More
positive plant-plant interactions have been reported in colder and dryer
sites (Armas et al. 2011;
Paquette & Messier 2011) as facilitative
interspecific interactions tend to increase with the reduced
availability of resources, as suggested by the stress gradient
hypothesis (Maestre et al. 2009;
Forrester & Bauhus 2016). This
interspecific facilitation might be decreased with mean annual
temperature (MAT) and mean annual precipitation (MAP) in plant mixtures
due to higher soil resource availability, resulting from faster
fine-root decay rates in higher MAT and MAP stands
(See et al. 2019). Therefore, the
high resource demands for fine roots may be amplified to maintain the
facilitation in plant mixtures in colder and dryer sites, which could
affect fine-root traits in species-rich plant communities. Moreover,
plant diversity effects and their temporal trends between forests and
grasslands are expected to be different primarily due to variable
species or individual recruitment rates
(Forrester & Bauhus 2016). Nevertheless,
whether plant diversity effects on fine-root traits diverge between
ecosystem types remains unclear.
Here we compiled data from
103 studies to examine the effects of plant mixtures on fine-root traits
associated with their resource uptake capacity and efficiency.
Specifically, we endeavoured to address the following queries: (1) how
do fine roots modify their traits in response to plant mixtures? (2) do
the responses change with species richness in mixtures, stand age, and
soil depth? and (3) do plant-mixture induced responses of root traits
change with variable environmental parameters?