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?