A functional trait framework for integrating nitrogen‐fixing cover crops into short‐rotation woody crop systems

Developing approaches to simultaneously maximize short‐rotation woody crop (SRWC) productivity while minimizing footprints associated with intensive management is imperative to profitable and sustainable bioenergy production systems. Intercropping nitrogen (N)‐fixing cover crops in SRWC systems is an overlooked approach to sustainably intensify SRWC production by increasing N availability using less environmentally costly inputs. Here, we discuss how functional traits (e.g., seasonal activity, lifespan, leaf habit, soil exploration) of cover crops and SRWCs may interact through space and time influencing access to light, water, and nutrients to provide a framework for successful integration of cover crops into SRWCs. Next, we summarize the literature on intercropping forest plantations with N‐fixing cover crops to identity research gaps and outline future research needs and opportunities. And then, using empirical N demand and productivity data from SRWCs and cover crop N inputs from the literature, we illustrate how SRWC leaf habit (conifer evergreens and deciduous hardwoods) would influence successful integration of cover crops and potential N fixation. We estimate that integrating cover crops into SRWCs could supply 27% and 72% of the N demand across a 10‐year rotation for an evergreen and a deciduous hardwood, respectively. These figures suggest these integrated SRWC systems may approach a virtual minimal external N input when other biogeochemical cycles are considered. The guiding principles presented here are grounded in ecological theory and provide a framework for sustainable intensification of forest production.

. Hereupon, short-rotation woody crops (SRWCs) have emerged as a promising and sustainable option to increase woody feedstock supply (Kline & Coleman, 2010). SRWCs are intensively managed production forestry systems harvested in shorter timescales (e.g., ~3-10 years) than traditional forestry (e.g., 25+ years). Production forestry generally is a net carbon (C) sink, but intensive management (e.g., soil preparation and repeated herbicide, pesticide, and fertilizer applications) unbalances production footprint. As a result, these activities, while fundamental to achieving higher productivity in shorter timescales, may shift the final energy product further from a net C sink or neutrality (Markewitz, 2006). Moreover, minimizing nitrogen (N) pollution and reducing greenhouse gas (GHG) emissions from intensive management practices (e.g., leaching or gaseous N losses from excessive fertilizations) are fundamental to maintain environmental quality and achieve climate change targets Griffiths et al., 2019;Kanter, 2018). Therefore, developing innovative approaches to simultaneously maximize SRWC productivity while minimizing the environmental costs associated with intensive management is imperative to make SRWCs profitable and sustainable bioenergy production systems.
Intensive management of SRWCs resembles row-crop agriculture with respect to inputs (e.g., herbicide, pesticide, and fertilization), but the perennial nature of the cropping system resembles traditional forestry (Griffiths et al., 2019;Rubilar et al., 2018). As such, SRWCs are at the interface of agriculture and traditional production forestry; exploring ways to maximize SRWC productivity and reduce the environmental footprint should then begin with assessing techniques and approaches that have moved agricultural and forestry systems toward these goals. Agriculture has increased the sustainability of production systems for decades through reduced or zerotill practices and cover cropping/crop rotation (Harvey et al., 2014;Paustian et al., 2016;Robertson et al., 2014;Robertson & Swinton, 2005;Steenwerth et al., 2014). In forestry, mixed-species plantations take advantage of potential complementarity between species to offer greater levels of ecosystem services and shift the focus away from extensive industrial monocultures (Forrester & Pretzsch, 2015;Kelty, 2006;Nichols et al., 2006). Similarly, agroforestry, that is, integrating trees into agricultural systems, is often considered a low C land use system that exhibits other benefits, such as increased nutrient use efficiency, improved soil and water quality, and provisioning of habitat to support biodiversity Muchane et al., 2020;Tsonkova et al., 2012).
These more sustainable production systems are often built upon multi-species interactions through space and time. Benefits of species interactions are maximized when the mixture contains a N-fixing species, which lessens the need for external N addition and minimizes potential N losses and threats caused by excessive inorganic N inputs (Reich & Oleksyn, 2004). Yet, the mentioned alternatives cannot be directly transferred to SRWCs. For instance, agroforestry alley cropping uses wider planting alleys between tree rows, thus have limited wood yield on a hectare basis (Zamora et al., 2009). Mixed-species forest plantations add complexity to forest management (e.g., distinct silviculture demand and harvesting cycles), but benefits to overall yield are highly context dependent (Bouillet et al., 2013;Liu et al., 2018;Marron & Epron, 2019). Plus, species interactions are not consistent throughout stand development in mixed-species forests (Paula et al., 2018;Rothe & Binkley, 2001). Often, interspecific interactions are limited during early stand development due to the open canopy, relatively low litterfall deposition, and undeveloped site exploration and root associations (Forrester, 2014;Paula et al., 2018;Rothe & Binkley, 2001). The shorter harvesting timeframe in SRWCs makes early stand development a critical period. First, early gains in tree growth can be long lasting and more cost-effective (Subedi & Fox, 2016). Second, while trees respond to nutrient inputs, fertilizer-uptake efficiency is relatively low (Aubrey et al., 2012), which can generate significant nutrient losses (leaching and/or gaseous) (Lee & Jose, 2005). And third, early stand development is a period when stands are most prone to erosion, water evaporation, and weed development. Many of these issues have been addressed in production systems by mixing species with different traits (e.g., seasonal activity, lifespan, and rooting patterns) in space and time and having better and longer soil coverage through rotating crops, cover cropping, and intercropping, but still lack in SRWCs.
Cover cropping is primarily implemented to minimize losses, reduce inputs, and improve aspects of soil health (e.g., reduce erosion, weed development, and nutrient leaching, add N-fixation, and increase soil C) rather than being a standalone harvest crop. Intercropping annual crops in the inter-row of regularly spaced SRWCs (e.g., cover cropping) may provide similar benefits, but there is no guiding principles and limited documentation of the integration of cover crops into SRWCs, that is, into forest plantations where regular spacing was not altered. A common concern limiting the integration of cover crops into SRWCs is the exacerbation of competition for resources (e.g., light, nutrients, water), restricting either wood production or cover crop cultivation. Nevertheless, understanding of species interactions related to resource acquisition may minimize these potential issues. We posit that consideration of SRWC and cover crop traits such as leaf habit and seasonal physiological activity control species interactions and may shift interactions from competition to facilitation, thereby driving integration success.
Here, we discuss a largely overlooked, but promising alternative for ecological intensification of tree plantations and climate-smart forestry (see Gómez-González et al., 2022;Verkerk et al., 2020). We summarize literature on integrating N-fixing cover crops into SRWCs and discuss how functional traits (e.g., seasonality, lifespan, leaf habit, soil exploration) of cover crop and SRWC species may interact spatially and temporally to influence light, water, and nutrient (mainly N) availability. The consideration of functional traits provides a framework for integrating N-fixing cover crop species into SRWC systems such that their simultaneous cultivation increases wholesystem N cycling potential while minimizing competition for resources in space and time, which ultimately maximizes SRWC productivity and minimizes external inputs. We explore and illustrate the potential benefits and necessary considerations of integrating N-fixing cover crops into SRWCs (i.e., mixing species in space) throughout the rotation, and provide guiding principles for an approach that can facilitate the sustainable intensification of SRWC production. In the end, we bring the attention to the potential of rotating N-fixing and non-N-fixing SRWCs (i.e., mixing species in time) to mitigate soil N depletion and serve as an alternative to further enhance overall soil health and sustainably explore marginal lands, which is still incipient and seemed unthinkable in traditional forestry given long rotation periods, but may be conceivable in SRWC systems.

SRWCs
SRWCs are production systems that share a similar principle with intensive agriculture and plantation forests namely land sparing or plantation conservation benefit, which proposes that increasing yields in limited area spares land for conservation (Baudron et al., 2021;Heilmayr, 2014;Pirard et al., 2016). As such, SRWCs differ dramatically from native environments in the ecosystem services provided (Paquette & Messier, 2010). While SRWCs offer wood provisioning, C sequestration, bioenergy feedstock, and reduce pressure on native forests, SRWCs have a costly environmental impact of lacking biodiversity. Also, routinely employing silviculture practices such as soil preparation, herbicide, pesticide, and fertilizer applications, may impair wildlife habitat (Miller & Miller, 2004), soil properties (Mayer et al., 2020), water quality (Griffiths et al., 2017;Lee & Jose, 2005), and contribute to GHG emissions (Albaugh et al., 2012;Markewitz, 2006). Intensive management of forest plantations has evolved concurrently with our better understanding of silvicultural effects on the environment and forest productivity as well as advances in technologies (Rubilar et al., 2018). As consequence, current best management practices seem effective at reducing environmental impacts on water and soil quality (Griffiths et al., 2019) and also provide temporary habitat and corridors for wildlife (Amazonas et al., 2018). Yet, while SRWCs take advantage of this silviculture development, the greater intensity and frequency of silvicultural practices employed in SRWCs challenge the applicability of forestry best management practices to SRWCs (Griffiths et al., 2019) and can undermine expected C-sink strength given the reliance on environmentally costly inputs.
The C footprint of SRWC production is intimately related to silvicultural practices. While silvicultural practices have a C-cost, they increase the C-sink strength of forests through increased biomass production, often surpassing associated C emissions (Albaugh et al., 2012). Silvicultural practices influence components of the forest C budget other than biomass such as the forest floor and soil organic C (Mayer et al., 2020), which must be accounted for in thorough C balances (Bossio et al., 2020;King, 2004). In fact, a positive influence of management on soil C accumulation may be pivotal for a net positive forest C storage when GHG emissions from silvicultural practices are accounted for (Markewitz, 2006). Calculations of GHG emissions from forest intensive management are scarce, with most being estimated for traditional forestry (Albaugh et al., 2012;Markewitz, 2006). For instance, the C emission (as kg of C-CO 2 ) for N fertilization ranges between 0.9 and 1.8 kg of C for each kg of N, as a result of production, packaging, storage, and distribution of fertilizers (Lal, 2004). Direct N 2 O emissions are around 1% for each kg of N applied (De Klein et al., 2006). Additional costs may need to be considered associated with indirect N 2 O emissions (e.g., leaching and volatilization) to fully account the environmental costs of fertilizer application (De Klein et al., 2006). These costs may substantially add up given the large amounts of N needed to sustain expedited tree growth (e.g., 100 kg N ha −1 year −1 ; Borders & Bailey, 2001;Coyle et al., 2016;Lee & Jose, 2005), but particularly since tree fertilizer-N uptake can be less than 50% of the N input during periods of stand development (Albaugh et al., 2008;Aubrey et al., 2012;Raymond et al., 2016). In SRWCs, the impact of silvicultural activities per unit of captured C is likely more intense than traditional forestry since C accumulation in the living biomass is short-lived and forest floor and soil C accretion are more strongly dependent upon management (Mayer et al., 2020). Moreover, short-rotation management implies reduced nutrient cycling potential and more frequent nutrient and C exports, which suggest higher dependency on external inputs, thus raising concerns about the sustainability of SRWCs across multiple rotations (Heilman & Norby, 1998).
To finalize, we highlight two additional issues that may be a concern in future SRWC management dependent on external inputs. Current increases in atmospheric CO 2 concentration are expected to act as a CO 2 fertilizer, but downregulation mechanisms are also expected to occur. Nutrient limitation is speculated to be the primary cause for reduced or null response of forest productivity to increasing CO 2 (Gedalof & Berg, 2010;Reich et al., 2006). Higher tree growth will likely increase N demand and enhance N sequestration in long-lived tissues and exported biomass at harvesting. Thus, N availability may progressively decline (Luo et al., 2004), which may have cascading consequences for ecosystem productivity and capacity to store C (Van Groenigen et al., 2017). These predicted patterns and processes frame important questions for the future of SRWCs. It is not the objective of this study to provide any economic consideration, but a few questionings are in order. Maximizing financial returns in forestry is dependent upon increased yields and so upon optimized silvicultural practices (Coyle et al., 2013;Gallagher et al., 2006;Munsell & Fox, 2010). Can we rely only on mineral fertilizer inputs? Will SRWC be profitable with the increasing fertilizer demand, depleted mineral sources, and fertilizer price fluctuation? For instance, urea prices have increased 480% in the last 30 years, with prices fluctuating more 100% in a single year (Indexmundi, 2022). This highly dynamic market increases uncertainty in long-term planning activities such as forestry. Thereby, exploring approaches that can reduce fertilizer inputs while maintaining productivity is imperative for the sustainable management of SRWCs.

IN MIXED -SPECIES PRODUCTION SYSTEMS
The economic and environmental costs of fertilizers and pesticides, productivity losses from pests, diseases, and climate change, and reduced biodiversity have raised concerns about monocultures and encouraged research on mixed-species production systems. These systems aim at mimicking natural environment species interactions to provide a broader range and greater levels of goods and environmental services, albeit in a simplistic fashion that allows operationalization and maximize yield (Ashton & Ducey, 1996;Cardinael et al., 2020;Kelty, 2006;Loreau & Hector, 2001). Species interactions are ubiquitous in plant mixtures and are often described in terms of competition, competitive reduction, and facilitation. These interactions occur both spatially, belowground (e.g., access to water and nutrients) and aboveground (e.g., access to light) (Cardinael et al., 2020;Loreau & Hector, 2001;Vandermeer, 1989), and temporally, through seasonal changes or across stand development (Forrester, 2014). Competition occurs when species or populations interact with one exerting a negative effect on the other. Competitive reduction and facilitation are positive species interactions (or interspecific competition is less than intraspecific competition) that are often collectively described as complementarity as they occur simultaneously and are difficult to quantify individually (Forrester, 2014).
Comparisons of monoculture and mixed-species forest plantations have indicated that mixed species plantations can provide higher levels of nutrient cycling and soil fertility (Bouillet et al., 2008;Forrester et al., 2005;Pereira et al., 2018;Santos et al., 2017) and reduced demand for external inputs (e.g., herbicides and/or fertilizers) with the presence of a N-fixing species (Marron & Epron, 2019). However, concerns about overall productivity are still an obstacle. To minimize competition, tree stocking is frequently held constant and mixed stands are established following a replacement series design where one species replaces a percentage of the other. Therefore, total stand complementarity effects should be strong enough to result in overyielding-when the mixed-species stand is more productive than the monoculture stand under the same density. A meta-analysis demonstrated that mixed-species forest plantations containing N-fixing and non N-fixing tree species (economic target) were ~18% more productive than monocultures (Marron & Epron, 2019). However, the success of mixtures was geographic and site dependent; mixed-species plantations were most productive across temperate regions and on sites with low nutrient availability (Marron & Epron, 2019). These results are consistent with the slower N mineralization rates in temperate than tropical regions, which increase productivity responses to external N additions, and with the stress-gradient theory, which predicts positive effects (complementarity) should prevail over negative effects (competition) in sites with adverse conditions (Forrester, 2014;Marron & Epron, 2019).
An issue of mixed-species forestry for SRWCs is the temporal dynamics of species interactions (Forrester, 2014). The extent of N-fixation is species dependent and also proportional to the N-fixing tree basal area (Staccone et al., 2020); however, a disaggregation of the basal area influence on N fixation suggests that this relationship may be more complex (Rothe & Binkley, 2001). For instance, studies suggest that N fixation is linearly related with the percentage of N-fixing trees within a stand and positively, but nonlinearly, associated with the increase of N-fixing tree size (Paula et al., 2018;Rothe & Binkley, 2001). The interspecific N cycling is dependent on litterfall deposition and belowground processes-direct N transfer from intermingling roots and common mycorrhizal networks (Paula et al., 2015). Considering that most mixed-species, evenaged plantations are established following the replacement series design, tree N-fixation and nutrient return to soil presumably will increase through development and greater site occupancy (Paula et al., 2018). However, interspecific competition will increase concurrently as sites reach carrying capacity (Rebola-Lichtenberg et al., 2021). Altogether, one can argue that N-fixation and interspecific N cycling can only be increased until a certain extent and may be particularly limited during early stand development. Increasing N availability through N fixation during early forest development may be most critical and cost-effective because trees respond positively to fertilization  and expedited early growth may persist throughout a rotation (Coyle et al., 2008(Coyle et al., , 2016Subedi & Fox, 2016). However, fertilizer-uptake efficiency is relatively low (Aubrey et al., 2012), which can generate significant N losses (Lee & Jose, 2005). The biologically fixed N may have a slower turnover and favor N uptake (Di & Cameron, 2002;Gómez-Rey et al., 2008;Kramer et al., 2006;Poudel et al., 2002), minimizing environmental threats of highly mobile excess N.

COVER CROPS INTO SRWC
Increasing soil cover with annual winter N-fixers during early SRWC development may minimize the asynchrony in N dynamics previously discussed. Annual plants reach maximum fixation within a single growing season; winter annuals would senesce during the SRWC's active growing season, making the fixed N available. In addition, covering SRWC inter-rows can buffer soils against erosion (Malik et al., 2000) and reduce water evaporation and weed development (Teasdale, 1996), which are all prevalent during early forest stand development (Zutter & Miller, 1998). SRWCs customarily implement regular, dense spacing to ensure fast and homogeneous site occupancy. Therefore, a common concern limiting the integration of cover crops into SRWCs is the exacerbation of competition for resources (e.g., light, nutrients, water), restricting site capacity to either wood production or cover crop cultivation. However, until individual tree crowns and root systems expand and overlap with neighbors (i.e., canopy and root closure, respectively), there is ample space for cultivating an annual crop between tree rows with respect to both light and soil resource availability. Given the distinct pattern of soil exploration and physiological activity, the use of winter annual crops intercropped with SRWC may actually increase the spatial and temporal complementarity in site resource use throughout the year. Furthermore, we posit that consideration of regional climate and species functional and physiological traits may provide ample opportunity for cultivating cover crops in the alleys between tree rows throughout a SRWC rotation.
Canopy closure occurs around years 3-5 in fast-growing forest plantations across tropical and warm temperate climate zones (Binkley et al., 2010;Will et al., 2005). While understory light availability will depend on canopy complexity, it seems impractical to grow any light dependent cover crop within an evergreen SRWC stand after canopy closure (Balandier et al., 2006;Gaudio et al., 2011). On the other hand, deciduous trees shed leaves during cold seasons, which would allow ample light through the canopy to grow a winter active or overwintering cover crop throughout a rotation (Figure 1a,b). Similarly, water and nutrient availability limit forest productivity worldwide. While introducing N-fixing cover crops into SRWC may exacerbate competition for water and nutrients, consideration of species traits and complex belowground interactions can alleviate competition and even promote complementarity through interspecific interactions, better soil exploration, and alteration of ancillary soil properties. Perennials and warm season cover crops are more likely to compete with SRWC as periods of peak photosynthetic activity overlap. In contrast, winter annual crops activity peaks when SRWCs exhibit reduced activity or dormancy (evergreens and deciduous hardwoods, respectively) ( Figure 1c). These contrasting seasonalities are more evident across temperate regions. Moreover, annual crops tend to root shallower than trees. Therefore, the integration of winter annual cover crops in deciduous SRWC may not result in substantial interspecific competition in temperate zones and provide for a spatial and temporal complementarity in light and soil exploration throughout the rotation (Figure 2). It is important to note that cold-temperate regions may offer harsh environmental conditions for winter cropping and more careful species selection may be needed.
Differences in seasonal activity and soil exploration may favor direct and indirect nutrient and water transfer between species. Specifically, by increasing the temporal complementarity of interspecific N-cycling through a more synchronized litter deposition and root senescence with other species peak demand, and by promoting the safetynet and pump hypotheses (Jobbágy & Jackson, 2000;Rowe et al., 1999;van Noordwijk et al., 1999). These hypotheses explain the potential resource synergy between different niche plants when grown on the same site. The safety-net hypothesis is based on the premises that deep rooting tree species can utilize nutrients that have leached from upper soil layers, where most roots from annual crops are concentrated (Rowe et al., 1999;van Noordwijk et al., 1999). The pump hypothesis posits that trees work as a water and nutrient pump redistributing water and nutrients from deeper to upper soil layers, respectively (Jobbágy & Jackson, 2004). These processes limit nutrient leaching and promote the access of shallow rooted plants to water and nutrients that were previously inaccessible (Bayala & Prieto, 2019). While these mechanisms are known to exist, they are complex and the extent of their contribution to water and nutrient uptake in production systems is yet unclear. The proximity between trees and annuals intercropped in SRWC and the intensity of management makes it an ideal system to study the safety-net and water and nutrient pump hypotheses under field conditions.
To support our claims and better understand the impacts of the integration of winter annual N-fixing cover crops into SRWCs, we extensively compiled evaluations of intercropping forest plantations with N-fixers in which regular plantation spacing was not altered (Text S1). We used the following criteria: (1) field study with a reference SRWC monoculture under similar stocking; (2) rotation length or plantation age <10 years; (3) minimum tree stocking density of 1000 trees ha −1 ; and (4) availability of a tree growth metric. Details about the literature search are presented in Text S1. We identified a total of 20 peerreviewed studies representing tropical (n = 3) and temperate (n = 17) regions.
Our literature review suggests that woody crop responses to cover cropping with N-fixers vary by climate conditions and the seasonality and other traits of the cover crop and/or the woody crop species. In tropical regions, N-fixing cover crops had null or negative effects on tree growth; these studies provided limited information about ecosystem-soil or plant-N status (Little et al., 2002;Lulandala & Hall, 1987;Mendham et al., 2004). In temperate regions, N-fixing cover crops had mixed effects on tree growth (Table 1) (Cogliastro et al., 1990;Haines et al., 1978;Malik et al., 2001;Smethurst et al., 1986), but there is evidence that winter crops are less likely to compete with trees compared with perennials or summer crops (Haines et al., 1978;Redmon, Rouquette, Goad, et al., 1997;Silvestri et al., 2018;Smethurst et al., 1986;Van Sambeek et al., 1986). The evidence for better complementarity in intercrops with deciduous hardwoods than evergreens was rather weak, but few studies provided multiyear or rotation length comparisons. Studies that reported negative effects of cover crop on hardwood growth indicated that competition could be alleviated by adjusting cover crop seeding rate or alley width (Malik et al., 2001;Shults et al., 2020). Indeed, consideration of total site carrying capacity may be warranted as the two studies with Salix sp. reported negative effects of cover cropping (Albertsson et al., 2016;Arevalo et al., 2005); Salix sp. stands are often established using a stocking density up to 10 times greater than other common SRWCs. It is important to note that we compiled the performance of integrated SRWCs against the best alternative treatment (e.g., monocultures treated with herbicide and/or fertilizer; F I G U R E 1 Expected temporal patterns in deciduous hardwood and evergreen short-rotation woody crop (SRWC) stands with respect to resource availability in temperate regions. (a) Light availability is high throughout the year in both evergreen and deciduous hardwood SRWCs during early stand development (e.g., 3-5 years); afterwards, light availability during winter remains high in a deciduous hardwood stand because of annual leaf shedding, whereas canopy progressively closes and decreases light availability through development in an evergreen SRWC. (b) Seasonal changes in understory light availability in evergreen and deciduous hardwood SRWCs after canopy closure development stage; leaf shedding increase understory light availability during cold seasons in deciduous hardwood SRWC, whereas understory light availability remains low in evergreen stands throughout the year. (c) Seasonal competition dynamics for water and nutrients in evergreen and deciduous hardwood SRWCs; deciduous hardwood and evergreen SRWCs exhibit dormancy or reduced activity, respectively, during cold seasons; deciduous hardwoods would exhibit a more expressive seasonal pattern. Table 1). However, all integrated SRWCs but Albertsson et al. (2016) performed better or at least rivalled no input controls. Some studies reported no effect on tree growth but indicated that introducing N-fixing cover crops into SWRC has potential to reduce external N dependence by increasing overall site N availability or tree N status (Carlson et al., 1994;Silvestri et al., 2018;Smethurst et al., 1986;Van Sambeek et al., 1986;Vidal et al., 2019), which may have a positive effect on tree growth in subsequent growing seasons. There is limited information on N fixation rates, but studies suggest that cover crops can accrue 37-136 kg N ha −1 year −1 (Shults et al., 2020;Silvestri et al., 2018;Smethurst et al., 1986)-estimated as N balance. The fact that literature on the topic is sparse and inconsistent stresses the need for further research to better understand and deploy these systems. Some inconsistencies likely arise from variation in species, study duration, or the management approach, which should be somewhat standardized in future studies for meaningful comparisons.
To illustrate the amount of N that could be supplied by intercropping a N-fixing cover crop within SRWC stands, we used empirical N demand and productivity data from SRWCs and cover crop N inputs from the literature in a modeling exercise (Figure 3). We used empirical above-and belowground N uptake data from sweetgum (deciduous hardwood) and loblolly pine (evergreen) SRWCs grown side-by-side under optimal conditions (fertilization and irrigation) to estimate peak rotation-length N uptake (Coyle et al., 2016). We assumed canopy dynamics and below-canopy light availability changed with stand development (Figure 1) to infer competition between the cover crop and SRWC species throughout a rotation. Cover crop N content F I G U R E 2 Conceptual representation of short-rotation woody crop (SRWC) monocultures (left) and integrated SRWC with N-fixing winter cover crops (center and right). SRWC integrated or not systems are assumed to exhibit similar productivity (which varies by SWRC species) due to the different soil exploration zones and seasonal growth activity. SRWC's leaf habit will influence cover-crop cultivation (and the magnitude of fixed-N input) throughout the rotation by controlling understory light access during winter. N-inputs from cover crops will be limited by canopy closure (~3-5 years) in evergreens (center) but will continue through the entire rotation for deciduous woody crop species (right). SRWC's traits (leaf and N demand) will then influence external N requirements and interspecific N-cycling, with external N requirements and N-leaching maximized in monocultures, particularly for non-N-fixing SRWC's, and minimum in deciduous SRWC intercropped with N-fixing winter cover crop. Deciduous SRWC intercropped with N-fixing winter cover crop will exhibit greater complementarity (N cycling) between species (cover crop and tree root interactions are represented by yellow dots at root connecting points; yellow and blue arrows represent nutrient and hydraulic uplifts, respectively, and subsequent access by shallower root plants), higher C and N inputs to the soil, and thus an overall healthier soil (represented by a darker soil color).
T A B L E 1 Literature summary of intercropping forest plantations with N-fixers in which regular plantation spacing was not altered across temperate regions. See Text S1 for detailed information about search parameters.
↑, ↓, and ─ indicate positive, negative, and null effects on different properties, respectively. n/a means information was not available; mix means a mixture of species were used. The outcome of cover cropping effect on stand properties is compared with the best performing monoculture treatment (e.g., treated with herbicide or fertilizer) available in each study. Timeframe refers to either study duration or stand age during the evaluation. Latitude (Lat) and longitude (Long) are given in decimal degrees. Climate definitions follow Köppen-Geiger classification and were obtained using the "kgc" package (Bryant et al., 2017)  was used as a surrogate for N fixation as it was the most commonly reported property from compiled studies ( Table 1) that had any metric of N input (Shults et al., 2020;Silvestri et al., 2018;Smethurst et al., 1986). Direct measurements of N fixation were unavailable. Regardless, studies consistently compared intercropped stands with monoculture stands, so the metric seemed reasonable as additional N in the system sequestered by the N-fixer. Also, the average N input (86 ± 29 kg N ha −1 ; Figure 3) is conservative if compared with potential cover crop N inputs (e.g., 143 kg N year −1 ; Anderson et al., 2022) in the southeastern US-where our tree N demand data came from-and it is within range of N fixation rates by grain legumes globally (Palmero et al., 2022). F I G U R E 3 N input and demand in simulated short-rotation woody crops (SRWCs) based on N uptake of a deciduous hardwood (sweetgum) and an evergreen (loblolly pine) with a winter N-fixing cover crop (N input) throughout a 10-year rotation. Sweetgum and loblolly pine exhibit similar cumulative N uptake (total difference <50 kg N ha −1 ) and were combined for simplicity. Error bars represent standard deviation. The mean and standard deviation N input (86 ± 29 kg N ha −1 ) from cover crop was obtained by a Monte Carlo simulation with 10,000 replications and a uniform distribution function based on literature N input range in intercropped SRWC systems (37-136 kg N ha −1 year −1 ; Shults et al., 2020;Silvestri et al., 2018;Smethurst et al., 1986). SRWC's leaf traits will influence cover-crop cultivation (and the magnitude of fixed-N input) throughout the rotation by influencing understory light availability during winter. N inputs from cover crop could meet 100% of N requirements of loblolly pine and sweetgum for the first 4 and 6 years of stand development, respectively. Afterwards. N-inputs from cover crops will be limited by canopy closure (~3-5 years) in evergreen and would account for 27 ± 9% of rotationlength N demand, while N-inputs from cover crops will continue through the entire rotation for deciduous woody crop species and could be responsible for ~72 ± 24% of total N demand; no leaching, volatilization, competition, or immobilization was considered for simplicity.
Our model suggests that N inputs from cover crop could meet 100% of N requirements of loblolly pine and sweetgum for the first 4 and 6 years of stand development, respectively ( Figure 3). Cover crop N-fixation would continue to reduce fertilizer requirements throughout a sweetgum rotation, whereas N inputs would be limited to the first 3-5 years of the loblolly pine rotation because canopy closure would inhibit cultivation. Thereby, cover crop N-fixation could supply ~72 ± 24% and 27 ± 9% of N-requirements throughout a 10-year harvest rotation in sweetgum and loblolly pine, respectively (Figure 3). These figures correspond to peak tree N-demand, that is, growing under optimal conditions. Side-by-side investigations indicate that N uptake from unfertilized trees can be ~ one-half of fertilized trees (Albaugh et al., 2008;Aubrey et al., 2012). Therefore, by increasing N availability in the system, it is likely that integrated SRWC will promote SRWC N uptake and outperform low input systems. This assumption corroborates observations from available literature (Table 1), of which almost all integrated SRWC systems performed better than no input controls. At the same time, it may be cautious to stress that our estimates may be overly optimistic as no N losses (leaching, volatilization, competition, or immobilization) were considered, that is, 100% of the fixed N would be then uptaken by the SRWC. Assuming a N acquisition by the SRWC ranging from 50% to 100%, the N fixation supply is reduced to 54 ± 21% and 20 ± 8% of sweetgum and loblolly pine N demand, respectively. We are unaware of documentation of these processes in integrated SRWC systems. Nonetheless, it may be plausible to assume that the significance of N losses or competition may be of lesser extent than current representations of N cycling in intensively managed forests (Ferreira et al., 2021;Griffiths et al., 2017) given (1) the potentially available N is of somewhat slower cycling (e.g., decomposition and mineralization processes) than mineral N, which reduces potential leaching and volatilization and (2) cover cropping SRWC inter-rows may buffer competition (Teasdale, 1996).
A few more notes on our modeling are warranted. The estimated N fixation is based on the N found in cover crop biomass and assumes cover crops are being cultivated only as soil amendment (i.e., the N incorporated in their biomass becomes available for SRWC uptake as senescence and decomposition occurs). Thus, if cover crops are planted as an additional biomass feedstock, figures may be reduced. On the other hand, potential soil N enrichment by cover crop N-fixation has not been accounted for, so N inputs could be higher than our estimates. Our numbers considered total annual N uptake, but not nutrient cycling from litterfall or fine-root turnover. Nevertheless, these assumptions were the same for all systems and external N input requirements may be reduced proportionally in a full biogeochemical cycle. Considering sequential rotation scenarios, external N input requirements are substantially reduced and may be virtually null in the integrated SRWC if the intensity of harvesting is reduced (e.g., stem-only harvest), particularly for deciduous hardwoods, which can have up to 50% of their total N in belowground pools (Ferreira et al., 2023). And finally, we emphasize that while we were careful to use potential peak-N tree demand and simulate N-fixation through a robust approach, our data are limited by two tree species in a single environment and few N-fixation observations and assumptions and may not be generalized. Thus, both tree N demand and N-fixation by the cover crop may vary when considering other environments or species; however, rates may not hold proportional.
We finalize our discussion bringing the attention for the potential of boosting N fixation and inputs in SRWC using crop rotations of non-N-fixing and N-fixing trees intercropped with N-fixing winter cover crops. The long rotations of traditional forestry (i.e., >25 years) precluded the exploration of potential benefits of crop rotation. However, the relatively short duration of SRWC makes thinking about rotation woody crops feasible and provides an opportunity to mix species temporally (i.e., crop rotation). Evidence shows that rotating crops reduces soil N depletion as well as provides an overall enhanced soil health and improved protection from pests and diseases, which in the long-term can increase production security and might even enhance current attainable productivity levels (Oldfield et al., 2019;Renard & Tilman, 2019). As with crop rotation in agricultural systems (Zhao et al., 2022), it may be beneficial to follow a SRWC rotation of a high yielding, high nutrient demanding species with a rotation of an N-fixing species to help replenish soil nutrients and maintain soil health. Currently, leguminous trees (e.g., Robinia pseudoacacia, Acacia mangium, Leucaena leucephala) exhibit lower yield grown under similar conditions compared with non-fixing fast-growing species such as Eucalyptus and Pinus (Biswas et al., 2011;Bouillet et al., 2013;Nouvellon et al., 2012). However, they are successfully used to reclaim degraded areas and improve site quality with small investments (e.g., fertilizers) while also reasonably yielding biomass. Improving genetic material and designing tailored silvicultural practices for tree legumes has potential to increase productivity (Biswas et al., 2011), which would expand landowner and market acceptance for those species. We thus consider a SRWC rotation scheme of alternating N-fixing and non-fixing trees between consecutive rotations (mixing species in time) along with intercropping with N-fixing cover crop species (mixing species in space) as a promising system to attain reasonable productivity with minimal environmentally costly inputs (Text S2). Such scheme has potential to attain zero external N demand while sustaining adequate N supply across rotations ( Figure S1); however it needs empirical evidence, knowledge, and technology development to come to fruition.

| FINAL REMARKS
We explored the potential of integrating N-fixing winter cover crops into SRWC systems to offer greater levels of ecosystem functioning, that is, maximizing SRWC productivity while minimizing external inputs by increasing whole-system N cycling potential. While this concept is not new, the approach has been commonly overlooked in discussions for alternatives for ecological forestry intensification (Gómez-González et al., 2022). We demonstrated the fundamental basis by which integrating N-fixing winter cover crops into SRWC could provide a spatial and temporal complementarity in resource utilization ensuring stand productivity and minimizing inorganic N additions. The potential spatial and temporal complementarity makes this integrated SRWC a promising understudied system that can be added to the toolbox of ways SRWCs can be sustainably intensified. Nonetheless, many research gaps were identified. Few studies addressed how species functional traits can influence intercropping success. Straightforward research needs are identifying the best N-fixing cover crop and SRWC mixtures locally or regionally and reducing the uncertainty in potential N-fixation rates. The development of N budgets is key for a sustainable N management of any production system (Zhang et al., 2021). Also, there is a need to develop site-specific management practices for integrated SRWC (e.g., tree planting density and cover crop seeding rate or alley width, soil preparation, and other amendments) to alleviate competition and maximize both productivity and species synergy. In addition, more research is needed to demonstrate the potential direct and indirect species complementarity in resource use (e.g., nutrient and hydraulic uplifts, direct nutrient transfer from intermingling roots, and common mycorrhizal networks). The intensity of management adopted and maintained in SRWC makes this integrated alternative an ideal system to study direct and indirect interactions between distinct niche plants. Finally, research is needed to evaluate the financial considerations and unintended consequences (e.g., attraction of potentially SRWC damaging mammals; Albertsson et al., 2016), and to inform policy to promote adoption of these systems.
While central, the implications of using N-fixing cover crops are not simply a replacement of fertilization. The integration of cover cropping and N-fixing species into production systems is known to result in overall healthier soils (Farmaha et al., 2022;Koudahe et al., 2022), which is currently not straightforward to value but has potential implications for long-term forest productivity and resilience. Benefits include increased biological activity and nutrient cycling (Rachid et al., 2013;Rachid et al., 2015;Tiemann et al., 2015), reduced erosion and improved soil structural stability (Blanco-Canqui et al., 2015), and soil C accrual (Kaye et al., 2000;Mayer et al., 2020;Resh et al., 2002). While the mechanisms driving some of these changes may be similar as with N fertilization in monocultures (e.g., increased biomass driving more C inputs to the soil, and thus soil C accretion; Johnson & Curtis, 2001;Mayer et al., 2020), comparison of adjacent studies indicates that soil C and biological activity are generally higher in more diverse systems than in N-fertilized monocultures (Forrester et al., 2013;Kaye et al., 2000;Resh et al., 2002;Rifai et al., 2010). Most of these properties are relevant to wood production, but a comprehensive understanding of management effects on both soil health and forest productivity is still missing (Schoenholtz et al., 2000). Understanding the direct relationship between soil health indicators and SRWC productivity is critical to guide sustainable management practices in forestry and offers opportunity to push forest production and sustainability beyond current knowledge.

ACKNOWLEDGMENTS
This work was supported by the USDA National Institute of Food and Agriculture, Agriculture and Food Research Initiative McIntire Stennis project (1023985) and was based upon work supported by the U.S. Department of Energy to the University of Georgia Research Foundation (DE-EM0004391) and to the U.S. Forest Service Savannah River (DE-EM0003622). We thank Dr. Ivan Souza for kindly commenting on an earlier version of this manuscript, the two anonymous reviewers for valuable suggestions, and Art'n'Science Caparelli for the illustration of our conceptual figure.

CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.

DATA AVAILABILITY STATEMENT
Tree N uptake data are openly available in figshare at https://doi.org/10.6084/m9.figsh are.22138 085.v1. Other data that support the findings of this study were extracted from the literature and can be found in associated references.