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Plant roots spanning spatially disconnected areas of soil moisture can serve as conduits to redistribute moisture within the soil profile. Breazeale (1930) and Breazeale and Crider (1934) performed experiments investigating the ability of catclaw (Acacia gregii), date palm (Phoenix dactylifera), corn (Zea mays), and tomato (Lycopersicon esculentum Mil.) to grow roots into soil below the wilting point and then translocate moisture from disconnected wet soil into dry soil layers over a period of days to weeks in pot and field culture. Further studies by Breazeale and Crider (1934) with tomato plants identified the potential for this translocated moisture to help nearby wheat (Triticum aestivum) seedlings survive otherwise lethal levels of soil moisture stress in a pot-culture. Many years later, the phenomenon was studied in a natural system by Mooney et al. (1980) who found increased soil moisture overnight in the dry shallow soil under phreatophytic Prosopis tamarugo trees growing in the Atacama Desert and proposed that this moisture movement and subsequent release happened at night when the trees were not transpiring. Later Richards and Caldwell (1987) observed the phenomenon of overnight increase in water potential using thermocouple psychrometers in a natural field setting beneath sagebrush (Artemesia tridentata), which has deep tap roots. They coined the term “hydraulic lift,” [later termed “hydraulic redistribution (HR)” by Burgess et al. (1998)] to describe the process.

The stable and radioactive isotopes of hydrogen are extremely useful tools for tracking water movement in ecological studies (Rundel et al., 1989). Studies using natural abundance hydrogen isotopes (Dawson and Ehleringer, 1993), as well as deuterium (Caldwell and Richards, 1989), and tritium (Corak et al., 1987) enriched water, have been used to trace the path of HR water from deeper to shallower soils. HR has been identified across a variety of ecosystem types (Emerman and Dawson, 1996; Warren et al., 2007; Bleby et al., 2010). Hydrogen isotopes have been important tools in observing HR water transfer in natural environments between Acer saccharum trees and multiple nearby species, where the proportion of A. saccharum HR water used correlated linearly to the growth of nearby shallow-rooted species (Dawson and Ehleringer, 1993). Dawson and Pate (1996) continued this work measuring HR in several Australian ecosystems and identified how the dimorphic (i.e., deep and shallow) habit of tree roots in seasonally dry environments can lead to seasonally distinct patterns of water uptake from different elevations within the soil profile.

The presence of HR has been linked to numerous ecosystem processes beyond simple transfer from one plant to another. For example, in greenhouse conditions under severe water stress, Querejeta et al. (2003) showed that HR water can be transferred to mycorrhizal symbionts of oak trees. Furthermore, Cardon et al. (2013) provided evidence that HR promoted nitrogen mineralization and plant nitrogen uptake by Artemesia tridentata. Although HR has been suggested to provide a potential benefit to agroecosystems (Corak et al., 1987; Liste and White, 2008), the transfer of HR water from a deep-rooted woody species to an important food crop species as a mechanism to buffer against a severe, in-season drought that would otherwise cause crop-failure has not been conclusively shown to the best of the authors' knowledge.

To address whether HR can increase crop production, we investigated the existence of this pathway with the native woody shrub, Guiera senegalensis J.F. Gmel, which often grows in the agricultural fields of farmers throughout the Sahel (Figures 1A,C). The Sahel is a transitional climate zone between the arid Sahara desert in the North and the Savannah to the South, where one-third of the 20.2 million inhabitants face food and economic insecurity (United Nations, 2014). The majority population is directly employed in agriculture, which is 97% rain-fed on low-fertility soils where external inputs are not affordable for subsistence farmers (Calzadilla et al., 2013). Furthermore, unsustainable land management such as discontinuation of fallowing, cropping intensification, overgrazing (United Nations, 2014) and scavenging for fuel wood have contributed to severe degradation and no increase in crop yield over the last 50 years (FAO, 2015). Another important agronomic challenge for the Sahel is low and unpredictable rainfall and in-season drought periods, which lead to low yield or crop failure (Figure 1B) (Terrasson et al., 2009). Therefore, water is the most important factor that farmers must use effectively to optimize crop productivity.

Previously, our team documented benefits to soils and food production when crops are inter-planted with the native woody shrub, G. senegalensis, which is found throughout the Sahel between the 500 and 800 mm isohyets (Figure 1C) (Le Houerou, 1980). This is an optimized system where the density of shrubs is elevated (~1500 shrubs ha⁻¹ or 3 to 4 times greater than the natural density) and coppiced shrub residues are annually returned to the soil. Studies conducted in experimental plots and farmers' fields in the past 15 years concluded that shrubs improve soil quality (Dossa et al., 2009; Diedhiou-Sall et al., 2013) via root and litter inputs that build soil structure, organic matter concentrations, nutrient availability, and water storage (Dossa et al., 2009, 2010).

G. senegalensis has tap roots that that extend beyond 3 m which enable retrieval of water from the subsoil during the dry season and drought periods of the cropping season when the upper 50 cm of soil becomes very dry (Gaze et al., 1998; Wezel and Böcker, 1999; Kizito et al., 2006). Because of this adaptation to the dry climate, G. senegalensis uses minimal amounts of water during the critical early phases of crop germination and growth and does not compete with crops for water (Kizito et al., 2007). Our previous studies (Kizito et al., 2012) also documented elevated soil moisture and diurnal soil water potential fluctuations beneath shrub canopies during drought periods as evidence G. senegalensis performs upward HR of water via roots from wet subsoil to dry surface soil (Caldwell and Richards, 1989; Neumann and Cardon, 2012) due to a soil water potential gradient.

In the coarse soils typically found in the region, water potential ranges widely from near-saturation (−0.01 MPa) to permanent wilting point (−1.50 MPa) with only a 7% change in volumetric water content (Bogie et al., 2018). Rapid drying of the surface soils through crop and shrub evapotranspiration can lead to large gradients in moisture content and water potential, creating the necessary conditions for HR. We hypothesized that HR water could buffer crops against in-season periods of water stress. Furthermore, an 11 year study on P. reticulatum (Bright et al., 2017) and a 4 year study on G. senegalensis (Dossa et al., 2012) showed that crops near shrubs had significantly higher crop yield per mm of rainfall, even in dry years, over non-shrub treatments. In our earlier work, only indirect evidence that HR water from shrubs is available to adjacent crops was documented. To accept or refute this hypothesis, an irrigated field experiment in the dry season was conducted in tandem with a deuterium tracer study during a simulated drought to determine if HR water was taken up by adjacent millet plants.

Millet was grown with fully sufficient levels of water for plant growth until early flowering and then water was withheld for 41 days until harvest. Soil water potential rapidly declined during the drought period with soil at the 20 cm depth reaching −2.0 MPa after 12 days, which was drier than the 60 cm and 100 cm depths (Figure 2).

Soil moisture measured at three distances from the closest shrub remained stable until mid-May, when the near-shrub moisture began a steep decline of ~10 mm over the course of a week (Figure S2). Profile soil moisture declined continuously in all subplots after irrigation was stopped on May 9. Declines in the crop+shrub “far” moisture and crop only treatments were less pronounced than the crop+shrub “near” treatments in crop+shrub subplots A and B, in crop+shrub subplot C the declines crop+shrub “far” and “near” were similar (Figure S2). In an earlier study, Kizito et al. (2012) found elevated near-surface moisture in crop+shrub subplots during the early part of the season as compared to crop only treatments. They also found there was movement of moisture upwards toward the shrub and laterally away from the shrub at night indicating G. senegalensis was performing HR during times of extreme drying in the surface soil.

There was little observable difference in moisture content in the upper 1 m of the soil profile between treatments in the early season which does not resemble the pattern observed by Kizito et al. (2007). These authors showed that in the early part of the growing season, crop+shrub treatments had an elevated moisture content of up to 0.03 m³ m⁻³ in the upper 1.10 m of the profile, integrated over neutron probe measurements at 0.10 m depth increments. The differences Kizito et al. observed may be due to differences in infiltration rates between plots or due to the existence of hydraulic redistribution in the shrub root zone (Kizito et al., 2007). Kizito et al. found higher saturated infiltration rates near the shrub which they attribute to higher macroporosity. Saturated infiltration would then lead to deeper moisture penetration and higher total profile moisture content beneath the shrubs following a large rainfall event. However, the rate of water infiltration by the drip emitters in this study was low enough that there was no ponded infiltration, therefore the role of macropores in infiltration was likely diminished compared to many of the precipitation events during the rain-fed growing season. Smaller, more frequent low-intensity events (such as drip irrigation) could lead to similar infiltration rates across treatments in this study and a more uniform profile moisture depth when compared between treatments. Additionally, the shrub density in this irrigation and tracer study was ~7 times as high as the native density in the field studied by Kizito et al. (2007), so the shrub water uptake was likely higher in this study which could diminish any shrub-mediated increases to profile moisture content due to infiltration or hydraulic redistribution.

Not surprisingly because of the very low soil moisture levels during the drought, millet without shrubs resulted in crop failure with virtually no panicle production and very low biomass (Figure 3 and Figure S3). Although millet is one of the staple crops in the region, biomass yields in fields without the presence of shrubs or additional fertilizer can routinely fall below 200 kg ha⁻¹. Sometimes crops produce no grain at all as they did in 2007 (Dossa et al., 2012) and 2013 at this site (M. Bright, personal communication).

However, it was surprising to find that millet in the presence of shrubs, despite experiencing soil water potential well below the wilting point at −3.0 MPa, was not only able to keep growing but actually produced a harvestable product. The millet in crop+shrub subplots produced almost 10 times the biomass and over seven times more panicles than the crop only treatment (Student's t-statistic 15.8, −4.7 for panicle mass and biomass, respectively, P < 0.05 for both) (Figure 3 and Figure S3). These results are consistent with Dossa et al. (2012) who found millet planted near G. senegalensis maintained significantly higher crop yields during low rainfall years.

This raises a fundamental question on how shrubs keep a crop growing when soil moisture is so low. Somehow this shrub is making water available to the crop and apparently very efficiently.

One mechanism for assisting millet could be the higher soil organic matter that has accumulated in the optimized shrub-intercropping system (Dossa et al., 2009, 2010, 2012; Diedhiou-Sall et al., 2013). In particular, Dossa et al. (2012) found that the particulate organic matter fraction (undecomposed plant litter) was significantly higher when soils were under an optimized system which was highly correlated with crop yields. The improved soil quality due to annual incorporation of coppiced shrub biomass and root turnover for 9 years prior to our current study would be expected to increase aggregation and porosity to store water (Carminati, 2012) and make it more readily available for crops. However, the extremely low water potential after the drought was imposed (well below the wilting point), would suggest that improved soil quality and water holding capacity cannot fully account for the positive growth response of millet in the presence of G. senegalensis.

This leaves the second, and reasonably, the most important mechanism, HR, as a plausible explanation for the phenomenal ability of G. senegalensis to keep millet growing through the severe in-season drought that was imposed. Indeed, all sensors recorded the typical signature of HR with an increase of water potential from sunset until sunrise. During this imposed drought period the largest overnight increase in water potential was 0.57 MPa over a 12-h period at 20 cm depth on May 25 (Figure 2). However, these diurnal shifts in water potential do not confirm that hydraulically lifted water by this shrub is actually taken up by adjacent crops.

To address this question the ²H-tracer experiment was done toward the end of the drought period. Figure 4 shows temporal shift of ²H-tracer in shrub tissue increasing in the first 24 h and then declining; whereas millet tissue adjacent to the shrub started showing the signal from 12 h after the tracer was applied. In crop+shrub subplot A and B above-background δ²H was observed in millet with peak δ²H values at 36 and 84 h after tracer application, respectively. In crop+shrub subplot C, above background δ²H was first observed 36 h after ²H tracer application in millet, which was also the time at which it reached its maximum value.

The strongest ²H signal in millet was in crop+shrub subplots A and B, which exhibited above-background δ²H at all but one sampling time after the introduction of the tracer on the evening of May 24 (Figure 4). In subplot C of the crop+shrub treatment the tracer was significantly above background levels (δ²H = –18‰) once at the “near” sampling site and twice at the “far” (> 3 m from labeled shrub, but still within shrub subplot near other shrubs) sampling site. The most positive (enriched) δ²H values in the millet in crop+shrub subplots A, B, and C were 335, 208, and −17‰ respectively. The δ²H values in the shrub stems in crop+shrub subplot A showed the greatest enrichment (δ²H = ~5000‰ increase) and an above-background signal in all but one sampling after tracer introduction (Figure 4). These results confirm that G. senegalensis can move water from deep in the profile by HR to surface soil that can be taken up by nearby millet plants.

Although it was not possible to quantify the exact amount of water transferred, the crop yields in crop+shrub vs. crop only subplots indicate the amount of water transferred is important. Sap flow data measured in the crop+shrub subplot of plot C confirms that the millet plants near the shrubs were, in fact, transpiring even after 17 days without added irrigation water, and the moisture content was considerably higher in crop+shrub subplot A where sap flow was measured than in plot C where the water potential was measured (Figures S2, S4).

Despite the fact that the soil moisture nearest to the shrubs was the lowest, the plants closest to the shrubs were 267% taller than the crop only plants, and 142% taller than the millet 1 m away from the shrub (Figure S5). Surprisingly, the largest plants in the field were in the driest conditions, in the presence of shrub roots Thus one can only conclude HR water must have kept millet growing, and done so very efficiently. Additionally, the quantity of water transferred during HR is very small, but the water potential, which can vary widely with a small amount of moisture change, determines the limit to nitrification (Stark and Firestone, 1995) and plant water uptake (Richards and Weaver, 1943). Using an indirect water balance method, Kizito et al. (2012) estimated the quantity of HR to be 35–47 mm annually, which accounts for 8–10% of the mean annual precipitation of 450 mm. With the cessation of irrigation there was no available water to the millet other than that stored in the rooting zone, or HR water.

Water enriched in, ²H was not strongly detected in shrub stems in two of three crop+shrub subplots even though it was applied directly to one of the shrub's tap roots. Guiera senegalensis has an extensive vertical and horizontal rooting system and many aboveground stems (Kizito et al., 2006). It is therefore conceivable that some of the sampled shrub stems were not directly connected to the roots that received the isotopic tracer thus the absence of a ²H signal in the shrubs at some time steps is not unexpected (Figure 4 and Figure S6).

This observation does not, however, explain why all HR water was not completely reabsorbed by the shrubs themselves. One explanation is that a plant may not use its own HR water, as deep water may be easier to take up in wetter conditions of the subsoil due to potential differences in hydraulic conductivity between surface and tap roots (Mcelrone et al., 1999). Alternatively, millet may be better adapted, through its high density of roots in the 0-1 m range, to exploit HR water than a woody species such as G. senegalensis (Brück et al., 2003).

Another mechanism that could contribute to efficient transfer of HR water from shrubs to crops is mycorrhizal hyphae connecting roots of two plant species (Egerton-Warburton et al., 2007). The strong HR signal in the soil water potential (Figure 2) demonstrates the release of moisture into the shallow soil depths, but does not rule out the possibility of a mycorrhizal transfer pathway between species.

We propose three mechanisms by which a relatively small volume of water in an environment of very high potential evaporation can contribute to improved crop performance. First, from soil water potential data (Figure 2) and other similar studies (Richards and Caldwell, 1987; Caldwell and Richards, 1989) HR is particularly strong during times of extreme drought and increases the longevity of shrub roots by maintaining contact between the root and the rhizosphere soil which, if broken, can lead to cavitation and loss of root function (Horton and Hart, 1998). It has been shown that soil with root exudates (extracellular polymers) can retain a greater amount of water than bulk soil under drying conditions (Carminati and Vetterlein, 2013). This mechanism could help prevent drought-induced cavitation of shrub roots when soil water potential is near the wilting point. The same logic could be extended to include the maintenance of root health of the millet roots when they are intermingled with shrub roots. During the rainy season in nearby farmers' fields, the authors observed millet roots growing closely around G. senegalensis roots, supporting the assertion that HR water is involved in the maintenance and functioning of the roots of both species.

Second, in many arid and semi-arid regions shrubs have been shown to create resource “islands” with greater carbon and nutrient contents than in surrounding soils (Dossa et al., 2009, 2012; Hernandez et al., 2015; Diakhate et al., 2016). Improved crop yields near these “islands” are associated with higher microbial activity and abundance in the rhizosphere (Diedhiou-Sall et al., 2013; Debenport et al., 2015). While shrubs provide water during drought stress, they also create higher quality soils and harbor beneficial microbes (Debenport et al., 2015) that improve crop nutrient and health status, all of which can contribute to drought resistance. Indeed, some microbes have the ability to assist plants during water stress (Timmusk and Wagner, 1999).

Third, quantity of water used during grain filling is extremely important to grain yields (Vadez et al., 2013b). Vadez et al. (2013a) showed in a pot study that for every additional kg of moisture used by millet during grain filling, yield can be increased by 4.7 and 3.5 g plant⁻¹. Scaling this result up, at a planting density of 10,000 plants ha⁻¹ this could result in a yield increase of 35–47 kg ha⁻¹ mm⁻¹ additional moisture that plants receive during grain filling. This shows that even a relatively small quantity of moisture, such as that provided by HR from G. senegalensis to millet, can have a strong impact on crop yield.

In areas with less than 800 mm of mean annual precipitation, trees in agroforestry systems will outcompete crops for limited water resources, unless the deep rooted species can access groundwater (Van Noordwijk and Ong, 1999). Additionally, pearl millet yields along a transect in Senegal show 800 mm of annual precipitation as a threshold below which yields begin to decline (Figure 1B) In the presence of shrubs in this study, however, millet continued to grow and was more productive than millet grown alone, and the mean annual rainfall at the site is 450 mm (Kizito et al., 2006). This observation demonstrated that G. senegalensis does not compete with crops for soil water in times of water scarcity.

These results show that shrubs can assist crops through within-season drought periods. This is a particularly critical growth period because at the mid-to-late crop stage as it is no longer possible to replant. Many arid and semi-arid regions including the West African Sahel will experience an increase in drought severity and a decrease in soil moisture with climate change (Dai, 2013), HR from associated shrubs in croplands will increase in their importance for providing adequate food for the population.

Feeding the large and rapidly growing populations in the socioeconomically and environmentally precarious region of the Sahel is a major challenge. For the Sahel, where the majority rural populations depend on drought-tolerant pearl millet, groundnut, sorghum (Sorghum bicolor), and cowpea (Vigna unguiculata), shrub intercropping is a logical and locally available solution for increasing yields and stabilizing productivity in high and low rainfall years.

The findings provide confirmation of an unprecedented agricultural system that performs “bioirrigation” by shrubs, literally transferring hydraulically redistributed water to adjacent crops. Using soil moisture sensors and stable isotope tracing this study provided direct evidence for HR to be the key mechanism of G. senegalensis to sustain millet during extreme water stress. However, further in-depth research is needed to understand how such small amounts of hydraulically lifted water can be so efficiently transferred from shrubs to crops. Also, HR research is needed for Piliostigma reticulatum the other dominant shrub species found in farmers' fields throughout the Sahel.

These results have implications for all semi-arid regions where in-season drought is a common occurrence with increasingly erratic climate patterns owing to global climate change. For highly mechanized semi-arid agroecosystems in other parts of the world, engineered intercropped systems for rain-fed crops should be investigated as a novel approach to manage water for crops to buffer against drought. For the Sahel, optimized shrub intercropping with elevated planting density and the return of coppiced biomass to soils, offers an ecological and locally available solution to buffer against droughts and remediate degraded soils that subsistence farmers can readily utilize.

The data in Figures 1–4 are either the output from the raw data in this manuscript will be made available in a timely manner to any qualified researcher who requests it.

ID, TG, RD, and NB developed the original idea for the study. NB, TG, RD, RB, ID, MF, and MC Planned the experiment. NB and RB managed lab and field data collection. MF helped with laboratory experimental design and data collection. NB and TG performed data analysis, wrote manuscript, and managed the manuscript editing process. NB, RB, TG, RD, MF, and MC edited manuscript.