Leave No “Dead” Tree Behind: How Neighboring Root Systems Sustain A Seemingly Dead Tree Stump

Trees are commonly regarded as distinct entities, but the roots of many species fuse to form natural root grafts allowing the exchange of water, carbon, mineral nutrients, and microorganisms between individuals. Exploiting the phenomenon of leafless (photosynthetically inactive) tree remnants being kept alive by conspecifics, we show tight physiological coupling of a living kauri (Agathis australis) stump to conspecific neighbors. The trunk remnant displayed greatly reduced, inverted daily sap flow patterns compared with intact kauri trees. Its stem water potential showed strong diel variation with minima during daytime and maxima at night, coinciding with peak and minimal sap flow rates in neighbors, respectively. Sudden atmospherically driven changes in water relations in adjacent kauri trees were very rapidly and inversely mirrored in the living stump’s water status. Such intimate hydrological coupling suggests a “communal physiology” among (conspecific) trees with far-reaching implications for our understanding of forest functioning, particularly under water shortage.

Graphical Abstract

Subject Areas

• Biological Sciences
• Plant Biology
• Botany
• Plant Physiology

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Introduction

Aboveground most trees appear as individuals, but they are often intricately connected belowground through mycorrhizal networks and also through natural root grafts, facilitating the exchange of carbon, nitrogen, and other mineral nutrients (Bormann, 1966, Stone and Stone, 1975, Tarroux, 2011). While mycorrhiza-mediated nutrient transfer between trees has attracted considerable interest in recent decades (Brownlee et al., 1983, Vogt, 1991, Courty et al., 2010, Klein et al., 2016), the role of natural root grafts has received little attention over the past half century, despite some 150 woody angio- and gymnosperm species (Beddie, 1941, Bormann, 1966) reported to show the phenomenon globally, and accounts for more than 60% grafted individuals within a population (Graham and Bormann, 1966, Basnet et al., 1993). It is important to distinguish between three fundamentally different types of root connections: those within an individual (self-grafting, Baret, 2011), which are common to most, possibly all trees (Graham and Bormann, 1966); those between genetically different individuals of the same species (intraspecific grafting, Fraser et al., 2006); and those between different species (interspecific grafting, La Rue, 1934, Beddie, 1941). While self-grafting is little surprising and its adaptive value is easily explained (e.g., increased stability and transport of water and nutrients within individuals), intra- and interspecific grafting raise important questions as to their evolutionary advantage (Callaway and Mahall, 2007, Keeley, 1988). Several hypotheses trying to explain this trait have been put forth, ranging from evolutionary neutrality, increased resistance to windthrow, improved water and nutrient exploitation, all the way to a parasitic nature of the phenomenon (Loehle and Jones, 1990, Lev-Yadun, 2011). However, there is no consensus, and natural root grafting may have evolved several times for different reasons. The question as to the adaptive value of intraspecific root grafting becomes more challenging yet when one of the grafted individuals is a leafless tree stump, a phenomenon that was first reported in 1833 for European silver fir (Abies alba) and several times since (Dutrochet, 1833, Eis, 1972, Graham and Bormann, 1966), including in the species we investigate here (Ecroyd, 1982). A “living stump” without foliage, provided an intact root system, needs to receive at least carbohydrates from neighboring trees. Assuming that the grafting was in place before the tree became a leafless stump, it is far from obvious what causes conspecifics to continue the provisioning of carbohydrates to a photosynthetically inactive individual. It has been argued that the host tree may benefit from mechanical stability through enhanced soil anchorage (Rigg and Harrar, 1931, Keeley, 1988) or through improved access to soil resources via the extended root system provided by the stump (Bormann, 1966), but no increased growth was observed in trees that were artificially grafted to living stumps (Holmsgaard and Scharff, 1963). Because carbohydrates are transported in solution, and because the transpirational pull is absent in living stumps, the question of what physiological processes orchestrate such intriguing symbioses is eminent, yet has not been addressed to date.

Results and Discussion

In living, leafless stumps, the lack of foliar transpiration implies a cyclic flow of water requiring an extensive rearrangement of water transport pathways, which prompted us to examine vertical and horizontal sap flow patterns simultaneously (Figure 1). The amplitude of the normalized diel sap flow velocity (hereafter simply referred to as sap flow) in the trunk remnant was about two times larger in the vertical compared with the horizontal direction (Figures 2C and 2D). The stump’s vertical sap flow maxima were more than five times smaller relative to the surrounding intact conspecifics (Figures 2A and 2B), whereas its stem water potential exhibited a pronounced diel cycle ranging from values close to 0 MPa at night to −3.7 MPa around midday (Figure 2E). Interestingly, the stump’s sap flow and stem water potential were both inversely related to the water flux seen in the tall, surrounding kauri trees (Figures 2A–2E and inset). On sunny days, when neighboring trees were transpiring vigorously, little or no water movement could be detected in the living stump, neither vertically nor horizontally, but its water potential dropped to minimal values (Figures 2E and 2H). At night, however, when transpiration of the surrounding kauri trees was minimal, complete relaxation of the stump’s water potential occurred, and its sap flow reached maximum values (Figures 2C and 2I). In the absence of transpiration in the tree stump, this phenomenon can only be explained by osmotically driven water movement or root pressure (Sperry et al., 1987) (Figures 2H and 2I). During daytime, sudden changes in atmospheric vapor pressure deficit resulting in instantaneous sap flow reductions in adjacent kauri trees were rapidly mirrored by an equivalent, but opposite, pattern in sap flow and immediate relaxation of stem water potential in the living trunk remnant, suggesting intimate hydraulic coupling between the host tree and the stump (see arrows in Figures 2A–2E). Further strong evidence for this tight hydraulic connection came to light under conditions of low evaporative demand. On two consecutive days (April 12 and 13) with either very low vapor pressure deficit or exceedingly high precipitation (ca. 80 mm on April 13), sap flow in the surrounding intact trees dropped to minimal values, whereas in the trunk remnant it stayed continuously high (Figure 2). The strong reduction in transpiration of neighboring trees translated into higher water potentials and increased water availability in the soil and within the joint root system, allowing for sustained daytime sap flow rates in the living stump. The CO₂ release rates from the bark of the living stump and neighboring kauri trees were similar (1–1.5 μmol m⁻² s⁻¹), with almost no diel variation in both host and stump, confirming metabolic activity and thus living tissue in the trunk remnant (Figure 3).

The above evidence for substantial xylem flow in a living stump raises substantial questions on the anatomical, physiological, and evolutionary mechanisms that enable this process, particularly when assuming that the graft was in place before the loss of photosynthetically active tissues of one of the connected trees (Lanner, 1961). With the loss of the foliage, transpiration, and basipetal assimilate transport, the provisioning of living tissues must change considerably. This supply process must be highly efficient, as the here reported stem respiration rates suggest similar metabolic activity between the host and the living stump. The measurable horizontal and substantial vertical sap flow rates suggest that a circular, rather than unidirectional, sap flow pattern may evolve rapidly following the loss of autotrophic tissues, which may explain the 5-fold lower acropetal sap flow rates in the stump compared with the host trees. If no anatomical adaptations take place, the horizontal sap flow presumably occurs via existing vascular rays. The observed sap flow patterns and their associated (likely osmotic) regulation seem to be largely decoupled from the atmosphere, but instead highly dependent on the host trees’ physiology. This stands in contrast to the way plants normally function, with both xylem and phloem transport ultimately driven by the highly negative water potential of the atmosphere, which is coupled to the plants via stomata.Our results strongly suggest intraspecific root grafting in kauri and contribute to our understanding of the evolutionary advantage of root grafts, particularly those between trees and leafless stumps. Intact kauri trees grafted to a closely intertwined root network may adopt the root system of a connected tree that has lost its crown, thereby extending their rooting space and at the same time allowing trunk remnants to persist over long periods of time. The extra resource costs linked to the maintenance of the aboveground part of living trunk remnants may be minor compared with those associated with the suddenly enlarged root system (Figure 2H). Our findings suggest that the adaptive advantage of the hydraulic coupling may be a lot more important than previously assumed, and may indeed be a means of compensating for the carbohydrates the trunk remnant receives. On the downside, our study also corroborates the notion of facilitated pathogen transmission through root grafts (Graham and Bormann, 1966, Epstein, 1978), which is especially alarming because kauri has recently been classified as threatened owing to the rapid spread of kauri dieback disease, caused by the fungus-like soilborne pathogen Phytophthora agathidicida (De Lange et al., 2013).In conclusion, although observations of living tree stumps have been reported widely (Lanner, 1961), our results on the physiological interactions with host trees indicate that such symbioses may be much more complex than previously assumed: by physiologically exploiting “downtimes” of transpiring trees during the night or rainy days with high water potentials in the root network (Figure 2I), living stumps seem to act partially autonomously, strategically tapping into resources rather than simply becoming part of the neighboring trees’ extended root networks. Although a few studies have suggested that carbon and possibly nutrients are exchanged universally in forests (Simard et al., 1997, Klein et al., 2016), our results indicate that such a “wood-wide web” (Sen, 2000) may in fact extend to the hydraulic system of trees, with far-reaching consequences for drought-related impacts (Allen et al., 2015) and pathogen transfer (Epstein, 1978).

 Limitations of the Study

Clearly, only having observed a single living kauri tree stump prevents us from drawing broader conclusions. Although we personally have not yet seen a second occurrence of a living stump belonging to this iconic New Zealand species, from talking to local foresters, we know that this phenomenon has apparently been noticed in the past and the formation of natural root grafts in kauri was already suspected 80 years ago (Beddie, 1941). However, because the reported results are of physiological rather than ecological nature, and through highly consistent temporal replication and reoccurrence of very similar patterns measured with different sensors, we trust our data. Another shortcoming is the lack of direct evidence for root grafting, which can only be achieved with isotope labeling experiments, involving tremendous logistic effort (Klein et al., 2016). In our case, the host tree crowns would need to be labeled with ¹³C, for example; other options may be phloem labeling or destructive root exposure. However, this would only confirm the stump’s supply with carbohydrates by host trees. To provide further evidence of hydraulic coupling, similar measurements as presented here, possibly adding root sap flow measurements, would be required. Belowground carbon trading among trees has been shown in the past, but if our admittedly limited data on hydraulic coupling among trees can be confirmed, we might have to revise our general understanding of forest ecosystems as communal “superorganisms.”