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Folia Geobotanica

, Volume 52, Issue 3–4, pp 345–352 | Cite as

Initial evidence for simultaneous, bi-directional sap flow in roots of interconnected aspen ramets (Populus tremuloides)

  • Mario Bretfeld
  • Scott B. Franklin
  • Robert M. Hubbard
Article

Abstract

Approximately 40% of the world’s currently known plant species exhibit some form of clonality. Yet, little is known about the extent of clonal integration (e.g. the sharing and translocation of resources among ramets), especially in woody species. Aspen (Populus tremuloides Michx.), a widespread clonal tree species of high ecological value and conservation concern, is an excellent model species to study clonal integration. We used sap flow sensors on the root system of aspen located in the Fraser Experimental Forest (Colorado) to quantify water fluxes, assess directionality of flow and assess responses to a root severing experiment. Our results indicate simultaneous, bi-directional flow in roots with 3–4 times more flow in one direction. Flow towards ramets that were subjected to severing of roots (except the measured root) decreased considerably, and an increase in root flow ‘down the line’ towards connected, untreated ramets suggests complex interactions within the root system. Our results are intriguing and provide a first account of directionality of flow and distribution of water in an interconnected root system of a clonal tree species. Based on these findings, we formulate a set of further research questions and discuss methodology and experiments to test them.

Keywords

clonal integration parent root system Populus tremuloides resource sharing root hydrology sap flow 

Introduction

It has been estimated that approximately 40% of the world’s currently known plant species exhibit some form of clonality (Tiffney and Niklas 1986), i.e. the ability of a genetic individual (genet) to produce genetically identical modules (ramets) that have the potential to survive as independent organisms (Stuefer et al. 2002). Clonal integration – the sharing and reallocation of water, nutrients, and carbon resources within clonal plants (Stuefer et al. 2002) – has become the focus of research worldwide (Sudová and Vosátka 2008; Luo et al. 2015), including its effect on competitive ability (Wang et al. 2008), invasiveness (Otfinowski and Kenkel 2008), and growth and resource allocation under heterogeneous conditions (Baker and van Bavel 1986; Pennings and Callaway 2000; Wang et al. 2004; Touchette et al. 2013; Chen et al. 2015; Saunders and Pezeshki 2015). However, knowledge is based predominantly on herbaceous species and applicability to woody species remains largely unknown.

We used sap flow sensors to investigate clonal integration in an interconnected root system of a clonal tree species (quaking aspen; Populus tremuloides Michx.). Aspen is the most widely distributed tree species in North America (Little 1971) and considered to be a keystone species in most of its range (Bartos 2001; Buck and St. Clair 2012), making it an ideal model tree species for studies on clonal integration. Furthermore, because successful sucker establishment and survival of aspen ramets are strongly dependent on resources from the parent root system for at least 25 years (Zahner and DeByle 1965), an improved understanding of clonal integration in this species can aid in conservation efforts.

Studies on clonal integration in aspen have shown that integration has a relatively low impact on competitive ability of aspen invading into prairie in Saskatchewan, Canada (Peltzer 2002), but that grafting and resulting functional connections between ramets within the same clone have a positive effect on growth in very old clones in north-central Alberta, Canada (DesRochers and Lieffers 2001). Roots of top-killed aspen stems remain alive for several years, presumably supported by photoassimilates from neighboring healthy ramets (DesRochers and Lieffers 2001; Peltzer 2002) and carbon storage in the parent root system enhances aspens’ ability to resprout following stand-replacing disturbances in Colorado (Shepperd and Smith 1993). Root water flow in one-year-old aspen has been shown to be positively correlated with total leaf area, shoot length, and new root growth (Wan et al. 1999), and water and solutes are translocated through the xylem of functional root connections over a distance up to 16.9 m (Tew et al. 1969). While aspen have been shown to physiologically interact through the parent root system and trigger compensatory photosynthesis in connected ramets (Baret and DesRochers 2011), induction of defense traits following simulated herbivory were transmitted through airborne volatiles rather than root connections (Jelínková et al. 2012). Studies on balsam poplar (Populus balsamifera L.), a close relative of aspen, showed that connected ramets are more resilient to insect outbreaks and drought compared to non-connected ramets (Adonsou et al. 2016a; Adonsou et al. 2016b).

Although studies utilizing sap flow measurements on roots of woody species are common (e.g. Howard et al. 1996; Lott et al. 1996; Green et al. 1997; Burgess et al. 1998; Burgess and Bleby 2006; Bleby et al. 2010; Naithani et al. 2012; David et al. 2013), most studies focused on non-clonal species. To date, no studies known to the authors have experimentally investigated clonal integration using sap flow sensors in an interconnected root system. We tested for directionality of sap flow between aspen ramets observationally and experimentally (root severing) and predicted that (1) flow is bi-directional in roots of aspen depending on demand of immediate and ‘down the line’ ramets, and that (2) flow increases towards ramets with severed roots. Based on our initial observations and results, we outline and propose future research directions.

Material and methods

All experiments were performed at approximately 2,700 m elevation in the Fraser Experimental Forest (FEF) in Colorado between 2009 and 2013 (Table 1 ). There had been a pulse of aspen regeneration following a mountain pine beetle infestation in 2002 followed by mechanical removal of dead conifers in 2007 (Collins et al. 2011). Sites were selected based on ramet sizes to accommodate size limitations of sensors and were only gently sloped (Table 1 ). We assigned single-letter labels to stems while root labels reflect connections to neighboring stems, if known (Fig.  1 ). A summary of the stem and root diameters, along with leaf areas for trees used in this study is given in Table 2 .
Table 1

Overview of site locations, elevation and sensor setups for each sampling year.

Year

GPS

Elevation

# Root sensors

# Stem sensors

Sampling period

2009

105°52′42.95″ W

39°54′46.02″ N

2,735 m

4

2

June 25 – August 14

2011

105°51′33.59″ W

39°55′44.39″ N

2,730 m

5

0

May 31 – September 20

2013

105°51′49.20″ W

39°55′45.60″ N

2,706 m

1

2

September 4 – September 17

Fig. 1

Illustration of root/ramet relationships in a complex, connected aspen root system. Black arrows indicate assumed primary direction of flow. Dots and lines indicate stems and roots, respectively, with larger sizes indicating older stems/roots. Labels denote stems (e.g. a) and roots (e.g. root of unknown origin connecting to ramet a – Ra; root connecting ramet a and b – Ra/b). Illustration A shows directionality and location of sap flow sensors (light grey arrows) and root severing treatment (black circle with diagonal line) for the 2011 experiment. Root severing in the 2013 experiment occurred in a similar location but no sensors were installed on Rbc and Ra. Instead, stem flow was measured for ramets a and b. Illustration B shows the potential complexity of an aspen root system with stem ages not conforming to root ages: Stem x resprouted from the root between a and y and is therefore younger than both a and y. It is also younger than c, despite originating from an older root.

Table 2

Overview of aspen stem and root diameters (in cm) and leaf area (in cm2) for each sampling year. Note that for each year new ramets were chosen.

  

Independent

Pair

Ramet a

Ramet b

Ramet a

Ramet b

2009

Stem

2.8

2.5

  
 

Root 1

2.9

3.2

  
 

Root 2

3.2

2.5

  
 

Leaf Area [cm2]

5,280

5,880

  

2011

Stem

n/a

 

3.8

2.5

 

Root 1

n/a

 

1.8

1.9*

 

Root 2

2.4/2.7#

 

1.9*

2

 

Leaf Area [cm2]

n/a

 

8,795

5,271

2013

Stem

  

2.4

3

 

Root 1

  

n/a

2.5*

 

Root 2

  

2.5*

n/a

 

Leaf Area [cm2]

  

5,000

6,627

* same root, i.e. connecting ramets a and b.

# two sensors on same root at different locations.

Sap flow measurements were performed using non-invasive Dynamax™ (Houston, TX) Dynagage™ stem-heat balance sensors (models SGB13-WS, SGB19-WS, and SGB25-WS). Data were logged using two Dynamax™ Flow4-DL data loggers. Root sensors were installed measuring either towards or away from a ramet, stem sensors measured upward flow. Sensors were compared to gravimetric measurements using aspen cuttings (max. 3.2 cm in diameter) under laboratory conditions. Results indicate that sensors are accurate (R 2 = 0.86) but lack precision, with an overestimation of flow (between 50–75 g·hr−1) compared to gravimetric measurements.

In 2009, two independent ramets were instrumented on two roots and the stem of each ramet (Table 2 ). To test for bi-directional flow, root sensors were turned around on July 22 (ramet a) and August 7 (ramet b) because roots were not long enough to accommodate two sensors in opposing directions at the same time. Leaf area was estimated using ‘LAFORE’ software (Carl-von-Ossietzky University, Oldenburg, Germany) by scanning five sample leaves and extrapolating using the estimated total number of leaves, based on counts.

In 2011, data were collected starting on May 31 (before bud break) until September 20 (dormancy), resulting in a total of 106 days (excluding 7 days due to missing data). Bi-directional flow was measured using two sensors installed in opposing direction on the same root of an independent ramet. A root severing treatment was applied to a pair of connected ramets (a and b) at the end of the 2011 growing season (Table 2 ). Sensors were installed on the connecting root measuring from ramet a to ramet b, on a root measuring towards ramet a, and on a root measuring away from ramet b (Fig.  1a ). Severing included all roots of ramet b, with only the connection to ramet a left intact (Fig.  1a ). Branch diameters and associated branch leaf area were determined using a LI-3100C (LiCor Biosciences, Lincoln, NE). The resulting regression (y = −1,503.7 + 2,710.2x; R 2 = 0.5) was used to estimate total leaf area for other ramets based on branch diameter measurements.

In 2013, sensors were installed on each stem and the connecting root between a pair of ramets (a and b), measuring flow from ramet a to ramet b (Table 2 ). A root severing treatment similar to 2011 was performed on September 7 on ramet b. Leaf area per ramet was estimated using the regression formula from 2011.

Results

Results from 2009 show that flow rates in roots and stems of both instrumented ramets were similar with clear diurnal patterns (Fig.  2 ). Stem sap flow decreased considerably around 15:00, while root flow remained high until around 19:00. Turning root sensors around to measure flow in opposing directions suggests that flow is bi-directional and shows a clear indication of a dominant flow direction, with approximately four-fold higher daily average flow compared to the opposite direction (Fig.  3 ). Results from 2011 show similar patterns, with simultaneous bi-directional flow that is three to four times higher in one direction (Fig.  4 ). Root flow in both directions started increasing rapidly around 8:00 and remained high until 20:00. Daily root flow increased with leaf expansion from June to July, decreased with progressing leaf senescence early in September, and was highest from late June to mid-August (Online Resource 1 ).
Fig. 2

Diurnal sap flow for two independent aspen ramets (a and b) from July 4–11, 2009. Lines are half-hourly average flow rates; bars indicate standard deviations for each half-hourly measurement. Root sap flow was measured towards the stems of ramets a and b.

Fig. 3

Bi-directional root sap flow for two independent aspen ramets (a and b) over three days in 2009. Measurements were taken every 30 minutes on two roots per ramet. a – Flow towards the ramets, measured from June 7–9. b – Flow away from the ramets, measured from August 8–11.

Fig. 4

Simultaneously measured, bi-directional root sap flow. Measurements were taken every 30 minutes on the same root of one aspen ramet from June 15 to September 19, 2011. a – Diurnal root sap flow of flow towards (inward) and away from (outward) the aspen ramet. Lines are hourly average flow rates; error bars indicate standard deviations for each hourly measurement. b – Time series of root sap flow towards (inward) and away from (outward) the aspen ramet.

Results from the 2011 root severing of ramet b show a changed flow pattern from ramet a to ramet b, with a notable peak around 9 a.m. (Fig.  5a ). Average daily flow volume from ramet a to ramet b and through the severed root of ramet b decreased considerably, while root flow towards ramet a roughly doubled (Fig.  5b ). Results from the 2013 root severing experiment show changed daily flow volumes and patterns following root severing of ramet b, especially in the connecting root between ramet a and ramet b (Online Resource 2 ). Root flow from ramet a to ramet b decreased by 95%, and upward stem flow decreased by 41% and 50% in ramet a and ramet b, respectively.
Fig. 5

Results of root severing treatment on September 3 2011. Data are from August 20 to September 2 (before) and from September 6–15 (after). a – Diurnal root sap flow of flow from ramet a to ramet b. Lines are hourly average flow rates; error bars indicate standard deviations for each hourly measurement. b – Average daily sap flow volume for all measured roots. Error bars indicate standard deviations of daily flow volumes. Flow was measured ‘one-way’ through the pair of aspen ramets: root flow towards ramet a, root flow from ramet a to ramet b, and root flow away from ramet b.

Discussion

Our results provide a first account for simultaneous, bi-directional flow in an interconnected root system of a clonal tree. Although several studies have demonstrated the ability of roots to transport soil water from wet to dry horizons, these studies only provide data of temporary flow reversals driven by gradients in soil water potential (e.g. Richards and Caldwell 1987; Burgess et al. 1998; Caldwell et al. 1998; Burgess et al. 2001), foliar uptake of fog water (Eller et al. 2013), or rain events (Naithani et al. 2012). Scholz et al. (2016) provide a comprehensive review of the concept of hydraulic redistribution and possible facilitation between redistributing species and their neighbors. Clonal integration provides a more direct vector to share resources and our results show that aspen roots serve as a two-way street, with higher flow in one direction (hereafter ‘primary flow’) compared to the opposing direction (hereafter ‘secondary flow’).

The difference in average and peak flow rates in the connecting roots between 2011 and 2013 can likely be attributed to installation of sensors in the opposite or the same direction as primary flow, respectively. Leaf area and stem diameter data hint towards ramet size/age as a potential driver for primary flow direction from larger to smaller ramets (Table 2 ). However, ramet and root ages can be disparate in the root system of aspen, complicating an assessment of such relationships (Fig.  1b ). Considerably more research is required to elucidate if there is truly a primary flow direction throughout a clone, and if such primary flow direction can be explained by allometric relationships or environmental conditions, such as local soil moisture or irradiance. Because heat transfer of water within a vessel moving in one direction is influenced by water in neighboring vessels moving in the opposite direction, we also solicit research to optimize measurement techniques. Heat-ratio and Granier-type sensors require less space and considerably increase sample size when large enough roots are accessible, and stable isotope tracers or dye can be applied to confirm bi-directional flow.

Changes in daily flow pattern and volume in the connecting root following the severing treatment suggest that single ramet-to-ramet connections do not sufficiently compensate for the loss of other roots. Lott et al. (1996) performed a root severing experiment on silky oak (Grevillea robusta A. Cunn. ex R. Br.) and found no significant increase in root flow, indicating that the remaining root was functioning near maximum capacity. The decrease of root flow observed in our study suggest that ramets under stress may be separated from the clone as a compartmentalization response to prevent the spread of pathogens or limit adverse effects of injury (Shigo 1984; Smith 2006). Severing also affected root flow ‘down the line’, as indicated by the increase in root flow towards the untreated ramet a (Fig.  5b ), providing a potential trade-off to the benefits of sharing water and nutrients.

Phenomena such as ‘Sudden Aspen Decline’, the regional, widespread mortality of aspen, have been linked to hydraulic failure (Anderegg et al. 2012; Anderegg et al. 2015). Understanding the role of water distribution in the root system and thresholds for ramet survival following stress will further improve predictive power of models of aspen dynamics under a changing climate. Locally induced drought and light stress are other possible treatments to study stress responses and possible compartmentalization thresholds. While we performed three shading experiments in 2011, results were conflicting and more rigorous testing is required, furthermore highlighting the necessity for additional research in this emerging field.

Notes

Acknowledgements

The authors thank the Fraser Experimental Forest for facilitating access to experimental sites and permitting the use of the on-site laboratory. For field and laboratory assistance we thank Daniel P. Beverly and Michone Duffy. For helpful comments on the manuscript, we thank James P. Doerner, Mitchell E. McGlaughlin, Jitka Klimešová, Katherine L. Gross, and two anonymous reviewers. Funding for this research was provided by an in-house University of Northern Colorado Provost Grant.

Supplementary material

12224_2017_9285_MOESM1_ESM.pdf (125 kb)
ESM 1 (PDF 124 kb)

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Copyright information

© Institute of Botany, Academy of Sciences of the Czech Republic 2017

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of Northern ColoradoGreeleyUSA
  2. 2.USDA Forest ServiceRocky Mountain Research StationFort CollinsUSA
  3. 3.Smithsonian Tropical Research InstituteAncónRepública de Panamá

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