Forest Ecology and Management 409 (2018) 749–756

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Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Precision subsurface drip irrigation increases yield while sustaining water- T

use efficiency in Mediterranean poplar bioenergy plantations
⁎
Pierluigi Parisa, Giovanni Di Matteob, , Massimo Tarchic, Luca Tosia, Luciano Spaccinoa,
Marco Lauteria
a
Consiglio Nazionale delle Ricerche, Istituto di Biologia Agroambientale e Forestale (CNR-IBAF), Porano, Italy
b
Council for Agricultural Research and Economics (CREA), Research Centre for Agriculture and Environment, Rome, Italy
c
W2 Agency, Osimo, Ancona, Italy

A R T I C L E I N F O A B S T R A C T

Keywords: Bioenergy production in poplar Short Rotation Coppice plantations (SRC) is strongly limited in drought prone
Drought areas due to the high crop water requirement. Appropriate scheduling of subsurface drip irrigation (SDI) could
Irrigation scheduling be a practice for ensuring adequate biomass production with reduced water inputs while maintaining high
Precision agriculture water-use efficiency. We tested SDI in a commercial SRC cultivated with the hybrid poplar clone Monviso under
Soil moisture
Mediterranean environmental conditions. We applied two irrigation treatments during the summer season, i.e. a
Carbon stable isotopes
control irrigation treatment with an average amount of 115 mm (CI) and a double irrigation treatment for an
average amount of 239 mm (DI) over two growing seasons of the second triennial rotation. We analyzed tree
growth, yield, shoot diameter increments (PDI) and carbon isotope composition (δ13C) in both litterfall and tree-
rings. We also measured soil moisture at 10, 20, 30, 40, 60 and 100 cm soil depths to explore more efficient
irrigation scheduling. The results showed that CI and DI recovered 23–49 and 43–90% of the April-September
precipitation deficit over the two growing seasons, respectively. We observed higher yield increments in DI
compared to CI, with mean yields of 11.4 and 20.4 Mg ha−1 for CI and DI respectively. DI significantly affected
biomass quality (biomass allocated to shoots with greater dimensions); however, stem moisture and shoot basal
density did not significantly change after the irrigation treatments. δ13C in tree-rings showed non-significant
differences after CI and DI applications for two growing seasons. Congruently, the analysis of litterfall δ13C did
not show significant differences comparing the two irrigation regimes. Thus, the isotopic analyses indicate a
constancy of intrinsic water-use efficiency (iWUE), irrespective of the watering regime. We found significant
positive linear relationships (R2 from 0.89 to 0.96) between PDI and soil moisture at 30 and 40 cm soil depths for
both CI and DI when compared to the rest of the monitored soil layers. We suggest, therefore, the monitoring of
soil moisture at 30–40 cm as a reference for scheduling irrigation practices during the growing season. In
conclusion, DI significantly increased the overall plantation yield while sustaining the same iWUE observed in
the deficit irrigation regime (CI).

1. Introduction
Bioenergy feedstocks are widely recognized as valid alternatives to
fossil fuels in mitigating global climate change (IPCC, 2014).
In the European Union (EU) the share of renewable energies is ex-
pected to increase from 14% in 2010 to 20% in 2020 and up to 27% by
2030 (Mantau et al., 2010). Yet, by 2030, about 26 Million ha of
plantations dedicated to bioenergy productions will be required to meet
the EU bioenergetics needs. Bioenergy coppice plantations, managed
under short rotation cycles of 2–5 years and characterized by high
planting densities (i.e., up to 10,000 trees per ha) (SRC), have received
much attention worldwide due to their large biomass productivity for
bioenergy purposes (Morhart et al., 2014; Sixto et al., 2015).
Hybrid poplars are the most common species used in SRC (Zamora
et al., 2015) because of their high yield potential (i.e., up to 25 Mg dry
matter ha−1 year−1) (Paris et al., 2011), depending on site conditions,
cultivar choice and rotation cycle duration. However, under Medi-
terranean conditions, water availability represents the most limiting
factor affecting poplar yield due to its hydrophilic behavior, which
requires constant soil moisture throughout the growing season. There-
fore, it is essential to take into account irrigation practices to increase
poplar SRC yield.

⁎
Corresponding author at: Council for Agricultural Research and Economics (CREA), Research Centre for Agriculture and Environment, Via della Navicella 2-4, I-00184 Rome, Italy.
E-mail address: giovanni.dimatteo@crea.gov.it (G. Di Matteo).

https://doi.org/10.1016/j.foreco.2017.12.013
Received 22 August 2017; Received in revised form 5 December 2017; Accepted 6 December 2017
Available online 22 December 2017
0378-1127/ © 2017 Elsevier B.V. All rights reserved.
P. Paris et al.
Poplar water requirement under SRC conditions is particularly re-
levant due to high evapotranspiration rates (Fischer et al., 2013). Yet,
Fisher et al. (2013) noticed a mean annual crop coefficient (Kc) value of
0.91, ranging between 0.42 and 1.51, depending on site conditions. By
studying the poplar SRC water requirement in a lysimetric trial under
Mediterranean conditions, Guidi et al. (2008a) found that Kc value
peaked at 3, with daily evapotranspiration (ET0) values ranging be-
tween 5 and 10 mm.
European SRC plantations cover an estimated area of
50,000–70,000 ha, with about 12,000 ha in Sweden, and 10,000 ha in
Italy and Hungary, respectively (Facciotto et al., 2015). In Italy, most
poplar SRC plantations are cultivated across northern continental areas
as these are particularly suitable due to their climatic and edaphic
conditions (Paris et al., 2011). Conversely, southern Mediterranean
areas are particularly exposed to prolonged drought periods (four
months or more without adequate rainfall). These site conditions
strongly limit poplar SRC cultivation, mainly due to water shortages (Di
Matteo et al., 2012). Efficient irrigation systems are, therefore, urgently
required to ensure the cultivation of bioenergy plantations (Navarro
et al., 2015).
Poplar SRC in Europe is mostly irrigated via gravity-fed and
sprinkler systems. Drip irrigation systems are sometimes used, mainly
in research plots and for evaluating the performance of additional tree
species to be cultivated under SRC conditions (Bianconi et al., 2011;
Cañellas et al., 2012; Perez et al., 2014; Pérez-Cruzado et al., 2014).
Subsurface drip irrigation (SDI) is an advanced irrigation system that
minimizes the water losses by evapotranspiration from soil and weeds
and by soil drainage below the root system. SDI has been successfully
tested on several crops under Mediterranean conditions (Ayars et al.,
1999, 2015). It seems particularly suitable for perennial woody crops
since its high installation costs could be amortized within multi-annual
plans. SDI could be a very promising irrigation system for poplars under
SRC conditions and its application could optimize the overall plantation
water-use efficiency, with positive economic and environmental bene-
fits. To the best of our knowledge, no study has reported the use of SDI
in poplar SRC in drought prone areas. Therefore, we carried out a pilot
experiment in a Mediterranean poplar SRC in central Italy by applying
the SDI system with different irrigation levels, according to the opera-
tional guidelines required by commercial plantations.
SDI can result in an increase of the agronomic water-use efficiency
(WUE), the ratio of crop yield to total water consumption, when com-
pared with other irrigation systems (Najafi and Tabatabaei, 2007). In-
trinsic water-use efficiency (iWUE) is, at the leaf level, the ratio be-
tween net CO2 assimilation rate (A) and stomatal conductance to water
vapor (gs). In poplar, the leaf carbon isotope composition (δ13C) has
been often used as an indicator of iWUE along the period of accumu-
lation of leaf structural carbon (Ripullone et al., 2003, 2004), while
δ13C in the tree-rings reflects long-term tree physiological responses, in
interaction with phenological, environmental and anthropogenic fac-
tors (McCarrol and Loader, 2006; Di Matteo et al., 2014, 2017). An
isotope composition (e.g., δ13C) is the deviation from the unit of the
ratio of the isotope ratio of a sample to that of the standard. Whenever
the δ13C value of atmospheric CO2 can be assumed as constant among
the treatments, the value of carbon isotope composition of photo-
assimilates is controlled by stomatal conductance and photosynthetic
capacity, which determine the intercellular to atmospheric CO2 partial
pressure ratio (pi/pa). Since iWUE is negatively related to pi/pa, carbon
stable isotope analysis is a reliable proxy of iWUE itself (Farquhar et al.,
1989). For instance, iWUE seasonal fluctuations in poplar were asso-
ciated to variations in soil water availability, which potentially affect
the photosynthetic operational point via the pi/pa value (Broeckx et al.,
2014).
The tree iWUE might be enhanced by scheduling proper irrigation
practices according to the actual crop water consumption. Thus, mon-
itoring the physiological responses in relation to phenology, soil
moisture availability and atmospheric evapotranspiration demand,
750
Forest Ecology and Management 409 (2018) 749–756
would suggest the best management for a sustainable plant carbon and
water economy. Three methods can be used to accomplish this target,
based on the monitoring of: i) soil moisture, ii) tree water status via leaf
water potential or crop water stress indices by remote sensing (Bellvert
et al., 2013; Gago et al., 2015), and iii) soil water budget according to
FAO recommendations (Allen et al., 1998). The most promising drip
irrigation system in terms of irrigation efficiency considers soil moisture
monitoring by using sensors positioned at different soil depths (Soulis
et al., 2015). A key-issue in this method is the choice of representative
crop rooting volume points in order to place the soil probes properly
and, consequently, to measure the crop soil moisture as accurately as
possible.
However, little is known about these experimental practices, as no
study has been conducted to clarify these issues, especially in poplar
SRC managed with SDI systems. This is because few experiments have
considered soil moisture probes at different soil depths to investigate
the relationships between tree growth and soil moisture profile
(Intrigliolo and Castel, 2006).
The aims of this study are: i) to determine the effects of SDI regimes
applied during the summer season on yield and growth in poplar SRC,
under Mediterranean conditions; ii) to estimate poplar iWUE responses
to SDI regimes via δ13C analysis in litterfall and tree-rings; iii) to
quantify the effect of SDI system on soil moisture at different soil
depths; iv) to examine the relationships between tree growth and soil
moisture at different soil depths, in order to identify the soil layers
where moisture content significantly affects tree growth.
2. Materials and methods
2.1. Site descriptions
The experiment was carried out in central Italy, at the Risiere lo-
cality, in the municipality of Viterbo (42°22′48′′ N; 12°01′45″ E, ele-
vation 204 m a.s.l.). The main land-use surrounding the study area is
arable agriculture, the main crops being rain-fed wheat, alfalfa and
clover. Secondary crops are irrigated corn and vegetables.
The climate is typically Mediterranean (i.e., dry summer-subtropical
climate, type Csa, Köppen climate) with dry summers and cool and wet
winters. Mean annual temperature and annual total precipitation are
13.25 °C and 736 mm, respectively. The coldest month is January
(mean temperature: 5.6 °C), and the hottest month is August (mean
temperature: 22.8 °C). The precipitation pattern is bimodal, i.e. it peaks
in autumn (263 mm), followed by wet and rainy late winters and early
springs (almost 175 mm in each season), and dry summers (121 mm)
(30 years average data, 1971–2000, for the city of Viterbo. Source:
Italian Air Force-Meteorological Service). In order to schedule the ir-
rigation treatment during the experiment, we monitored the site pre-
cipitation patterns by using meteorological data from a meteorological
station located near the experimental plantation (Table 1). Summer
precipitation (i.e., June, July and August) was 119, 12 and 115 mm for
2011, 2012 and 2013, respectively. The year 2012, therefore, was drier
than the average.
The soil originates from limestone volcanic deposits which char-
acterize the three horizontal layers, with a clay loam texture and a
significant percentage of gravel, up to 25% in the deepest layer, and a
low water holding capacity of around 15% (Table 2).
2.2. Plant material and plantation management
Experimental plots are part of a 40 ha poplar commercial plantation
managed under SRC conditions (Table 3). The tested poplar clone is
“Monviso” [(P. X generosa Henry) X P. nigra L.], which is registered in
the Italian Registry of Forestry Clones for biomass production and re-
corded as having a very high tolerance to Poplar rust. We planted the
stem cuttings mechanically at 2.5 × 0.66 m spacing with an overall
plantation density of 6,060 cuttings ha−1. In the establishment year, i.e.
P. Paris et al. Forest Ecology and Management 409 (2018) 749–756

Table 1 Table 3
Summary of precipitation and precipitation deficit during the study period (2011–2013) Plantation management practices and dates concerning the irrigation treatments carried
and mean precipitation values for the last seven years (2004–2010). out at the experimental site.

Precipitation (mm) Precipitation-ET0 (mm) Plantation establishment date March 2008

Period (year) Poplar clone investigated Monviso
Period (month) Planting spacing and density 2.5 × 0.66 m (6,060 trees ha−1)
Sprinkler irrigation date June-August 2008 (R1; S1)
2011 2012 2013 2004–10 2011 2012 2013 Establishment of subsurface drip Winter 2008 (R1; S2)
(average) irrigation
Subsurface drip irrigation June-August 2009 and 2010 (R1; S2-3)
April 31.9 56.6 50.7 64.4 −23 10 −4 application dates
May 20.3 53.6 81 70.3 −67 −21 11 First harvest of the plantation December 2010 (R1; S3)
June 51.1 6.7 29.4 55.3 −67 −125 −78 Second harvest December 2013 (R2; S3)
July 65.3 4.2 34.2 13.5 −61 −150 −111 Irrigation study period 2011–13 (R2; S1-3)
August 2.4 0.9 51.7 22.9 −138 −153 −89 Irrigation 2011 115 mm
September 72.7 65.7 37.4 73.4 −31 −23 −52
Irrigation regimes applied in Control irrigation Double irrigation
Total 243.7 187.7 284 300 −387 −462 −345
2012–13 (CI) (mm) (DI) (mm)
Irrigation 118.8 11.8 115.3 91.8 −138 −428 −278
Irrigation levels (R2-S2, 2012) 110 228
Period
Irrigation levels (R2-S3, 2013) 120 250
(June -
Irrigation average (2012–2013) 115 239
August)

first growing season (S1), overhead sprinkler irrigation was used from
early June to late August. We installed the SDI system during the winter
of 2008–2009. We placed the SDI tubing at 30 cm soil depth, with an
emitter spacing of 80 cm and an emitter flow of 2.2 L h−1. We carried
out agronomic practices during the two growing seasons in 2012 and
2013 (S2-3), over the first triennial rotation cycle (R1), in order to re-
move weed vegetation by applying 2–3 harrowings per year. R1 was
coppiced in December 2010. Concerning the second triennial rotation
cycle (i.e., R2, 2011-13), just one harrowing was applied during the
first growing season.
2.3. Irrigation experiment and experimental design
The study compares different irrigation treatments, which started in
late spring 2012 during R2. We irrigated the plantation in S2-3 by SDI
system during the summer season (from late June to late August). We
divided the experimental plantation into two sub-areas, each of them of
2,500 m2, i.e. 100 m length (along tree rows) and 25 m width (10 tree
rows). One sub-area received the standard irrigation regime according
to irrigation practices applied in commercial SRC by local farmers
(Control, CI 115 mm), whereas the second area received a double irri-
gation regime (Double Irrigation, DI 239 mm). In the study, the irri-
gation regime values refer to the mean values of the S2-3 (detailed
information were reported in Table 3). We established three experi-
mental plots per irrigation treatment, with plots arranged as a rando-
mized block design. Each plot consisted of 10 trees, with a surface of
16.5 m2. In considering the rainfall patterns and visual assessments of
tree water status, we decided to apply irrigation treatments every 3 or
7 days for DI and CI, respectively over the duration of the experiment.
2.4. Tree growth and above-ground biomass
We conducted growth and yield measurements during the second
and third growing season of the second triennial rotation cycle (i.e., R2-
S2-3). We measured tree growth within each plot by counting all living
shoot populations, and measuring their diameter at 1 m above soil level
(d) and total height (h). We then identified the thickest-shoot per stool
(TS) as the one with the largest diameter. The linear dimensions of TS
refers hereafter as diameter (D) and height (H). We determined stem
moisture, stem basal density and relationships between d and shoot dry
weight by performing a random sampling based on the diameter class
distribution of the shoot population (every 10 mm). We measured stem
moisture (SM) and shoot basic density (SD) by sampling woody discs at
1 m stem height, approximately 7–10 cm long, and collecting them
immediately after shoot cutting to get the fresh weight (Wf). We de-
termined woody disc fresh volume (Vf) via water displacement method
(Giordano, 1981). Stem samples were then oven-dried at 103 °C to get
the constant dry weight (Wd). We calculated SD and SM using the fol-
lowing equations: SD = Wd/Vf and SM = [(Wf−Wd)/Wf)] × 100.
We estimated the above-ground woody biomass (expressed as dry
matter) according to Pontailler et al. (1997), based on the allometric
relationship between the mean shoot dry weight (w) and d, as described
by the equation: w = b. dc, where b and c are empirical parameters. We
estimated b and c through a destructive sampling of ca. 25 shoots per
year and irrigation treatment. We calculated the mean shoot weight as
the total shoot-dry-weight per plot divided over the number of shoots.
Mean shoot weight of the thickest shoot (W) was calculated as above,
but restricting the sampling to TS population. We calculated the total
stool-weight-to-thickest-shoot ratio (TS in %) as the percentage ratio
between W and total shoot-dry-weight per stool.
2.5. Shoot diameter increment, litterfall dynamics and soil moisture
We selected six stools per plot to measure the shoot diameter in-
crement during R2-S3 and consequently identified the thickest shoot
per stool. We selected the stools as six consecutive stools along the
central tree row of each plot. Diameter growth (D) was, therefore,
measured every 15 days (from April to November) with a caliper
(precision 0.1 mm), by measuring two orthogonal sides of the stem at
1 m above the soil surface. We calculated the shoot diameter increment
(PDI) as the percentage ratio of D at time t over D at time t-1.
To measure soil moisture, we used the PR2/6 Soil Moisture Profile
Probe (HH2 Readout Unit, Delta-T device) which provides the soil
water content as volumetric water content (in %), at 10, 20, 30, 40, 60
and 100 cm soil depths. To use the probe effectively, six epoxy-

Table 2
Soil physical characteristics at the experimental site.

Depth (cm) Gravel (%) Sand (%) Silt (%) Clay (%) Soil classification Wilting point (%) Field capacity (%) Available water (%)

20–30 18.3 28 31 41 Clay loam 14.6 30.3 15.6

40–50 18.1 36 28 36 Clay loam 13.2 27.6 14.4
60–70 26.6 33 29 38 Clay loam 13.7 28.6 15

751
P. Paris et al.
fiberglass tubes (one per plot, located at the centre of the row of the
selected stools) were inserted into the soil by manual soil coring, paying
particular attention to fill the space between the soil pit and the ex-
ternal surfaces of the tube according to the original soil stratification.
We buried access tubes in the soil at the beginning of the growing
season (April 2013); this allowed us to record the soil moisture every
15 days, from mid-May 2013 to the end of November 2013. For each
observation, we collected three measurements by rotating the probe by
120° within the access tube.
In the same growing season, we installed two litter traps per plot by
using plastic baskets with a rectangular base of 40 × 60 cm. We col-
lected litterfall samples every 15 days. The samples were immediately
transported in the lab to be oven-dried at 45 °C to constant dry weight.
2.6. Carbon isotope analyses in tree rings and litterfall
We sampled eighteen trees per irrigation treatment during the
second harvest in December 2013 to analyze the carbon isotope com-
position (δ13C) in tree rings. We took stem disks at a height of 130 cm to
extract woody matter from tree rings over the three growing seasons.
The woody matter was extracted at the centre of each tree ring with a
magnetic core drilling machine. Twenty-five litterfall samples per irri-
gation treatment (collected during the third growing season, from July
26th to December 13th) were also analyzed for δ13C. The sampled
material was finely grounded and sub-samples of about 500 μg were
quantitatively burned in an Elemental analyser (NA 1500, Carlo Erba,
Milan). The produced CO2 was injected through helium continuous
flow into an isotope ratio mass spectrometer (CF-IRMS; ISOPRIME,
Elementar Analysensysteme GmbH, Germany). Isotope ratios of sam-
ples and of internal standards were measured to allow the calculation of
δ13C values, anchored to the reference scale of IAEA standard VPDB.
Based on δ13C values in tree-rings and litterfall, iWUE dynamics were
reconstructed on a time scale of three years and one growing season,
respectively.
2.7. Statistical analysis
We used analysis of variance (ANOVA) to evaluate the irrigation
treatment effects on growth, wood quality (i.e., stem moisture and
shoot basal density), yield (above-ground woody biomass and litterfall
mass) and δ13C in litterfall and tree-rings. This was carried out using a
randomized block design with irrigation and year treatments as the
fixed factor, and block as a random factor. We used ANOVA post hoc
Tukey’s test to detect significant differences between irrigation treat-
ment means. We used Pearson’s correlation between PDI and soil
moisture from 10 to 100 cm soil depth measured during the growing
season of 2013 (from June to August) to find significant relationships
under site conditions of high precipitation deficit and active stem
growth. Statistical tests were conducted using SigmaPlot 12.5 (Systat
Software, Inc.).
3. Results
3.1. Growth and yield
We did not find significant effects of the SDI treatments on growth
traits related to the average shoot (d, h and w) after three growing
seasons (Table 4). Conversely, irrigation treatments significantly in-
creased the dimensions (D and H) and weight (W) of the TS population
(p < .001; < .05; < .001, respectively). This was because, in DI, TS
dry weight values were almost twofold compared to CI, with 2.0 and
1.1 kg at the end of R2-S3, respectively. DI significantly increased TS
biomass allocation pattern (p < .05) in both growing seasons (e.g., in
the 2nd growing season, 63% of the stool biomass was allocated to TS
under DI, and 55% under CI) (Supplementary material, Table 1).
Above-ground woody biomass was significantly higher for DI
752
Forest Ecology and Management 409 (2018) 749–756
compared to CI in both years (p < .001), i.e. 10.565 versus
8.075 Mg ha−1 during 2012, and 20.416 versus 11.399 Mg ha−1 during
2013, respectively (Table 5). SM significantly differed by years
(p < .001), even if non-significant differences between irrigation
treatments were found (Tables 4 and 5). SD did not significantly change
by years and irrigation treatments. Litterfall mass significantly differed
by irrigation treatments (p < .01), with DI showed higher values
(3.7 Mg ha−1) compared to CI (2.5 Mg ha−1).
3.2. Shoot diameter increment and soil moisture
TS stem diameter trend showed higher values for DI compared to CI
(Fig. 1a). In May, at the beginning of measurements (DoY 135), there
was a difference of 4.5 mm between DI and CI, which became 9.9 mm at
the end of the year (DoY 347). DI significantly increased PDI as com-
pared to CI (Fig. 1a). Mean soil moisture values recorded between 10
and 100 cm soil depth were higher for DI compared to CI (Fig. 1c).
Litterfall mass in CI peaked almost 15 days before DI (Fig. 1c).
We found several significant relations between PDI and soil
moisture at different depths. In DI these relations were always sig-
nificant but at 10 and 100 cm soil depths (Supplementary material,
Table 2), determination coefficient (R2) ranging from 0.50 (10 cm soil
depth) to 0.99 (20 cm soil depth). CI showed significant regression
coefficients at 30, 40 and 100 cm soil depth, with R2 values ranging
from 0.91 to 0.99 at 30 and 100 cm soil depth, respectively. Con-
sidering the mean soil moisture value for the whole soil profile, re-
gression coefficients were significant for both CI and DI (R2=0.90 for CI
and R2 = 0.93 for DI).
3.3. δ13C in tree-rings and litterfall
There was no effect of irrigation treatments in tree-rings δ13C
(Fig. 2). Conversely, the treatment “year” significantly affected tree-
rings δ13C (p < .001). In fact, the value of 2011, the year before
starting the irrigation, showed significantly more negative values than
the following two years.
DI had poor effect on litterfall δ13C when compared to CI, with
significantly decreasing δ13C values only in the sampling of August the
12th (p < .05) (see Fig. 3).
4. Discussion
4.1. Effect of irrigation volumes on growth and yield
This study points out as the tuning of irrigation volumes by means of
SDI can sustain the poplar tree growth and plantation yield. Preliminary
experiments (Paris et al., 2011) showed reduced tree growth and sur-
vival under rainfed conditions. On its side, sprinkler irrigation, which is
most commonly used in poplar SRC, has been clearly demonstrated,
along 40 years of empirical experience in California, to be less bene-
ficial than drip irrigation (Taylor and Zimmerman, 2017). Therefore,
we compared two subsurface irrigation treatments (i.e., DI, 239 mm vs
CI, 115 mm) in order to verify their sustainability, with particular re-
ference to the efficient use of the water resource. The yield increment
under DI was particularly relevant at the end of the third growing
season, with values as high as 20 Mg ha−1 (i.e., 6.8 Mg ha−1 year−1).
Tree growth was higher under DI conditions because of the higher in-
crease in TS biomass, relatively to CI. Besides a larger productivity, the
growth of larger shoots could have important consequences on the
wood quality during the transformation processes from biomass to
bioenergy. In fact, a larger stem diameter of poplar shoots under SRC
conditions is associated to lower proportions of bark tissue (Guidi et al.,
2008b). This determines a lower ash production during the combustion
and a lower release of nitrogen and nitrous oxides (NOx and N2O) into
the atmosphere (Paris et al., 2015).
It is noteworthy that the efficiency of water application by means of
P. Paris et al. Forest Ecology and Management 409 (2018) 749–756

Table 4
ANOVA p-values observed for growth and yield traits after irrigation treatments over two growing seasons. d, h, and w are the stem diameter (1 m above soil level), total height and total
shoot weight of the average shoot, respectively. D, H, and W are the diameter, total height and total shoot weight of the thickest-shoot per stool; TS is biomass of the thickest-shoot per
stool percentage; SB is the above-ground woody biomass; LF is litterfall mass; SM is stem moisture; SD is shoot basal density.

Source of variation Degree of freedom Average shoot Thickest shoot Yield

d h w D H W %TS SB LF SM SD

Irrigation 1 0.486 0.136 0.116 < 0.001 0.002 < 0.001 0.004 < 0.001 0.019 0.876 0.801
Year 1 < 0.01 < 0.01 < 0.01 0.044 < 0.001 0.004 0.73 < 0.001 < 0.001 0.269
Irr. x Year 1 0.857 0.656 0.241 0.315 0.145 0.032 2.249 0.059 0.893 0.545

Table 5
Mean poplar yield, litterfall mass, stem moisture and shoot basal density values (standard
errors in parenthesis) after CI and DI applications, for two growing seasons. Within each
year row, values followed by ns, ** and *** are not significantly different and different at
p < .01 and p < .001, respectively according to ANOVA; na = not available.

Year Above-ground Litterfall mass Stem moisture Shoot basal density

woody biomass (dry matter, Mg (%) (Mg m−3)
(dry matter, Mg ha−1)
ha−1)

CI DI CI DI CI DI CI DI

2012 8.1 10.6 na na 56.5 56.3 0.36 0.36

(1.2) (2.0)*** (0.7) (0.5)ns (0.007) (0.008)ns
2013 11.4 20.4 2.5 3.7 52.1 52 0.36 0.37
(3.1) (4.5)*** (0.52) (0.35)** (0.7) (0.7)ns (0.007) (0.007)ns

SDI can be indirectly estimated using our data. Indeed, the precipitation
deficit (PD) ranged between 468 and 278 mm, respectively for 2012
and 2013, owing to the difference of precipitation between the second
and the third growing season (Table 1). By applying CI, we covered
about 23.5 and 49% of the PD in 2012 and 2013, respectively. By ap-
plying DI, the recovery of PD increased from 43 to 90% in 2012 and
2013, respectively. Indeed, the choice of the irrigation volumes in this
trial ranges in between the conditions typical of deficit irrigation and
those of the full replenishment of the canopy water demand (e.g.,
Lauteri et al., 2014).

4.2. Effect of the irrigation volumes on WUE

Water-use efficiency is a basic parameter that may provide in-

formation on plant acclimation ability and adaptability to environment
with contrasting water availability (Lauteri et al., 1997, 2004). Wa-
tering commonly affects important physiological traits such as stomatal
conductance (gs) and net photosynthetic CO2 assimilation rate (A),
especially during summer when water availability may become a lim-
iting factor to tree growth. WUE can be studied on different biological
scales, ranging from the physiological leaf level to the ecosystem and
agronomic levels. It is noteworthy that WUE at the leaf level is usually
higher than that at the whole plant level. In fact, the respiratory losses
of carbon and those of water from the heterotrophic tissues and organs
and from the autotrophic tissues at night, affect the final ratio of carbon
gain to water consumption in a certain crop. However, irrespective of Fig. 1. Year 2013. Variation in stem diameter of the thickest-shoot per stool, reported as
the biological scale of investigation, the leaf level WUE must be seen as absolute (D) and shoot diameter increment (PDI) (a); Rainfall and irrigation patterns (b);
a relevant driver of the whole agronomic performance (Flexas et al., (c) Mean litterfall and soil moisture (10–100 cm soil depth). Bars represent the standard
2010). Aside its spatial dimension, WUE reflects also important tem- error of the means. DoY = Day of Year.
poral features, which describe the dynamics of plant responses to daily,
seasonal and inter-annual variations of the plant by environment in- indicating the absence of long term effects of the watering regimes on
teractions. Thus, in the meanwhile stable isotope applications on fast iWUE (Fig. 2). It is also noteworthy that δ13C in tree-rings refers to
turn-over metabolites or leaf structural carbon may provide short or integrated physiological responses, which enclose the tree perfor-
medium-term information, the same applications on tree rings have mances of the year preceding the xylogenesis of the ring itself
seasonal or annual meaning (McCarrol and Loader, 2006). In this study, (Kozlowski, 1992). This reinforces the evidence of a null effect of the
we integrate the long term analysis of carbon stable isotopes on tree irrigation treatments on iWUE, along the entire three years cycle of the
rings with the medium-term one on the litterfall. Tree-rings δ13C SRC trial. Congruently, δ13C values analyzed on litterfall along the third
showed no statistical differences between CI and DI within each year,

753
P. Paris et al.
Fig. 2. Mean tree-rings δ13C variations in the period since 2011 to 2013. Note that the
irrigation treatments have been applied since 2012. CI and DI values are the averages of
each year. Bars indicate the standard error of the means. Yearly values with different
letters are significantly different according to Tukey’s Test (p < .05); ns = not sig-
nificant.
Fig. 3. Mean litterfall δ13C values for CI and DI during the year 2013. Bars indicate the
standard errors of the means.; * = significant difference per p < .05; ns = not sig-
nificant.
growing season do not show any significant variation between the ir-
rigation treatments, with the exception of the second litter harvest on
the 12th of August. In this latter case, the DI treatment appears asso-
ciated to a more negative δ13C value than CI. However, it should be
clear that the isotopic signature of the litterfall refers to the physiolo-
gical conditions at the time of the leaf expansion, when most of the
structural leaf carbon is fixed. Many causes could have determined the
significant diversity of the δ13C values of the litterfall on the 12th of
August. For instance, the leaves could have been developed by the re-
mobilization of carbon synthetized and stored by the plant during a
mild or irrigated period of the previous year. However, both the agro-
nomic and the biological significance of this result is fairly poor, given
that those leaves were likely developed in early spring, before the start
of the irrigation. On the other side, it is noteworthy that the biomass
weighed means of the litterfall δ13C yield, respectively for CI and DI,
the identical values of −26.7‰ and −26.6‰. Thus, on a seasonal time
scale, δ13C analyses on both litterfall and tree rings indicate the lack of
difference in iWUE between the two watering regimes. Scaling up from
the physiological to the agronomic dimension of water-use efficiency
provides further insights on the plantation performances. Indeed,
taking into account the total amounts of watering of 345 and 593 mm,
respectively in CI and DI for the three years of productive cycle, the
irrigation water-use efficiency yields very similar values of 3.30 and
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Forest Ecology and Management 409 (2018) 749–756
3.44 kg of dry matter m−3 of water, comparing CI and DI. Furthermore,
taking also into account the amount of 1703 mm of precipitation
available to the experimental plantations along the three years, the
global WUE varies from 0.56 to 0.89 kg of dry matter m−3 of water,
respectively for CI and DI. Finally, such rough calculations indicate that
the homeostatic performances observed at the physiological level
(constancy of iWUE between CI and DI) are reflected in a relevant sy-
nergic effect of DI on the global WUE at the agro-ecosystem scale. This
synergism is likely mediated by beneficial effects of reduced evapo-
transpiration fluxes, due to an enlarged boundary layer on the canopy
scale in the DI thesis.
4.3. Some possible solutions to improve the cultivation of SRC in
Mediterranean environments
Our results provide experimental evidences with agronomic re-
levance for wide areas of the Mediterranean Basin, which share similar
climatic characteristics and farming systems. The experimental site falls
fully within the Csa type of the Köppen climate classification. The Csa
subtropical-dry summer climate is one of the most represented in the
Mediterranean area, especially in its northernmost part (Kottek et al.,
2006). We believe, therefore, that the benefits of using SDI on poplar
SRC can be easily transferred to other similar agricultural and agro-
forestry land uses. Despite of the above-mentioned benefits in using SDI
in poplar SRC under Mediterranean conditions, the case study showed
two main limitations: the first regards the absolute value of yield; the
second is related to the limited time span of the experiment (2 years) in
comparison to the theoretical possible duration of a poplar SRC (around
15 years). The obtained yield of 6.8 Mg ha−1 year−1 for the studied
clone Monviso under DI is lower compared to the yield of the same clone
grown under non-irrigated but fertile alluvial soils of northern, con-
tinental Italy (i.e., 13–21 Mg ha−1 year−1; Paris et al., 2011). We
should note that 10 Mg ha−1 year−1 represents the break-even point to
get financial profitability of poplar SRC in Italy (Manzone et al., 2009).
Three solutions could help to improve the yield under the site condi-
tions of our experiment: (i) using alternative species to poplar, more
resistant to drought; (ii) choosing the right poplar clone; (iii) scheduling
the irrigation more efficiently.
There are several alternative species to poplar for SRC in Italy and,
in general, for Mediterranean conditions. Black locust (Robinia pseu-
doacacia L.) is a relatively drought resistant species (Mantovani et al.,
2014). It produces reasonably under marginal conditions. It needs very
limited cultural inputs for yields ranging between 5 and 10 Mg ha−1
year−1 (Paris personal communication). Unfortunately, black locust use
is strongly limited because of its invasiveness. In fact, it is listed among
the alien species (Benesperi et al., 2012) although recent findings de-
monstrated that its invasiveness can be easily controlled (Crosti et al.,
2016). Eucalypts (Eucalyptus spp.) have extensively been used in Med-
iterranean countries, mostly in SRF (Short Rotation Forestry) planta-
tions and, to a lesser extent, in SRC. However, the low frost resistance of
the available planting material (Mughini et al., 2014) limits the diffu-
sion of Eucalypts for bioenergy purposes. Siberian elm (Ulmus pumilia
L.) is a drought and frost resistant species for inner Mediterranean
areas. It was particularly investigated in Spain (Perez et al., 2015).
Finally, Italian alder (Alnus cordata (Loisel.) Desf.) could be an inter-
esting fast-growing, drought resistant, nitrogen fixing species for bioe-
nergy purposes. However, currently, the investigations on this species
are rather limited (Lauteri et al., 2006; Scartazza et al., 2012).
Despite the above-described range of tree species, clones of hybrid
poplar are the only available planting material for Italian farmers in-
terested in establishing SRC. Thus, for Mediterranean areas, the choice
of drought tolerant poplar clones is crucial. Successively to the setup of
our experiment, several studies demonstrated that Monviso clone is
poorly adapted to the Mediterranean conditions of central Italy, when
compared to other poplar clones (Di Matteo et al., 2015, 2012). Here,
the Monviso yield was 5.72 Mg ha−1 year−1 versus 8.74 Mg ha−1
P. Paris et al.
year−1 of the clone AF2, under growing conditions of R9S3 (i.e., roots
aged nine and stem aged three). Neva is another modern poplar clone
showing yield and physiological characteristics particularly promising
for Mediterranean conditions (Navarro et al., 2014).
Finally, appropriate irrigation scheduling is a third option for in-
creasing the yield of poplar under limited water availability. Selecting
poplar clones in two dry sites in New Mexico and Oregon (USA), with
approximately 240 mm of annual precipitation, O’Neil et al. (2010)
used the irrigation scheduling based on Kc, in one site, and soil
moisture monitoring in the second site. Particularly, after three years,
the best clone showed yields ranging between 12 and 20 Mg ha−1
year−1, in the first and second site respectively. In the second site, soil
water status was measured with a tensiometer at 20 cm soil depth. Our
results showed strong and significant relationships between soil
moisture at 30 and 40 cm soil depths and shoot diameter increments.
We suggest therefore positioning soil moisture sensors in between 30
and 40 cm soil depth in order to schedule efficient irrigation practices.
4.4. Constraints to the application of SDI system in SRC
Long-term (25 years) farm observations on the applicability of SDI
in perennial woody crops revealed several problems, including root
strangulation of drip lines, fine root intrusion into the drippers as well
as tree vigor decline due to an unbalanced and restricted wetting vo-
lume for the root system (Ayars et al., 2015). To date, five years after
the SDI installation, we did not find the above mentioned problems
(Paris 2016, personal communication). Indeed, we prevented root in-
trusion by applying yearly, at the beginning of the irrigation season, an
aqueous solution of orthophosphoric acid (H3PO4). Root strangulation
is mostly due to big roots and it was noticed only in walnut plantations
(Ayars et al., 2015). In poplar SRC, due to the very high planting
density, the development of big roots is largely restricted, coarse roots
representing only a negligible percentage (1–3%) of the root system
(Chimento and Amaducci, 2015). Declining tree vigor and plantation
yield may represent an additional concern for poplar SRCs, which are
affected by repeated short-term copping cycles (Sabatti et al., 2015;
Dillen et al., 2013; Geyer, 2006). The interaction between poplar SRC
and SDI, especially adopting a deficit irrigation approach, should be
therefore carefully monitored by long-term observation experiments.
5. Conclusions
To the best of our knowledge, the present study represents the first
attempt to study the effect of the SDI system on growth, yield and
physiology of poplar SRC under Mediterranean conditions. From this
research, the following is concluded:
(i) CI and DI recovered 23–49 and 43–90% of the April-September
precipitation deficit, respectively;
(ii) DI increased significantly the overall crop yielding, biomass
quality and tree growth, when compared to CI;
(iii) CI and DI did not change stem moisture and shoot basal density;
(iv) analyzing δ13C in both tree-rings and litterfall biomass provided a
remarkably congruent information on the maintenance of a similar
intrinsic water-use efficiency, irrespective of the irrigation vo-
lumes; this indicates a similar coordination of the assimilatory and
transpiration fluxes at the leaf level, comparing the two watering
treatments. The physiological meaning of iWUE must be inter-
preted as fundamental in the final expression of the irrigation ef-
ficiency. However, on the agro-ecosystem scale, other ecophysio-
logical factors affecting the canopy gaseous exchanges appear
synergic in determining the global WUE of the plantation;
(v) we found a strong relationship between soil moisture profiles and
PDI, indicating that monitoring soil moisture in between 30 and
40 cm of soil depth allows an efficient scheduling of the irrigation;
(vi) long-term research is needed to identify possible constraints to the
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Forest Ecology and Management 409 (2018) 749–756
diffusion of SDI techniques in poplar SRC, especially concerning
the risk of declining tree vigor and plantation yield.
Acknowledgements
Funds for this study were provided by the international projects
AGFORWARD (Agroforestry that will advance Rural Development
(2014–2017)) and FACCE-SURPLUS SidaTim (2016–2018). We are
grateful to Mr. Alessio Trani, owner of the farm hosting the experi-
mental activity and to Mr. Filippo Ascenzi. Dr. Anil R. Graves, Cranfield
University – United Kingdom, is greatly acknowledged for the critical
review of the final manuscript. PP, MT, LT and ML planned, set up the
experiment and collected samples and data; in particular, GDM col-
lected the samples for δ13C analysis in the tree-rings and LS and ML
executed the carbon stable isotopes determinations; PP, LT, GDM and
ML analyzed the data; PP, LT, GDM and ML wrote the manuscript.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in the
online version, at http://dx.doi.org/10.1016/j.foreco.2017.12.013.
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