Long-term effects of stem girdling on needle structure in Scots pine - Sisef
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iForest Research Article
doi: 10.3832/ifor2648-011
vol. 11, pp. 476-481
Biogeosciences and Forestry
Long-term effects of stem girdling on needle structure in Scots pine
Roman Gebauer (1), Stem girdling is the process of completely removing a strip of cork and phloem
tissue. Phloem is the living tissue which serves as the main long-distance path-
Roman Plichta (1), way for transporting carbohydrates produced during photosynthesis to all parts
Jiří Foit (1), of the plant where needed, from source leaves to sinks. Stem girdling has
Václav Čermák (1), been used to study several functional aspects of phloem and their direct im-
Josef Urban (1-2) pacts on tree growth. Although both photosynthesis and transpiration pro-
cesses take place in needles, no studies exist which investigate the effect of
source-sink disturbance on needle structure. In this study, we evaluated
changes in needle morphology and anatomy in current-year Scots pine needles
227 and 411 days after girdling (DAG). Although the studied needle parameters
recorded 227 DAG were from 2 to 20% higher than the same parameters in
control needles, the differences were not significant. On the other hand, nee-
dles 411 DAG were thinner, with decreased cross-sectional areas, phloem ar -
eas, vascular cylinder areas, needle dry mass, needle density, and needle flat-
ness when compared to control needles. Marked variations in needle growth
were observed 411 DAG, with a smaller number of correlations among almost
all studied needle parameters in needles 411 DAG when compared to control
needles or needles 227 DAG. Structural development determining needle flat-
ness, needle density, and leaf mass per area (LMA) appeared to have driving
factors that were independent of the other studied needle parameters, as cor-
relations with other parameters were not significant in any treatment. The
changes in overall needle structure observed after long-term stem girdling
provide new insights into the processes that occur as a result of source-sink
disturbances. This type of data could be helpful, for example, in studies
specifically focused on phloem transport, tree carbon relationships, or investi-
gations modeling gas exchange. Our study might also support gene expression
studies, which could provide further knowledge about the regulatory mecha-
nisms that determine needle size and structural form.
Keywords: Anatomy, Cross-section, Morphology, Pinus sylvestris, Phloem,
Source-Sink Disturbance
Introduction on apical dominance (Wilson & Gartner 2002, Domec & Pruyn 2008). Despite its
Phloem serves as the long-distance path- 2002), on the phloem-xylem connection ecological significance, studies about the
way for transporting carbohydrates from (Zwieniecki et al. 2004), on processes in- anatomical and physiological effects of
source leaves to sink regions of active volving bark regeneration (Mwange et al. stem girdling in forest trees are scarce
growth, storage structures, and other non- 2003, Pang et al. 2008), and relationships compared to those carried out on branch
photosynthetic cells, including those in between tree water and carbon status girdling in horticulture (Lopéz et al. 2015).
roots (Lopéz et al. 2015). Artificial girdling, (Johnsen et al. 2007, De Schepper & Step- The effects of stem girdling differ from
i.e., the complete removal of a strip of bark pe 2011). Phloem girdling has also been those of branch girdling in that it promotes
and phloem around a tree’s outer circum- practiced in forestry as a pre-harvest treat- carbohydrate accumulation above the gir-
ference, has traditionally been used to ment to alter wood properties by manipu- dle and prevents carbohydrates from being
study several functional aspects of phloem lating annual ring width, wood density, the transported to the roots (Lopéz et al.
tissue and their impacts on tree growth as duration of cambial activity, and latewood 2015). The first visual symptom after girdl-
a transport pathway (Morandi et al. 2007), production (Noel 1970, Wilson & Gartner ing is an increase in stem diameter above
the girdle due to the growth of bark and
xylem stimulated by the accumulation of
(1) Mendel University in Brno, Faculty of Forestry and Wood Technology, Zemedelská 3, carbohydrates, coupled with the interrup-
Brno, 61300 (Czech Republic); (2) Siberian Federal University, Krasnoyarsk (Russia) tion of stem growth below the girdle (Dau-
det et al. 2005, De Schepper et al. 2010).
@ Roman Gebauer (gebo@email.cz) Roots are gradually depleted of their car-
bohydrate reserves and suffer starvation
Received: Oct 10, 2017 - Accepted: Apr 05, 2018 (Weaver & McCune 1959). Although the
structural adaptation of stems to disrup-
Citation: Gebauer R, Plichta R, Foit J, Cermák V, Urban J (2018). Long-term effects of stem tion in phloem long-distance transport has
girdling on needle structure in Scots pine. iForest 11: 476-481. – doi: 10.3832/ifor2648-011 been studied in detail, to the best of our
[online 2018-07-02] knowledge no research exists on the struc-
tural adaptation of leaves or needles in re-
Communicated by: Silvano Fares sponse to stem girdling. Only a handful of
studies have focused on the development
© SISEF http://iforest.sisef.org/ 476 iForest 11: 476-481Gebauer R et al. - iForest 11: 476-481
of leaf area and leaf mass per unit area cused on needle structural development 8 tex, secondary phloem, and cambium)
iForest – Biogeosciences and Forestry
(LMA) after girdling (Day & DeJong 1990, and 14 months after girdling (hereafter re- from around the entire stem at a height of
Domec & Pruyn 2008) and only one study ferred to as 227 and 411 DAG, days after 1.3 m above the ground. The girdled area
focused on needle xylem structure devel- girdling, respectively). This study follows was completely covered with resin at the
opment after stem girdling (Gebauer et al. up on our previous work (Gebauer et al. end of the experiment. Sap flow was moni-
2017). It was observed that long-term stem 2017), in which needle xylem structure, sap tored in all experimental trees from 1 April
girdling led to a reduction in the theoretical flow, and non-structural carbohydrate to 30 August 2014, using EMS 51 sap flow
hydraulic conductivity of Scots pine nee- (NSC) changes after stem girdling were an- meters (EMS Brno, Czech Republic). Cur-
dles, and in their xylem area and number of alyzed. We hypothesize that (i) needle rent year needles from sun-exposed
tracheids (Gebauer et al. 2017). The physio- growth will increase in response to carbo- branches were also used to analyze levels
logical adaptation of leaves after girdling, hydrate accumulation 227 DAG, (ii) needle of non-structural carbohydrates (NSC). A
on the other hand, has been studied more growth will be reduced 411 DAG, as root detailed description of girdling treatment,
thoroughly. The accumulation of carbohy- starvation will lead to decreased sap flow sap flow, and NSC analysis is given in Ge-
drates in leaves after girdling leads to the and to a subsequent water shortage in the bauer et al. (2017).
consequent down-regulation of photosyn- needles, and (iii) correlations among the
thetic rates (Rivas et al. 2007), decreased studied needle morphological parameters Needle structure analysis
stomatal conductance and transpiration will be different in girdled and control Five current-year shoots with fully devel-
(Sellin et al. 2013), the accumulation of ab- trees. oped needles were sampled from each of
scisic acid in leaves (Setter et al. 1980), and the trees. The shoots were obtained from
an increase in leaf water potential (Wil- Material and methods branches at the middle height of the
liams et al. 2000). It has also recently been crown. The shoots were facing south and
shown that non-structural carbohydrates Study site and description of the situated on the outer side of the crown.
(NSC) regulate the gene expression in- experiment Samples were collected on 30 August 2014
volved in several plant metabolic functions The study site is an even-aged mixed (i.e., 227 or 411 days after girdling, hereafter
(Hara et al. 2003, Murakami et al. 2008). coniferous/deciduous forest stand located referred to as DAG). In the field, the sam-
Such a broad range of physiological adap- near Brno (south-east of the Czech Repub- ples were fixed in FineFIX® solution (Mile-
tations in leaves after stem girdling should lic – 49° 15′ 39″ N, 16° 36′ 20″ E; 340 m stone, Bergamo, Italy). Subsequently, from
also trigger structural adaptation. In higher a.s.l.). The mean annual air temperature each of the collected shoots, four ran-
plants, the coordination of metabolism and and precipitation are 8.7 °C and 490 mm, domly selected fascicles (with two needles
morphogenesis often depends on hor- respectively. In 2014, the mean air temper- per fascicle, thus yielding 40 needles per
mone signals from one part of the plant to ature was 11.3 °C and the sum of precipita- tree) were collected for further needle
another (Taiz & Zeiger 2002). For example, tion was 609 mm. The stand was planted in structure analysis. One needle from each
the transport of auxin from the shoot to 1928, with Scots pine (Pinus sylvestris L.) fascicle was used for cross-sectional ana-
the root affects various developmental being the dominant tree species. The soil tomical analysis, while the second one was
processes, including stem elongation and type is mesotrophic Cambisol. Twenty two scanned immediately after removal from
leaf senescence (Taiz & Zeiger 2002). Thus, co-dominant Scots pine trees were se- the fixative solution to determine the pro-
the other interesting question is how the lected for detailed analysis. Six trees were jected needle area (PLA) and individual
disruption of the phloem transport of plant selected as controls, 8 trees were stem gir- needle length (Ln) using the software Im-
hormones affects the interplay among the dled in summer, on 15 July 2013, and 8 trees ageJ® (National Institute of Mental Health,
various highly correlated structural param- were girdled in winter, on 15 January 2014. Bethesda, Maryland, USA). Scanned nee-
eters of leaves. As both photosynthesis By the time of the summer girdling, the dles were then oven dried at 85 °C for 48
and transpiration processes take place in needles were fully developed in length. hours to determine needle dry mass (DM).
leaves, further knowledge about how Stem cambium was active until September; The leaf mass per unit area (LMA) was cal-
leaves adapt to girdling is important for a however, most of the cells in the growth culated as the ratio of DM/PLA and the
better understanding of the physiology of ring had already been formed at the time needle density (ND, g cm-3) was calculated
the whole tree (Yan et al. 2012). of summer girdling and a decline in the according to eqn. 1:
The aim of this study was to gain an in- number of cells upon the enlargement DM
N D= (1)
sight into the anatomical and morphologi- phase suggested a transition from early- A n Ln
cal responses of Scots pine (Pinus sylvestris wood to latewood formation (Fajstavr et
L.) needles to the disturbance of phloem al. 2017). Girdling consisted of removing a Cross-sections for anatomical analyses
long-distance transport channels. We fo- 7-10 cm wide band of bark (periderm, cor- were taken at the needle base and then ex-
amined under an Olympus BX51® light mi-
croscope (Olympus, Tokyo, Japan) at mag-
Fig. 1 - Measured nifications of up to ×400 and photo-
needle parame- graphed using a Canon EOS® 1100D digital
ters: needle camera (Canon Inc., Tokyo, Japan) con-
thickness (D1), nected to a computer by means of Quick-
needle width PhotoMicro 3.1 software (Promicra,
(D2), needle Prague, Czech Republic). The following pa-
cross-sectional rameters were measured using ImageJ
area (An, solid software (Fig. 1): cross-sectional needle
bold line), vascu- area (An), vascular cylinder area (Avas),
lar cylinder area phloem area (Ap), needle thickness (D1),
(Avas, dashed and needle width (D2). Needle cross-sec-
bold line), nee- tional shape (i.e., needle flatness, Fn) was
dle phloem area calculated as the ratio of D1/D2. A needle
(Ap , solid fine with a round or square cross-section would
line). have a value of Fn close to 1, and lower ra-
tios would characterize more flattened
needles.
477 iForest 11: 476-481Effects of girdling on the needle structure
Statistical analysis
iForest – Biogeosciences and Forestry
Tab. 1 - Overview of the needle parameters, their abbreviations, definitions and units
The linear mixed effect model (LME) em-
used throughout this study.
ploying the restricted maximum likelihood
method (REML) was used, where individual
trees were specified as a random effect Parameter Explanation Unit
(Zuur et al. 2009). Where appropriate (i.e., An needle cross-sectional area mm2
for the parameters DM, Ln, LMA, ND, and Ap needle phloem area mm2
PLA), the simple linear model was used. Avas vascular cylinder area mm2
Linear models were also used for correla- D1 needle thickness mm
tion matrices. Next, the Tukey’s honestly D2 needle width mm
significance difference (HSD) test was used DM needle dry mass mg
to indicate which treatments differed (sig- Fn needle flatness (D1/D2) -
nificance level 0.05), and p-values assess- Ln needle length mm
ing the probability of difference between LMA leaf mass per area (DM/PLA) g m-2
treatments were extracted. The R statisti- ND needle density g cm-3
cal program (R Core Team 2015) was used PLA needle projected area mm2
for statistical analysis. LME was fitted using
the lme function from the nlme library,
while Tukey’s test was performed using the statistically significant (Fig. 2 and Tab. 2). 36 and 30%, respectively, resulting in a sub-
glht function from the multcomp library. All Only LMA, which was approximately 9% stantial decrease in the cross-sectional di-
acronyms, abbreviations, and symbols are higher in needles 227 DAG than in control mensions of these needles compared to
defined in Tab. 1. needles, had a p-value close to the level of control needles (Fig. 2 and Tab. 2). Needles
significance (p = 0.06). In contrast, nearly 411 DAG were flatter (Fn decrease) than
Results all studied needle parameters were signifi- control needles due to substantial de-
cantly changed 411 DAG. On average, nee- creases in D1, and not D2. Contrary to most
Needle structure dles 411 DAG were shorter, thinner, denser, of the other needle parameters 411 DAG, Ln
Although all studied needle structural pa- and lighter than control needles by 10, 32, was not significantly different from the
rameters 227 DAG were slightly higher in 31, and 16%, respectively (Ln, D1, ND, DM, re- same parameter in control needles (Tab. 2).
girdled than in control trees (except no dif- spectively – Fig. 2). Also, the An, Ap, Avas, and Also, LMA and PLA values in needles 411
ference in Fn), these differences were not Fn of needles 411 DAG were lower by 26, 52, DAG and in control needles were similar
Fig. 2 - Means of mor-
phological and anatom-
ical parameters of
Scots pine control nee-
dles, needles 227 days
after girdling (DAG)
and needles 411 DAG.
Points in grey repre-
sent measured data.
Vertical bars are 95%
confidence intervals
derived from the
appropriate model.
Parameters that are
different at the 5% sig-
nificance level are indi-
cated by different let-
ters. See Tab. 1 for an
explanation of needle
parameters.
iForest 11: 476-481 478Gebauer R et al. - iForest 11: 476-481
PLA were relatively weak for both control
iForest – Biogeosciences and Forestry
Tab. 2 - P-values from Tukey’s HSD test showing the probability of differences in and girdled trees (Fig. 3 – right panel). The
parameters between control needles and needles 227 or 411 days after girdling (DAG), only exception was a correlation between
and between needles 227 and 411 DAG. For an explanation and definition of the para - Ln and PLA in control needles and needles
meters, see Tab. 1. 411 DAG, and a correlation between LMA
and ND in needles 227 DAG. In addition, DM
p-value was correlated with Ln and PLA in control
Parameter
control × 227 DAG control × 411 DAG 227 DAG × 411 DAG needles and needles 411 DAG (Fig. 3 – right
An 0.50Effects of girdling on the needle structure
in needle water shortage and eventual tree number of correlations that achieved the (2017). The effect of stem girdling on xylem and
iForest – Biogeosciences and Forestry
death (Negreros-Castillo & Hall 1994, Pari- required level of significance were ob- phloem formation in Scots pine. Silva Fennica
ona et al. 2003). This could be the reason served in needles 411 DAG (partially sup- 51 (4): artID1760. - doi: 10.14214/sf.1760
why needles 411 DAG were smaller than porting our third hypothesis). It was also Gebauer R, Cermák J, Plichta R, Spinlerová Z,
control needles (supporting our second hy- observed that the structural development Urban J, Volarík D, Ceulemans R (2015). Within
pothesis). Moreover, needles 411 DAG had determining Fn, ND, and LMA appeared to canopy variation in needle morphology and
a smaller xylem area and a lower number have driving factors that were indepen- anatomy of vascular tissues in a sparse Scots
of tracheids (Gebauer et al. 2017). Our re- dent of the other studied needle parame- pine forest. Trees - Structure and Function 29:
sults also correspond with a previous study ters, as correlations with other parameters 1447-1457. - doi: 10.1007/s00468-015-1224-1
(Baldwin 1934) in which poorer leaf devel- were weak in all treatments. This suggests Gebauer R, Plichta R, Bednárová E, Foit J, Cer-
opment and smaller leaf size were ob- that gene expression in the needles of con- mák V, Urban J (2017). How timing of stem
served for three deciduous species in the trol and girdled trees could provide further girdling affects needle xylem structure in Scots
second season following stem girdling. We insights into the regulatory mechanisms pine. European Journal of Forest Research 14:
should note that several other factors (site that determine the size and structural form 68. - doi: 10.1007/s10342-017-1090-z
conditions, climate, tree age, nutritional of needles. Hara M, Oki K, Hoshino K, Kuboi T (2003).
status, and tree health) also play an impor- Enhancement of anthocyanin biosynthesis by
tant role in needle development along with Acknowledgements sugar in radish (Raphanus sativus) hypocotyls.
carbohydrate concentration and water sta- This work was funded by Czech project Plant Science 164: 259-265. - doi: 10.1016/S0168-
tus. For example, Scots pine needles grow- MSMT COST LD 13017 under the framework 9452(02)00408-9
ing on dunes with poor water availability of the COST FP1106 network STReESS, by Johnsen K, Maier C, Sanchez F, Anderson P, But-
had An values similar to those of trees 411 the Ministry of Education, Youth and nor J, Waring R, Linder S (2007). Physiological
DAG (Lukjanova & Mandre 2008). In the Sports of the Czech Republic (Grant INTER- girdling of pine trees via phloem chilling: proof
present study, the mean values of D 1 (0.56 TRANSFER LTT17033), and by the project of concept. Plant Cell and Environment 30: 128-
mm) and D2 (0.91 mm) for control trees “Indicators of Tree Vitality” (Grant No. 134. - doi: 10.1111/j.1365-3040.2006.01610.x
were at the lower end or below the range CZ.1.07/2.3.00/20.0265) co-financed by the Lin J, Sampson DA, Deckmyn G, Ceulemans R
reported for adult Scots pine trees (0.4- European Social Fund and the state budget (2002). Significant overestimation of needle
0.72 mm and 1.13-1.32 mm, respectively – of the Czech Republic. surface area estimated based on needle dimen-
Lin et al. 2002, Luomala et al. 2005, Luk- sions in Scots pine (Pinus sylvestris). Canadian
janova & Mandre 2008). Interestingly, the Conflict of Interest Journal of Botany 80: 927-932. - doi: 10.1139/
reactions of D1 and D2 in response to The authors declare that they have no b02-081
girdling differed, as only D 1 was observed conflicts of interest. Lopéz R, Brossa R, Gil L, Pita P (2015). Stem
to have decreased in needles 411 DAG. It girdling evidences a trade-off between cambial
seems that needles 411 DAG still had a suffi- References activity and sprouting and dramatically reduces
cient water supply during the early stages Baldwin HI (1934). Some physiological effects of plant transpiration due to feedback inhibition
of needle development (i.e., in May 2014, girdling Northern hardwoods. Bulletin of the of photosynthesis and hormone signaling.
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59 ± 10% of that of control trees). However, 2480918 fpls.2015.00285
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