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Investigating the relationship between various measuring methods for determination of establishment success of urban trees
Urban Forestry & Urban Greening 28 (2017) 21–27
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Original article
Investigating the relationship between various measuring methods for determination of establishment success of urban trees
MARK
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Anna Levinsson , Ann-Mari Fransson, Tobias Emilsson Department of Landscape Architecture, Planning and Management, Swedish University of Agricultural Sciences, Slottsvägen 5, 20353 Alnarp, Sweden
A R T I C L E I N F O
A B S T R A C T
Keywords: Establishment definition Leaf size Nightly recovery Shoot growth Shoot water potential Stomatal conductance
Establishment is a key concept in urban forestry but it is currently inconsistently defined and measured. Thus, several different methods are being used to determine establishment success but their consequences and applications are rarely discussed. With this paper we would like to stimulate an increased discussion regarding these concepts both in relation to a theoretical definition but also to their practical use. The problem was approached through an experiment using sweet cherry (Prunus avium L.) and northern red oak (Quercus rubra L.) trees and the most common methods used for determination of establishment success. The trees were studied during the first three years after transplant and the association between the different measuring methods was examined. A Principal Component Analysis showed that terminal and lateral shoot length were strongly correlated, and that midday- and pre-dawn shoot water potential, and stomatal conductance were strongly correlated. We developed an index for nightly recovery of water status, which showed that terminal shoot growth was not related to nightly recovery until the third year after transplanting. Our results suggest that successful tree establishment is determined differently depending on which method is used for determination but that the differences might decrease with time. The lack of a firm definition of the term establishment may complicate communication, both within the scientific community and in practice.
1. Introduction Although not clearly defined, the term establishment is often used to describe a tree’s status after transplanting. Within practice, successful establishment is often demanded from contractors and promised by tree nurseries. Furthermore, numerous scientific studies have set out to compare the effects of various production, planting and/or management techniques on trees’ and tree seedlings’ capacity to become fully established (e.g. Struve, 1993; Gilman and Beeson, 1996; Gilman, 2004; Ferrini and Baietto, 2006; Davis et al., 2008; Jacobs et al., 2009). There are several different approaches on how to measure establishment success. It is often determined by survival, or shoot, leaf, or stem growth (Struve and Joly, 1992; Day et al., 1995; Radoglou and Raftoyannis, 2002; Harris et al., 2008; Pinto et al., 2011; Dostalek et al., 2014; Woolery and Jacobs, 2014; Sherman et al., 2016), or the treés resumption of pre-transplant shoot or trunk growth rates (Gilman and Beeson, 1996; Struve et al., 2000). Establishment success is sometimes determined by measurements of physiological attributes such as hydraulic conductivity or water potential (Carlson and Miller, 1990; Beeson 1994), or through a combination of both physiological and morphological attributes (Harris and Gilman, 1993; Lauderdale et al.,
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1995; Gilman et al., 1998). Gilman et al. (1998) used both growth and water potential measurements in a post-transplant study of trees exposed to different irrigation volumes, but the conclusions on establishment success were based on stem and height growth. In another study, Harris and Gilman (1993) based their conclusions regarding tree establishment success on both physiological and morphological determinations. Struve et al. (2000) considered trees established once they showed no signs of drought stress even under mild drought, and thus concluded that they did not need further irrigation. Struve (1990) has mentioned that there is no workable definition of the term establishment. As a consequence, establishment is defined, and measured, in different ways. It can be seen as a biological process (Rietveld, 1989) during which the transplanted tree becomes fully connected to the hydrologic cycle of the growing site (Grossnickle, 2005). It has been suggested that an urban tree might be considered established when it does not need further irrigation (Day and Harris, 2007), a definiton that is only applicable to trees that are being irrigated. However, it is unclear exactly when a transplanted tree is fully coupled to the hydrologic cycle and no longer needs further irrigation, and several methods for determining the water status during the establishment process are being used. A tree may also be considered
Corresponding author. E-mail address: [email protected] (A. Levinsson).
http://dx.doi.org/10.1016/j.ufug.2017.09.014 Received 19 January 2017; Received in revised form 21 September 2017; Accepted 26 September 2017 Available online 28 September 2017 1618-8667/ © 2017 Published by Elsevier GmbH.
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program during the first two post-transplant years of the study. They were irrigated approximately every second week. All trees were planted at the same depth with the root collar at the soil surface, in a threemetre-wide grass strip, alongside a street in a high-rise residential area. They were irregularly planted with a minimum distance of four metres. A one metre in diameter circle around the trees was covered with smallsized gravel to reduce grass competition. At Alnarp, the trees were planted in a field, with 4.5 metres between each tree in every direction. The soil was covered with a single layer of black polypropylene ground cloth (Mypex®) to inhibit weed growth. A drip-irrigation system was installed where the hose made a circle around each tree at the perimeter of the root ball to ensure that water was available for the planted root mass. The plant water availability was determined regularly using an HH2 moisture meter (Delta T Devices Ltd., Cambridge, UK) at 10, 20, 30 and 40 cm depths to ensure that the trees were never drought stressed during the two following growing seasons. The probes for the moisture meter were installed just beyond the planting zone, with controls installed in to the root balls of the air-potted and root control bag cultivated trees, as the growth substrate in these root balls varied substantially from the texture of the sandy loam at the experimental fields. Irrigation permitted the soil water content to remain near field capacity or just below. No tree at either site received any irrigation during the third year of the study and none of the trees were given additional nutrients.
established when it reaches a productive phase, that is, when it starts fulfilling the purpose for which it was planted (Day and Harris, 2007); this definition is based upon a functionality perspective rather than a biological one. For an urban tree, the purpose of planting is connected to the expected environmental and aesthetic benefits associated with urban forests (Schroeder and Cannon, 1983; Akbari, 2002; Nowak and Crane, 2002; Saebo et al., 2012). Significant growth and high crown density may thus be considered necessary attributes for an urban tree to be considered as established, leading to determination of establishment success being based on morphological characteristics rather than physiology (Summit and Sommer, 1999; Day and Harris, 2007). The aim of our study was to highlight how differently the concept of establishment has been approached in the field of urban forestry and what effect the approach has on determinations of establishment success. We did this by comparing the relationship between different methods for measuring establishment, both morphological and physiological. We analysed data from two commonly used urban tree species during the three consecutive years directly after planting. The analyses were performed on trees exposed to different post-transplant management regimes to allow for general validity. We compared measurements of midday and pre-dawn shoot water potential, stomatal conductance, terminal and lateral shoot growth, leaf area, and survival, all of which are commonly studied attributes in determinations of establishment. Measurements were performed to capture both seasonal and annual changes throughout the study. We also calculated a nightly recovery index, as a value for water status including both midday- and pre-dawn status.
2.2. Determinations Measurements were performed during the three seasons after transplanting (Table 1). Midday shoot water potentials (Ψm) were determined between 11.30 am and 16.00 pm and pre-dawn shoot water potentials (Ψpd) were determined the following day approximately one hour before sunrise. The time of the pre-dawn measurements varied over the season, depending on the time of sunrise. The determinations were performed with a three-week interval, except when bad weather prevented measurements and measurements had to be postponed. A pilot study showed that there were very small differences in shoot water potential within each tree, allowing us to use a single shoot from each tree at each occasion. Two to three cm of the shoot tip was cut off from a branch at the middle height of the crown and immediately installed in a pressure chamber (Model 1000, PMS Instrument Company, OR, USA). Pressure was increased in the chamber at a constant rate of 0.05 MPa/s (Turner, 1988). Before cutting the shoot for the water potential determination, leaf stomatal conductance (gs) was determined on two fully sun-exposed leaves on each shoot during the daytime measurements. Conductance was determined each year after transplanting using a leaf porometer (model SC-1, Decagon Devices, Pullman, WA, USA). Shoot elongation measurements were performed each season, after shoot elongation cessation. Both species grew with one flush per year. Two terminal and two lateral shoots in the south, the north, the east, and the west, from the middle height of the crown were measured. To reduce the impact of removing mature leaves from the small trees in 2007, leaf size was determined by measuring the leaves that had grown on the shoots cut off for water potential measurements. Three leaves on each shoot (the first, third, and fourth leaf, counting from the shoot tip) were scanned within one day after they had been sampled from the tree, with a total of nine leaves per season. Leaf size was analysed using ImageJ (http://imagej.nhi.gov/ij version 1.4.3.67, Broken symmetry software, USA). For determinations of survival, all trees were revisited in 2013 and the status of each tree was assessed as good, in decline or dead. Examples of signs of decline were dead main branches, low crown density, and/or discolouration.
2. Materials and Methods 2.1. Trees and study site In this study, 50 trees of Prunus avium and 50 trees of Quercus rubra, were used. They originated from two nurseries, situated in the south of Sweden. All trees within the same species came from the same nursery and they were selected early in the spring of 2007, before growth had started. All trees within a species originated from the same seed source, and they had been treated according to Swedish standards for field cultivation of trees until the start of the study (LRF, 2012). Their selection was based on stem circumference and general appearance, with the intention of choosing as uniform plant material as possible. Stem circumference was 14–17 cm at one metre above the root collar (standard measuring procedure in the Swedish nursery industry) and the nine-year-old trees were about four metres tall. They were randomly assigned one of five different root treatments – root pruning, barerooted, balled and burlapped, spring-ring cultivation (Superoots® plastic, The Caledonian tree Co., Edinburgh, UK), forming an Air-Pot® and root control bag cultivation in in-ground fabric container (Smart Pot®, High Caliper, OK, USA), as described in a parallel paper (Levinsson et al., 2014). The trees were then treated according to standard procedures for the assigned production system during the last growing season before transplanting (LRF, 2012). The production systems of urban trees can be seen as an integrated result of several production variables such as e.g. container design/root treatment, irrigation, and substrate/soil. Each treatment included 10 trees of each species. The bare-rooted and the balled and burlapped trees were left undisturbed in the field, and the root-pruned trees were pruned without being removed from their growing spots. For the two other treatments, the trees were harvested and the treatments were carried out at two different nurseries specialising in the particular production system. The trees were kept in the nurseries until the spring of 2008, when they were transplanted at two different sites; in the city of Malmö and in the experimental fields at the campus of the Swedish University of Agricultural Sciences, Alnarp. Four trees of each species and production system were planted in the city of Malmö and the trees were managed by the municipality and included in their establishment management
2.3. Statistical analyses Principal Component Analyses (PCA) were performed using R (version 2.15, R development Core team, 2014) running the 22
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Table 1 Mean values with SE of all parameters included in the analyses. The number of measuring occasions varied over the years, depending on weather conditions and the length of the growing season. Water potential determinations were performed on fully developed shoots. Quercus rubra
Water potential (MPa)
Stomatal conductance (mmol m−2 s−1)
Annual shoot growth (cm) Leaf size (cm2) Prunus avium Water potential (MPa)
Stomatal conductance (mmol m−2 s−1)
Annual shoot growth (cm) Leaf size (cm)
Year 2008
2009
2010
Midday, per occasion
−1.37 ± 0.06; −1.54 ± 0.07; −1.31 ± 0.09
Annual mean Pre−dawn
−1.40 −0.48 −0.64 −0.35
Annual mean Midday
−0.49 ± 0.04 117.6 ± 13.7; 89.8 ± 11.6; 308.9 ± 26.9
Annual mean Terminal Lateral
172.1 ± 13.4 12.70 ± 1.03 5.75 ± 0.50 53.60 ± 3.84
−1.3 ± 0.06; −1.36 ± 0.07; −1,52 ± 0.09; −1.44 ± 0.05; −1.70 ± 0.09 −1.43 ± 0.03 −0.43 ± 0.07; −0.53 ± 0.07; −0.66 ± 0.11; −0.29 ± 0.05; −0.56 ± 0.08 −0.49 ± 0.03 247.9 ± 25.8; 323.9 ± 28.3; 346.6 ± 36.3; 438.6 ± 25.4; 516.3 ± 46.5 374.5 ± 16.0 8.36 ± 0.93 4.88 ± 0.62 67.16 ± 3.07
−0.95 ± 0.03; −1.68 ± 0.08; −2.16 ± 0.17; −1.17 ± 0.05; −1.22 ± 0.07 −1.44 ± 0.04 −0.22 ± 0.03; −0.63 ± 0.09; −1.05 ± 0.15; −0.15 ± 0.03; −0.41 ± 0.02 −0.49 ± 0.04 312.0 ± 14.5; 196.3 ± 10.9; 176.1 ± 16.8; 801.8 ± 48.1; 722.9 ± 45.7 441.8 ± 22.1 7.62 ± 0.58 3.75 ± 0.37 90.45 ± 4.45
Midday, per occasion
−1.10 ± 0.04; −1.74 ± 0.07; −1.41 ± 0.06
−2.21 ± 0.05; −1.30 ± 0.03; −1.29 ± 0.06
Annual mean Pre-dawn
−1.41 −0.35 −0.60 −0.31
Annual mean Midday
−0.41 ± 0.03 124.6 ± 15.1; 173.4 ± 15.0; 653.3 ± 47.4
Annual mean Terminal Lateral
318.4 ± 26.3 11.95 ± 1.08 4.39 ± 0.63 25.49 ± 1.01
−1.41 ± 0.06; −1.61 ± 0.09; −1.65 ± .09; −1.49 ± 0.04; −1.81 ± 0.08 −1.60 ± 0.03 −0.44 ± 0.05; −0,63 ± 0.05; −0.68 ± 0.07; −0.45 ± 0.01; −0.71 ± 0.05 −0.50 ± 0.02 358.2 ± 37.2; 501.4 ± 37.5; 491.7 ± 43.6; 706.6 ± 39.5; 664.6 ± 50.6 544.5 ± 20.3 9.07 ± 0.94 2.12 ± 0.48 39.62 ± 1.05
± ± ± ±
± ± ± ±
0.04 0.06; 0.09; 0.07
0.04 0.03; 0.06; 0.04
−1.60 −0.79 −0.24 −0.61
± ± ± ±
0.05 0.07; 0.04; 0.02
−0.55 ± 0.03 232.5 ± 19.1; 1178.9 ± 57.4; 1164.7 ± 61.7
858.7 ± 46.5 34.1 ± 2.34 19.44 ± 2.55 40.78 ± 1.54
and pre-dawn shoot water potential were analysed using annual, species-specific linear regressions. The linear regression analyses were performed using Minitab 17 Statistical Software (2014) for Windows (Minitab, Inc., State College, PA, USA).
FactoMineR package (Le et al., 2008). The PCA was based on the correlation matrix and calculated on Euclidean distances. It was performed individually on Quercus rubra and Prunus avium respectively. Ψ m, Ψpd, gs, leaf size, terminal and lateral shoot length and year were used as main variables. Production system and site were included as supplementary parameters. To study the trees’ nightly recovery (NR) ability and how recovery was related to other measures of establishment, a recovery index was developed from the difference between midday and pre-dawn shoot water potential, as a proportion of the midday shoot water potential, as:
3. Results The shoot water potential showed seasonal fluctuations (Table 1). Increasing stomatal conductance and leaf sizes over time were clear in both species. PCA for Quercus rubra and Prunus avium revealed a similar relationship between variables (Figs. 1 and 2 respectively). For both species, a large proportion of the variation was captured by the first two PCA axes. The first axis corresponded to 35.8% of the total variation in the Q. rubra dataset (Table 2). The axis was found to be significantly correlated as well as having high cos2 values for Ψm, Ψpd, and gs. Leaf size also correlated to the first axis but with a slightly lower cos2 value. The second axis explained 29% of the total variation. The axis was found to be significantly correlated as well as having high cos2 values for terminal and lateral shoot growth, and year.
NR = (Ψm − Ψpd)/Ψm. Ψm = midday shoot water potential, Ψpd = pre-dawn shoot water potential. The nightly recovery rate was calculated for each measuring occasion. A seasonal mean was calculated for each tree and used as a response variable in year- and species-specific multiple regressions, with terminal and lateral shoot length, stomatal conductance and leaf size as predictors. The variations over years in the relation between midday
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The PCA for P. avium revealed that the first axis corresponded to 38.2% of the total variation. This axis was found to be significantly correlated as well as having high cos2 values for terminal and lateral shoot growth, and year. Leaf size was also correlated to the first axis but with a slightly lower cos2 value. The second axis was found to be significantly correlated as well as having high cos2 values for Ψm, Ψpd, and gs. The second axis explained 29% of the total variation (Table 2). 3.1. Shoot water potentials and nightly recovery The two species showed similar patterns over the years in how the seasonal mean NR was related to the predictors in the multiple regressions (Table 3). NR was related to stomatal conductance of the preceding day during all three years after transplanting for both species. Leaf size was related to NR in 2008 for Q. rubra, and in 2010 for both species. In 2010, terminal shoot length was also related to the NR for both species. There was a strong relationship between pre-dawn and midday measurements of shoot water potential for both species during all years of measurements (p < 0.001, across all occasions, Table 4). However, the relationship strength increased with each year following transplant. The tendency was the same for both species.
Fig. 1. Output of PCA for Quercus rubra, including measurements from the three first posttransplant years. Abbreviations in the figure: ψPD = pre-dawn shoot water potential; ψM = midday shoot water potential; SGT = terminal shoot growth; SGL = lateral shoot growth; gs = stomatal conductance; LS = leaf size; and Y = year.
3.2. Survival The survival of the trees was high; only one bare-rooted Q. rubra tree died during the year after planting in Malmö. Another Q. rubra had died and two showed signs of decline at the visual inspection in 2013. When examining data from 2008, 2009, and 2010 for these trees, no differences in nightly recovery were found between these trees and the other. 4. Discussion The results from this study indicate that determination of tree establishment may depend on the choice of measuring method. Assessments of either shoot length or water status are commonly used to determine tree establishment (Beeson, 1994; Day et al., 1995; Buhler et al., 2007) yet for both species studied, PCA showed that shoot elongation and water status are not correlated in the first few years following transplant. Shoot length is often reduced after transplanting compared to pre-transplant growth, and our results indicate that shoot length does not indicate whether the tree is water stressed or acclimated. Brouwer (1983) has described the functional equilibrium, claiming that either roots or shoots are limiting growth at any given time, since shoots are dependent on uptake from roots for development, and roots depend upon carbohydrates produced primarily by the leaves for their development (Brouwer, 1983). A model by Watson and Himelick (1997) shows that a period of reduced growth is expected after transplant and that establishment has occurred once shoot elongation has resumed to pre-transplant rates. But, restricted shoot growth and
Fig. 2. Output of PCA for Prunus avium, including measurements from the three first posttransplant years. Abbreviations in the figure: ψPD = pre-dawn shoot water potential; ψM = midday shoot water potential; SGT = terminal shoot growth; SGL = lateral shoot growth; gs = stomatal conductance; LS = leaf size; and Y = year.
Table 2 PCA summary of statistics for measured tree performance variables in Quercus rubra and Prunus avium during 2008–2010. The table shows summary statistics for correlation between PCA scores and original values (Corr, p < 0.05, non-significant values are omitted) and cosine2 (cos2: values above 0.45 in bold) between principal components and measurement variables. Ψm – midday shoot water potential, Ψpd – pre-dawn shoot water potential, gs – stomatal conductance, SGT – terminal shoot growth, SGL – lateral shoot growth, LS – leaf size, Y – year, Ssite, and PS – production systems. Species
PC
EV
% expl.
Ψm
Ψpd
gs
SGT
SGL
LS
Y
S
PS
Corr
cos2
Corr
cos2
Corr
cos2
Corr
cos2
Corr
cos2
Corr
cos2
Corr
cos2
R2
R2
0.84
0.71 < 0.01
0.67 0.29
0.45 0.09
0.37 0.83
0.14 0.70
0.45 0.77
0.20 0.59
0.56 0.41
0.32 0.17
0.16 0.71
0.03 0.50
0.40
0.02 0.10
< 0.01 0.78
0.55 0.55
0.30 0.30
0.84 0.19
0.70 0.04
0.81
0.66 < 0.01
0.63
0.40 < 0.01
0.77 0.23
0.60 0.05
0.05 0.34
Q. rubra
1 2
2.51 2.05
35.88 29.28
0.82 0.10
0.67 < 0.01
P. avium
1 2
2.68 2.02
38.24 28.84
0.12 0.92
0.01 0.84
0.88
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of the root/shoot balance, regardless of if one sees establishment from a biological or functional perspective. The use of shoot water potential measurements in studies of establishment is well reported. Several protocols are available, and measurements of midday shoot water potentials in transplanted trees have been compared to shoot water potentials in similar non-transplanted trees, and to pre-dawn potentials in the same trees, and between stressed and unstressed transplanted trees (Beeson, 1994; Montague et al., 2000; Scheiber et al., 2007; Levinsson et al., 2014). As there are no absolute values as to when water potential measurements indicate establishment, and because it is complex finding appropriate reference trees, assessments of establishment status by water potential measurements are often done as comparative studies. In this study, we used the midday and pre-dawn shoot water potential measurements to calculate a recovery index. The recovery index incorporates both midday water status and the trees’ ability to regain nightly equilibrium with soil water potential (Resco et al., 2008), and it reduces pre-dawn and midday measurements to one value, so that water status could be compared with other measuring methods used for determining establishment. In the present study, it was used to compare water status with growth, and the possibility to investigate the strength of the relationship between water status and shot elongation might provide valuable information of a treés process in becoming established. The absence of absolute values for either of the measuring methods to indicate establishment success may make such a comparison even more valuable. Williams and Araujo (2002) found a strong relationship between pre-dawn and midday leaf water potentials in vines grown in a 9-yearold vineyard. The strength of the relation between midday and predawn shoot water potentials increased with time in the present study. This increase in strength may be seen as the result of improved coupling to the hydrologic cycle of the site and thus, an indication of establishment. It has been shown that there are differences both in growth and water flow between terminal and lateral shoots (Joyce and Steiner, 1995). A study on transplant shock in Larix decidua showed that the lateral shoot growth was less affected by transplanting than the terminal (Tranquillini and Havranek, 1970). In our study, there was a strong correlation between terminal and lateral shoot growth during all years, showing no indications that either would be more relevant for establishment measurements of the two investigated species, despite our expectations. Determinations of water potential and measurements of shoot growth were both performed during the second part of the growing season since shoot water potential could only be determined on shoots that were fully developed. However, unlike the shoot water potential determinations, shoot growth measurements reflect the conditions that were prevalent during the first part of the growing season, when shoot elongation occurred. Thus, the two methods of measurement do not study the same time period, with the possibility that conditions might have changed from the early growing season’s period of shoot elongation to the later period of shoot water potential measurements. Such results have been shown in a drought-stress test, studying both physiological and morphological responses to drought (Fotelli et al., 2000). Nonetheless, it might be preferable if indications for establishment success could be measured at any point throughout the season, regardless of temporary circumstances. The establishment of the trees in our study could be seen as very good after the first year if evaluated by survival, as it sometimes is (Radoglou and Raftoyannis, 2002 Löf et al., 2004). However, survival might not be a relevant determination of establishment for trees planted in urban areas, as a declining tree, while surviving, would not fulfil the expected ecosystem services and probably cause a disagreement between contractor and municipality. Furthermore, it is unclear how long after transplanting survival should be assessed. In urban tree management there is often an establishment program, in which the newly planted trees are given extra irrigation during the
Table 3 Annual relevant predictors of mean seasonal nightly recovery (NR) in urban and fieldplanted trees analysed in a multiple regression, using NR as the response variable. Pvalues are included next to the significant predictor. Year
Quercus rubra
Prunus avium
Significant predictor
R2-values
Significant predictor
R2-values
2008
Conductance 0.0083 Leaf size 0.0076
0.39
Conductance < 0.0001
0.34
2009
Conductance < 0.0001
0.66
Conductance < 0.0001
0.59
2010
Conductance < 0.0001 Leaf size 0.011 Terminal growth 0.023
0.77
Conductance < 0.0001 Leaf size 0.030 Terminal growth 0.012
0.72
Table 4 The mean annual shoot water potentials for each species and the level of explanation of the variation in the mean annual midday (Ψm) and pre-dawn (Ψpd,) shoot water potentials for both species during the three first years after transplanting. Regression analyses are based on seasonal mean per individual tree. P < 0.001, at every occasion. Year
2008 2009 2010
Quercus rubra
Prunus avium
Ψm
Ψpd,
R2
Ψm
Ψpd
R2
−1.31 −1.52 −2.16
−0.35 −0.66 −1.04
0.60 0.82 0.93
−1.41 −1.65 −2.21
−0.30 −0.68 −0.79
0.38 0.81 0.83
allocation of nutrients and photsynthates to the root system might merely be a response to changed environmental conditions and is not necessarily connected to a treés potential incapability to absorb the root-available water at a new growing site, making the model by Watson and Himelick (1997) primarily applicable if considering establishment from a functional perspective. The model does not provide information on whether the tree is connected to the hydrologic cycle of the site. Plants are known to constantly change their development in response to changing external signals (Benkova et al., 2003). However, if resources are strongly limited at the new growing site, as they may be in an urban growing site, shoot elongation might never regain pretransplant levels, and could not be expected to. Although clearly related, biological and functional perspectives of establishment provide different approaches to the concept of establishment determinations. If tree establishment is regarded as a question of functionality rather than biology and one considers a tree to be established once it has reached its productive phase (Day and Harris, 2007), growth is indeed important since the productive phase for urban trees can be associated with the point when it meets the objectives for which it was planted. Benefits associated with urban trees, such as particle uptake rate, shading, carbon sequestration and aesthetic experience, increase with canopy size (Schroeder and Cannon, 1983; Summit and Sommer, 1999; Beckett et al., 2000; Escobedo and Nowak, 2009; Saebo et al., 2012; Searle et al., 2012). However, if instead one considers a tree established when it is coupled to the hydrologic cycle of the site (Grossnickle, 2005), then our results suggest that determinations of shoot length might not provide the pertinent information, since shoot length and water status determinations were not correlated in the PCA. Nonetheless, NR was related to terminal shoot growth in the third season after transplanting. This relation indicates that the trees had restored a functional root system for above-ground growth permitting shoot growth and that the shoot elongation then might be used as a proxy of the water status of the tree. Provided that the conditions at the new growing site permit shoot elongation values close to pre-transplant values, then measures of water status and growth might provide the same indications of establishment success after a period of restoration 25
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Sci. 118, 194–200. Jacobs, D.E., Salifu, K.F., Davis, A.S., 2009. Drought susceptibility and recovery of transplanted Quercus rubra seedlings in relation to root system morphology. Ann. For. Sci. 66, 235–251. Joyce, B.J., Steiner, K.C., 1995. Systematic variation in xylem hydraulic capacity within the crown of white ash (Fraxinus Americana). Tree Physiol. 15, 649–656. Lauderdale, D.M., Gilliam, C.H., Eakes, D.J., Keever, G.J., Chappelka, A.H., 1995. Tree transplant size influences post-transplant growth, gas exchange, and leaf water potential of ‘October Glory’ red maple. J. Environ. Hortic. 13, 179–181. Le, S., Josse, J., Husson, F., 2008. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18. Levinsson, A., Saebo, A., Fransson, A.M., 2014. Influence of nursery production system on water status in transplanted trees. Sci. Hortic. 178, 124–131. LRF, 2012. Kvalitetsregler för plantskoleväxter (Eng: Quality rules for nursery plants). Federation of Swedish Farmers (LRF). Retrieved June 14, 2013 from http://www.lrf. se/PageFiles/98759/Kvalitetsregler%20slutgiltig.pdf. Löf, M., Thomsen, A., Madsen, P., 2004. Sowing and transplanting of broadleaves (Fagus sylvatica L., Quercus robur L., Prunus avium L. and Crataegues monogyna Jacq.) for afforestation of farmland. For. Ecol. Manag. 188, 113–123. Montague, T., Kjelgren, R., Rupp, L., 2000. Surface energy balance affects gas exchange and growth of two irrigated landscape tree species in an arid climate. J. Am. Soc. Hortic. Sci. 125, 299–309. Nowak, D.J., Crane, D.E., 2002. Carbon storage and sequestration by urban trees in the USA. Environ. Pollut. 116, 381–389. Pinto, J.R., Marshall, J.D., Dumroese, R.K., Davis, A.S., Cobos, D.R., 2011. Establishment and growth of container seedlings for reforestation: a function of stocktype and edaphic conditions. For. Ecol. Manag. 261, 1876–1884. Radoglou, K., Raftoyannis, Y., 2002. The impact of storage, desiccation and planting date on seedling quality and survival of woody plant species. Forestry 75, 179–190. Resco, V., Ignace, D.D., Sun, W., Huxman, T.E., Weltzin, J.F., Williams, D.G., 2008. Chlorophyll fluorescence, predawn water potential and photosynthesis in precipitation pulse-driven ecosystems – implications for ecological studies. Funct. Ecol. 22, 479–483. Rietveld, W.J., 1989. Transplanting stress in bareroot conifer seedlings; its development and progression to establishment. North. J. Appl. For. 6, 99–107. Saebo, A., Popek, R., Nawrot, B., Hanslin, H.M., Gawronska, H., Gawronski, S.W., 2012. Plant species differences in particulate matter accumulation on leaf surfaces. Sci. Total Environ. 427, 347–354. Scheiber, S.M., Gilman, E.F., Paz, M., Moore, K.A., 2007. Irrigation affects landscape establishment of burford holly, Pittosporum, and sweet viburnum. HortScience 42, 344–348. Schroeder, H.W., Cannon Jr., W.N., 1983. The esthetic contribution of trees to residential streets in Ohio towns. J. Arboric. 9, 237–243. Searle, S.Y., Turnbull, M.H., Boelman, N.T., Schuster, W.S.F., Yakir, D., Griffin, K.L., 2012. Urban environment of New York City promotes growth in northern red oak seedlings. Tree Physiol. 32, 389–400. Sherman, A.R., Kane, B., Autio, W.A., Harris, J.R., Ryan, H.D.P., 2016. Establishment period of street trees growing in the Boston, MA metropolitan area. Urban For. Urban Green. 19, 95–102. Struve, D.K., 1990. Root regeneration in transplanted deciduous nursery stock. Hortscience 25, 266–270. Struve, D.K., 1993. Effect of copper-treated containers on transplant survival and regrowth of four tree species. J. Environ. Hortic. 11, 196–199. Struve, D.K., Burchfield, L., Maupin, C., 2000. Survival and growth of transplanted largeand small-caliper red oaks. J. Arboric. 26, 162–169. Struve, D.K., Joly, R.J., 1992. Transplanted red oak seedlings mediate transplant shock by reducing leaf surface area and altering carbon allocation. Can. J. For. Res. 22,
establishment phase. Being able to determine for how long this program needs to persist is an important part is succeeding with tree transplanting. The results highlight that the determination of establishment depends on the used measurement methods and the chosen timeframe and that the concept of establishment can be regarded in many different ways. This confirms that the term establishment of trees needs to be more clearly defined. 5. Conclusions There are several measuring methods for determining establishment, and the results from this study indicate that these methods do not always provide the same answer to when a tree is established. One reason is that the term “establishment success” for trees has not been firmly defined. The actual aim with establishment measurements in urban environments should be to evaluate a tree’s vitality and thereby the tree’s likelihood of long-term survival. The ambition in every study of establishment is to quantify the tree’s vitality under circumstances of transplanting. From a short-term perspective, measurements of water status or nightly recovery might be better indicators of establishment because they more accurately reflect whether the trees are waterstressed or acclimated to the new growing environment compared to shoot elongation measurements. The morphological measurements seem, on the other hand, to provide the same indications on a longerterm perspective. The results from this study were based on regressions and PCA-analyses. As these methods of analysis are exploratory and may provide an overview of the area, studies of the association between the measuring methods and the establishment phenomena they attempt to quantify, must be conducted for more generalizable results. Funding This work was supported by the Swedish Farmers Foundation of Agricultural Research (SLF), the city of Malmö, the Federation of Swedish Farmers - Nursery section (GRO), and Partnerskap Alnarp – the research funding organization of the Swedish University of Agricultural Sciences (SLU). Acknowledgements This project was undertaken in collaboration with the city of Malmö and the Swedish Nursery Industry, who provided space, assistance and experience in urban tree planting projects. Dr. Jan-Eric Englund provided statistical guidance. Karin Snarf provided assistance in the field work, and the Garden Laboratory of the Swedish University of Agricultural Sciences, with Joakim Tigerschöld and Alexandra Nikolic, assisted in tree maintenance. References Akbari, H., 2002. Shade trees reduce building energy use and CO2 emission from power plants. Environ. Pollut. 116, 119–126. Beckett, K.P., Freer-Smith, P.H., Taylor, G., 2000. The capture of particulate pollution by trees at five contrasting urban sites. Arboric. J. 24, 209–230. Beeson Jr., R.C., 1994. Water relations of field-grown Quercus virginiana Mill. from preharvest through containerization and 1 year into a landscape. J. Am. Soc. Hortic. Sci. 119, 169–174. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G., Friml, J., 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602. Brouwer, R., 1983. Functional equilibrium – sense or nonsense. Neth. J. Agric. Sci. 31, 335–348. Buhler, O., Kristoffersen, P., Larsen, S.U., 2007. Growth of street trees in Copenhagen with emphasis on the effect of different establishment concepts. Arboric. Urban For. 33, 330–337. Carlson, W.C., Miller, D.E., 1990. Target seedling root-system size, hydraulic conductivity, and water-use during seedling establishment. Target Seedling Symposium: proceedings. Comb. Meet. West. For. Nurs. Assoc. 200, 53–65. Davis, A.S., Jacobs, D.F., Overton, R.P., Dumroese, R.K., 2008. Influence of irrigation method and container type on northern red oak seedling growth and media electrical
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Watson, G., Himelick, E.B., 1997. Principles and Practice of Planting Trees and Schrubs. International Society of Arboriculture, Champaign, Illinois. Williams, L.E., Araujo, F.J., 2002. Correlations among predawn leaf, midday leaf, and midday stem water potential and their correlations with other measures of soil and plant water status in Vitis vinifera. J. Am. Soc. Hortic. Sci. 127, 448–454. Woolery, P.O., Jacobs, D.F., 2014. Planting stock type and seasonality of simulated browsing affect regeneration establishment of Quercus rubra. Can. J. For. Res. 44, 732–739.
1441–1448. Summit, J., Sommer, R., 1999. Further studies of preferred tree shapes. Environ. Behav. 31, 550–576. Tranquillini, W., Havranek, W., 1970. Studies on transplanting shock in Larch. I: the growth pattern after transplanting. Zentralblatt fur das gesamte Forstwesen 87, 238–250. Turner, N.C., 1988. Measurement of plant water status by the pressure chamber technique. Irrig. Sci. 9, 289–308.
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Contents lists available at ScienceDirect
Urban Forestry & Urban Greening journal homepage: www.elsevier.com/locate/ufug
Original article
Investigating the relationship between various measuring methods for determination of establishment success of urban trees
MARK
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Anna Levinsson , Ann-Mari Fransson, Tobias Emilsson Department of Landscape Architecture, Planning and Management, Swedish University of Agricultural Sciences, Slottsvägen 5, 20353 Alnarp, Sweden
A R T I C L E I N F O
A B S T R A C T
Keywords: Establishment definition Leaf size Nightly recovery Shoot growth Shoot water potential Stomatal conductance
Establishment is a key concept in urban forestry but it is currently inconsistently defined and measured. Thus, several different methods are being used to determine establishment success but their consequences and applications are rarely discussed. With this paper we would like to stimulate an increased discussion regarding these concepts both in relation to a theoretical definition but also to their practical use. The problem was approached through an experiment using sweet cherry (Prunus avium L.) and northern red oak (Quercus rubra L.) trees and the most common methods used for determination of establishment success. The trees were studied during the first three years after transplant and the association between the different measuring methods was examined. A Principal Component Analysis showed that terminal and lateral shoot length were strongly correlated, and that midday- and pre-dawn shoot water potential, and stomatal conductance were strongly correlated. We developed an index for nightly recovery of water status, which showed that terminal shoot growth was not related to nightly recovery until the third year after transplanting. Our results suggest that successful tree establishment is determined differently depending on which method is used for determination but that the differences might decrease with time. The lack of a firm definition of the term establishment may complicate communication, both within the scientific community and in practice.
1. Introduction Although not clearly defined, the term establishment is often used to describe a tree’s status after transplanting. Within practice, successful establishment is often demanded from contractors and promised by tree nurseries. Furthermore, numerous scientific studies have set out to compare the effects of various production, planting and/or management techniques on trees’ and tree seedlings’ capacity to become fully established (e.g. Struve, 1993; Gilman and Beeson, 1996; Gilman, 2004; Ferrini and Baietto, 2006; Davis et al., 2008; Jacobs et al., 2009). There are several different approaches on how to measure establishment success. It is often determined by survival, or shoot, leaf, or stem growth (Struve and Joly, 1992; Day et al., 1995; Radoglou and Raftoyannis, 2002; Harris et al., 2008; Pinto et al., 2011; Dostalek et al., 2014; Woolery and Jacobs, 2014; Sherman et al., 2016), or the treés resumption of pre-transplant shoot or trunk growth rates (Gilman and Beeson, 1996; Struve et al., 2000). Establishment success is sometimes determined by measurements of physiological attributes such as hydraulic conductivity or water potential (Carlson and Miller, 1990; Beeson 1994), or through a combination of both physiological and morphological attributes (Harris and Gilman, 1993; Lauderdale et al.,
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1995; Gilman et al., 1998). Gilman et al. (1998) used both growth and water potential measurements in a post-transplant study of trees exposed to different irrigation volumes, but the conclusions on establishment success were based on stem and height growth. In another study, Harris and Gilman (1993) based their conclusions regarding tree establishment success on both physiological and morphological determinations. Struve et al. (2000) considered trees established once they showed no signs of drought stress even under mild drought, and thus concluded that they did not need further irrigation. Struve (1990) has mentioned that there is no workable definition of the term establishment. As a consequence, establishment is defined, and measured, in different ways. It can be seen as a biological process (Rietveld, 1989) during which the transplanted tree becomes fully connected to the hydrologic cycle of the growing site (Grossnickle, 2005). It has been suggested that an urban tree might be considered established when it does not need further irrigation (Day and Harris, 2007), a definiton that is only applicable to trees that are being irrigated. However, it is unclear exactly when a transplanted tree is fully coupled to the hydrologic cycle and no longer needs further irrigation, and several methods for determining the water status during the establishment process are being used. A tree may also be considered
Corresponding author. E-mail address: [email protected] (A. Levinsson).
http://dx.doi.org/10.1016/j.ufug.2017.09.014 Received 19 January 2017; Received in revised form 21 September 2017; Accepted 26 September 2017 Available online 28 September 2017 1618-8667/ © 2017 Published by Elsevier GmbH.
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program during the first two post-transplant years of the study. They were irrigated approximately every second week. All trees were planted at the same depth with the root collar at the soil surface, in a threemetre-wide grass strip, alongside a street in a high-rise residential area. They were irregularly planted with a minimum distance of four metres. A one metre in diameter circle around the trees was covered with smallsized gravel to reduce grass competition. At Alnarp, the trees were planted in a field, with 4.5 metres between each tree in every direction. The soil was covered with a single layer of black polypropylene ground cloth (Mypex®) to inhibit weed growth. A drip-irrigation system was installed where the hose made a circle around each tree at the perimeter of the root ball to ensure that water was available for the planted root mass. The plant water availability was determined regularly using an HH2 moisture meter (Delta T Devices Ltd., Cambridge, UK) at 10, 20, 30 and 40 cm depths to ensure that the trees were never drought stressed during the two following growing seasons. The probes for the moisture meter were installed just beyond the planting zone, with controls installed in to the root balls of the air-potted and root control bag cultivated trees, as the growth substrate in these root balls varied substantially from the texture of the sandy loam at the experimental fields. Irrigation permitted the soil water content to remain near field capacity or just below. No tree at either site received any irrigation during the third year of the study and none of the trees were given additional nutrients.
established when it reaches a productive phase, that is, when it starts fulfilling the purpose for which it was planted (Day and Harris, 2007); this definition is based upon a functionality perspective rather than a biological one. For an urban tree, the purpose of planting is connected to the expected environmental and aesthetic benefits associated with urban forests (Schroeder and Cannon, 1983; Akbari, 2002; Nowak and Crane, 2002; Saebo et al., 2012). Significant growth and high crown density may thus be considered necessary attributes for an urban tree to be considered as established, leading to determination of establishment success being based on morphological characteristics rather than physiology (Summit and Sommer, 1999; Day and Harris, 2007). The aim of our study was to highlight how differently the concept of establishment has been approached in the field of urban forestry and what effect the approach has on determinations of establishment success. We did this by comparing the relationship between different methods for measuring establishment, both morphological and physiological. We analysed data from two commonly used urban tree species during the three consecutive years directly after planting. The analyses were performed on trees exposed to different post-transplant management regimes to allow for general validity. We compared measurements of midday and pre-dawn shoot water potential, stomatal conductance, terminal and lateral shoot growth, leaf area, and survival, all of which are commonly studied attributes in determinations of establishment. Measurements were performed to capture both seasonal and annual changes throughout the study. We also calculated a nightly recovery index, as a value for water status including both midday- and pre-dawn status.
2.2. Determinations Measurements were performed during the three seasons after transplanting (Table 1). Midday shoot water potentials (Ψm) were determined between 11.30 am and 16.00 pm and pre-dawn shoot water potentials (Ψpd) were determined the following day approximately one hour before sunrise. The time of the pre-dawn measurements varied over the season, depending on the time of sunrise. The determinations were performed with a three-week interval, except when bad weather prevented measurements and measurements had to be postponed. A pilot study showed that there were very small differences in shoot water potential within each tree, allowing us to use a single shoot from each tree at each occasion. Two to three cm of the shoot tip was cut off from a branch at the middle height of the crown and immediately installed in a pressure chamber (Model 1000, PMS Instrument Company, OR, USA). Pressure was increased in the chamber at a constant rate of 0.05 MPa/s (Turner, 1988). Before cutting the shoot for the water potential determination, leaf stomatal conductance (gs) was determined on two fully sun-exposed leaves on each shoot during the daytime measurements. Conductance was determined each year after transplanting using a leaf porometer (model SC-1, Decagon Devices, Pullman, WA, USA). Shoot elongation measurements were performed each season, after shoot elongation cessation. Both species grew with one flush per year. Two terminal and two lateral shoots in the south, the north, the east, and the west, from the middle height of the crown were measured. To reduce the impact of removing mature leaves from the small trees in 2007, leaf size was determined by measuring the leaves that had grown on the shoots cut off for water potential measurements. Three leaves on each shoot (the first, third, and fourth leaf, counting from the shoot tip) were scanned within one day after they had been sampled from the tree, with a total of nine leaves per season. Leaf size was analysed using ImageJ (http://imagej.nhi.gov/ij version 1.4.3.67, Broken symmetry software, USA). For determinations of survival, all trees were revisited in 2013 and the status of each tree was assessed as good, in decline or dead. Examples of signs of decline were dead main branches, low crown density, and/or discolouration.
2. Materials and Methods 2.1. Trees and study site In this study, 50 trees of Prunus avium and 50 trees of Quercus rubra, were used. They originated from two nurseries, situated in the south of Sweden. All trees within the same species came from the same nursery and they were selected early in the spring of 2007, before growth had started. All trees within a species originated from the same seed source, and they had been treated according to Swedish standards for field cultivation of trees until the start of the study (LRF, 2012). Their selection was based on stem circumference and general appearance, with the intention of choosing as uniform plant material as possible. Stem circumference was 14–17 cm at one metre above the root collar (standard measuring procedure in the Swedish nursery industry) and the nine-year-old trees were about four metres tall. They were randomly assigned one of five different root treatments – root pruning, barerooted, balled and burlapped, spring-ring cultivation (Superoots® plastic, The Caledonian tree Co., Edinburgh, UK), forming an Air-Pot® and root control bag cultivation in in-ground fabric container (Smart Pot®, High Caliper, OK, USA), as described in a parallel paper (Levinsson et al., 2014). The trees were then treated according to standard procedures for the assigned production system during the last growing season before transplanting (LRF, 2012). The production systems of urban trees can be seen as an integrated result of several production variables such as e.g. container design/root treatment, irrigation, and substrate/soil. Each treatment included 10 trees of each species. The bare-rooted and the balled and burlapped trees were left undisturbed in the field, and the root-pruned trees were pruned without being removed from their growing spots. For the two other treatments, the trees were harvested and the treatments were carried out at two different nurseries specialising in the particular production system. The trees were kept in the nurseries until the spring of 2008, when they were transplanted at two different sites; in the city of Malmö and in the experimental fields at the campus of the Swedish University of Agricultural Sciences, Alnarp. Four trees of each species and production system were planted in the city of Malmö and the trees were managed by the municipality and included in their establishment management
2.3. Statistical analyses Principal Component Analyses (PCA) were performed using R (version 2.15, R development Core team, 2014) running the 22
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Table 1 Mean values with SE of all parameters included in the analyses. The number of measuring occasions varied over the years, depending on weather conditions and the length of the growing season. Water potential determinations were performed on fully developed shoots. Quercus rubra
Water potential (MPa)
Stomatal conductance (mmol m−2 s−1)
Annual shoot growth (cm) Leaf size (cm2) Prunus avium Water potential (MPa)
Stomatal conductance (mmol m−2 s−1)
Annual shoot growth (cm) Leaf size (cm)
Year 2008
2009
2010
Midday, per occasion
−1.37 ± 0.06; −1.54 ± 0.07; −1.31 ± 0.09
Annual mean Pre−dawn
−1.40 −0.48 −0.64 −0.35
Annual mean Midday
−0.49 ± 0.04 117.6 ± 13.7; 89.8 ± 11.6; 308.9 ± 26.9
Annual mean Terminal Lateral
172.1 ± 13.4 12.70 ± 1.03 5.75 ± 0.50 53.60 ± 3.84
−1.3 ± 0.06; −1.36 ± 0.07; −1,52 ± 0.09; −1.44 ± 0.05; −1.70 ± 0.09 −1.43 ± 0.03 −0.43 ± 0.07; −0.53 ± 0.07; −0.66 ± 0.11; −0.29 ± 0.05; −0.56 ± 0.08 −0.49 ± 0.03 247.9 ± 25.8; 323.9 ± 28.3; 346.6 ± 36.3; 438.6 ± 25.4; 516.3 ± 46.5 374.5 ± 16.0 8.36 ± 0.93 4.88 ± 0.62 67.16 ± 3.07
−0.95 ± 0.03; −1.68 ± 0.08; −2.16 ± 0.17; −1.17 ± 0.05; −1.22 ± 0.07 −1.44 ± 0.04 −0.22 ± 0.03; −0.63 ± 0.09; −1.05 ± 0.15; −0.15 ± 0.03; −0.41 ± 0.02 −0.49 ± 0.04 312.0 ± 14.5; 196.3 ± 10.9; 176.1 ± 16.8; 801.8 ± 48.1; 722.9 ± 45.7 441.8 ± 22.1 7.62 ± 0.58 3.75 ± 0.37 90.45 ± 4.45
Midday, per occasion
−1.10 ± 0.04; −1.74 ± 0.07; −1.41 ± 0.06
−2.21 ± 0.05; −1.30 ± 0.03; −1.29 ± 0.06
Annual mean Pre-dawn
−1.41 −0.35 −0.60 −0.31
Annual mean Midday
−0.41 ± 0.03 124.6 ± 15.1; 173.4 ± 15.0; 653.3 ± 47.4
Annual mean Terminal Lateral
318.4 ± 26.3 11.95 ± 1.08 4.39 ± 0.63 25.49 ± 1.01
−1.41 ± 0.06; −1.61 ± 0.09; −1.65 ± .09; −1.49 ± 0.04; −1.81 ± 0.08 −1.60 ± 0.03 −0.44 ± 0.05; −0,63 ± 0.05; −0.68 ± 0.07; −0.45 ± 0.01; −0.71 ± 0.05 −0.50 ± 0.02 358.2 ± 37.2; 501.4 ± 37.5; 491.7 ± 43.6; 706.6 ± 39.5; 664.6 ± 50.6 544.5 ± 20.3 9.07 ± 0.94 2.12 ± 0.48 39.62 ± 1.05
± ± ± ±
± ± ± ±
0.04 0.06; 0.09; 0.07
0.04 0.03; 0.06; 0.04
−1.60 −0.79 −0.24 −0.61
± ± ± ±
0.05 0.07; 0.04; 0.02
−0.55 ± 0.03 232.5 ± 19.1; 1178.9 ± 57.4; 1164.7 ± 61.7
858.7 ± 46.5 34.1 ± 2.34 19.44 ± 2.55 40.78 ± 1.54
and pre-dawn shoot water potential were analysed using annual, species-specific linear regressions. The linear regression analyses were performed using Minitab 17 Statistical Software (2014) for Windows (Minitab, Inc., State College, PA, USA).
FactoMineR package (Le et al., 2008). The PCA was based on the correlation matrix and calculated on Euclidean distances. It was performed individually on Quercus rubra and Prunus avium respectively. Ψ m, Ψpd, gs, leaf size, terminal and lateral shoot length and year were used as main variables. Production system and site were included as supplementary parameters. To study the trees’ nightly recovery (NR) ability and how recovery was related to other measures of establishment, a recovery index was developed from the difference between midday and pre-dawn shoot water potential, as a proportion of the midday shoot water potential, as:
3. Results The shoot water potential showed seasonal fluctuations (Table 1). Increasing stomatal conductance and leaf sizes over time were clear in both species. PCA for Quercus rubra and Prunus avium revealed a similar relationship between variables (Figs. 1 and 2 respectively). For both species, a large proportion of the variation was captured by the first two PCA axes. The first axis corresponded to 35.8% of the total variation in the Q. rubra dataset (Table 2). The axis was found to be significantly correlated as well as having high cos2 values for Ψm, Ψpd, and gs. Leaf size also correlated to the first axis but with a slightly lower cos2 value. The second axis explained 29% of the total variation. The axis was found to be significantly correlated as well as having high cos2 values for terminal and lateral shoot growth, and year.
NR = (Ψm − Ψpd)/Ψm. Ψm = midday shoot water potential, Ψpd = pre-dawn shoot water potential. The nightly recovery rate was calculated for each measuring occasion. A seasonal mean was calculated for each tree and used as a response variable in year- and species-specific multiple regressions, with terminal and lateral shoot length, stomatal conductance and leaf size as predictors. The variations over years in the relation between midday
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The PCA for P. avium revealed that the first axis corresponded to 38.2% of the total variation. This axis was found to be significantly correlated as well as having high cos2 values for terminal and lateral shoot growth, and year. Leaf size was also correlated to the first axis but with a slightly lower cos2 value. The second axis was found to be significantly correlated as well as having high cos2 values for Ψm, Ψpd, and gs. The second axis explained 29% of the total variation (Table 2). 3.1. Shoot water potentials and nightly recovery The two species showed similar patterns over the years in how the seasonal mean NR was related to the predictors in the multiple regressions (Table 3). NR was related to stomatal conductance of the preceding day during all three years after transplanting for both species. Leaf size was related to NR in 2008 for Q. rubra, and in 2010 for both species. In 2010, terminal shoot length was also related to the NR for both species. There was a strong relationship between pre-dawn and midday measurements of shoot water potential for both species during all years of measurements (p < 0.001, across all occasions, Table 4). However, the relationship strength increased with each year following transplant. The tendency was the same for both species.
Fig. 1. Output of PCA for Quercus rubra, including measurements from the three first posttransplant years. Abbreviations in the figure: ψPD = pre-dawn shoot water potential; ψM = midday shoot water potential; SGT = terminal shoot growth; SGL = lateral shoot growth; gs = stomatal conductance; LS = leaf size; and Y = year.
3.2. Survival The survival of the trees was high; only one bare-rooted Q. rubra tree died during the year after planting in Malmö. Another Q. rubra had died and two showed signs of decline at the visual inspection in 2013. When examining data from 2008, 2009, and 2010 for these trees, no differences in nightly recovery were found between these trees and the other. 4. Discussion The results from this study indicate that determination of tree establishment may depend on the choice of measuring method. Assessments of either shoot length or water status are commonly used to determine tree establishment (Beeson, 1994; Day et al., 1995; Buhler et al., 2007) yet for both species studied, PCA showed that shoot elongation and water status are not correlated in the first few years following transplant. Shoot length is often reduced after transplanting compared to pre-transplant growth, and our results indicate that shoot length does not indicate whether the tree is water stressed or acclimated. Brouwer (1983) has described the functional equilibrium, claiming that either roots or shoots are limiting growth at any given time, since shoots are dependent on uptake from roots for development, and roots depend upon carbohydrates produced primarily by the leaves for their development (Brouwer, 1983). A model by Watson and Himelick (1997) shows that a period of reduced growth is expected after transplant and that establishment has occurred once shoot elongation has resumed to pre-transplant rates. But, restricted shoot growth and
Fig. 2. Output of PCA for Prunus avium, including measurements from the three first posttransplant years. Abbreviations in the figure: ψPD = pre-dawn shoot water potential; ψM = midday shoot water potential; SGT = terminal shoot growth; SGL = lateral shoot growth; gs = stomatal conductance; LS = leaf size; and Y = year.
Table 2 PCA summary of statistics for measured tree performance variables in Quercus rubra and Prunus avium during 2008–2010. The table shows summary statistics for correlation between PCA scores and original values (Corr, p < 0.05, non-significant values are omitted) and cosine2 (cos2: values above 0.45 in bold) between principal components and measurement variables. Ψm – midday shoot water potential, Ψpd – pre-dawn shoot water potential, gs – stomatal conductance, SGT – terminal shoot growth, SGL – lateral shoot growth, LS – leaf size, Y – year, Ssite, and PS – production systems. Species
PC
EV
% expl.
Ψm
Ψpd
gs
SGT
SGL
LS
Y
S
PS
Corr
cos2
Corr
cos2
Corr
cos2
Corr
cos2
Corr
cos2
Corr
cos2
Corr
cos2
R2
R2
0.84
0.71 < 0.01
0.67 0.29
0.45 0.09
0.37 0.83
0.14 0.70
0.45 0.77
0.20 0.59
0.56 0.41
0.32 0.17
0.16 0.71
0.03 0.50
0.40
0.02 0.10
< 0.01 0.78
0.55 0.55
0.30 0.30
0.84 0.19
0.70 0.04
0.81
0.66 < 0.01
0.63
0.40 < 0.01
0.77 0.23
0.60 0.05
0.05 0.34
Q. rubra
1 2
2.51 2.05
35.88 29.28
0.82 0.10
0.67 < 0.01
P. avium
1 2
2.68 2.02
38.24 28.84
0.12 0.92
0.01 0.84
0.88
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of the root/shoot balance, regardless of if one sees establishment from a biological or functional perspective. The use of shoot water potential measurements in studies of establishment is well reported. Several protocols are available, and measurements of midday shoot water potentials in transplanted trees have been compared to shoot water potentials in similar non-transplanted trees, and to pre-dawn potentials in the same trees, and between stressed and unstressed transplanted trees (Beeson, 1994; Montague et al., 2000; Scheiber et al., 2007; Levinsson et al., 2014). As there are no absolute values as to when water potential measurements indicate establishment, and because it is complex finding appropriate reference trees, assessments of establishment status by water potential measurements are often done as comparative studies. In this study, we used the midday and pre-dawn shoot water potential measurements to calculate a recovery index. The recovery index incorporates both midday water status and the trees’ ability to regain nightly equilibrium with soil water potential (Resco et al., 2008), and it reduces pre-dawn and midday measurements to one value, so that water status could be compared with other measuring methods used for determining establishment. In the present study, it was used to compare water status with growth, and the possibility to investigate the strength of the relationship between water status and shot elongation might provide valuable information of a treés process in becoming established. The absence of absolute values for either of the measuring methods to indicate establishment success may make such a comparison even more valuable. Williams and Araujo (2002) found a strong relationship between pre-dawn and midday leaf water potentials in vines grown in a 9-yearold vineyard. The strength of the relation between midday and predawn shoot water potentials increased with time in the present study. This increase in strength may be seen as the result of improved coupling to the hydrologic cycle of the site and thus, an indication of establishment. It has been shown that there are differences both in growth and water flow between terminal and lateral shoots (Joyce and Steiner, 1995). A study on transplant shock in Larix decidua showed that the lateral shoot growth was less affected by transplanting than the terminal (Tranquillini and Havranek, 1970). In our study, there was a strong correlation between terminal and lateral shoot growth during all years, showing no indications that either would be more relevant for establishment measurements of the two investigated species, despite our expectations. Determinations of water potential and measurements of shoot growth were both performed during the second part of the growing season since shoot water potential could only be determined on shoots that were fully developed. However, unlike the shoot water potential determinations, shoot growth measurements reflect the conditions that were prevalent during the first part of the growing season, when shoot elongation occurred. Thus, the two methods of measurement do not study the same time period, with the possibility that conditions might have changed from the early growing season’s period of shoot elongation to the later period of shoot water potential measurements. Such results have been shown in a drought-stress test, studying both physiological and morphological responses to drought (Fotelli et al., 2000). Nonetheless, it might be preferable if indications for establishment success could be measured at any point throughout the season, regardless of temporary circumstances. The establishment of the trees in our study could be seen as very good after the first year if evaluated by survival, as it sometimes is (Radoglou and Raftoyannis, 2002 Löf et al., 2004). However, survival might not be a relevant determination of establishment for trees planted in urban areas, as a declining tree, while surviving, would not fulfil the expected ecosystem services and probably cause a disagreement between contractor and municipality. Furthermore, it is unclear how long after transplanting survival should be assessed. In urban tree management there is often an establishment program, in which the newly planted trees are given extra irrigation during the
Table 3 Annual relevant predictors of mean seasonal nightly recovery (NR) in urban and fieldplanted trees analysed in a multiple regression, using NR as the response variable. Pvalues are included next to the significant predictor. Year
Quercus rubra
Prunus avium
Significant predictor
R2-values
Significant predictor
R2-values
2008
Conductance 0.0083 Leaf size 0.0076
0.39
Conductance < 0.0001
0.34
2009
Conductance < 0.0001
0.66
Conductance < 0.0001
0.59
2010
Conductance < 0.0001 Leaf size 0.011 Terminal growth 0.023
0.77
Conductance < 0.0001 Leaf size 0.030 Terminal growth 0.012
0.72
Table 4 The mean annual shoot water potentials for each species and the level of explanation of the variation in the mean annual midday (Ψm) and pre-dawn (Ψpd,) shoot water potentials for both species during the three first years after transplanting. Regression analyses are based on seasonal mean per individual tree. P < 0.001, at every occasion. Year
2008 2009 2010
Quercus rubra
Prunus avium
Ψm
Ψpd,
R2
Ψm
Ψpd
R2
−1.31 −1.52 −2.16
−0.35 −0.66 −1.04
0.60 0.82 0.93
−1.41 −1.65 −2.21
−0.30 −0.68 −0.79
0.38 0.81 0.83
allocation of nutrients and photsynthates to the root system might merely be a response to changed environmental conditions and is not necessarily connected to a treés potential incapability to absorb the root-available water at a new growing site, making the model by Watson and Himelick (1997) primarily applicable if considering establishment from a functional perspective. The model does not provide information on whether the tree is connected to the hydrologic cycle of the site. Plants are known to constantly change their development in response to changing external signals (Benkova et al., 2003). However, if resources are strongly limited at the new growing site, as they may be in an urban growing site, shoot elongation might never regain pretransplant levels, and could not be expected to. Although clearly related, biological and functional perspectives of establishment provide different approaches to the concept of establishment determinations. If tree establishment is regarded as a question of functionality rather than biology and one considers a tree to be established once it has reached its productive phase (Day and Harris, 2007), growth is indeed important since the productive phase for urban trees can be associated with the point when it meets the objectives for which it was planted. Benefits associated with urban trees, such as particle uptake rate, shading, carbon sequestration and aesthetic experience, increase with canopy size (Schroeder and Cannon, 1983; Summit and Sommer, 1999; Beckett et al., 2000; Escobedo and Nowak, 2009; Saebo et al., 2012; Searle et al., 2012). However, if instead one considers a tree established when it is coupled to the hydrologic cycle of the site (Grossnickle, 2005), then our results suggest that determinations of shoot length might not provide the pertinent information, since shoot length and water status determinations were not correlated in the PCA. Nonetheless, NR was related to terminal shoot growth in the third season after transplanting. This relation indicates that the trees had restored a functional root system for above-ground growth permitting shoot growth and that the shoot elongation then might be used as a proxy of the water status of the tree. Provided that the conditions at the new growing site permit shoot elongation values close to pre-transplant values, then measures of water status and growth might provide the same indications of establishment success after a period of restoration 25
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conductivity. Native Plants J. 9, 4–13. Day, S.D., Bassuk, N.L., Es, H.V., 1995. Effects of four compaction remediation methods for landscape trees on soil aeration, mechanical impedance and tree establishment. J. Environ. Hortic. 13, 64–71. Day, S.D., Harris, J.R., 2007. Fertilization of red maple (Acer rubrum) and littleleaf linden (Tilia cordata) trees at recommended rates does not aid tree establishment. Arboric. Urban For. 33, 113–121. Dostalek, J., Weber, M., Frantik, T., 2014. Establishing windbreaks: how rapidly do the smaller tree transplants reach the height of the larger ones? J. For. Sci. (Prague) 60, 12–17. Escobedo, F.J., Nowak, D.J., 2009. Spatial heterogeneity and air pollution removal by an urban forest. Landsc. Urban Plan. 90, 102–110. Ferrini, F., Baietto, M., 2006. Response to fertilization of different tree species in the urban environment. Arboric. Urban For. 32, 93–99. Fotelli, M.N., Radoglou, K.M., Constantinidou, H.I.A., 2000. 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Federation of Swedish Farmers (LRF). Retrieved June 14, 2013 from http://www.lrf. se/PageFiles/98759/Kvalitetsregler%20slutgiltig.pdf. Löf, M., Thomsen, A., Madsen, P., 2004. Sowing and transplanting of broadleaves (Fagus sylvatica L., Quercus robur L., Prunus avium L. and Crataegues monogyna Jacq.) for afforestation of farmland. For. Ecol. Manag. 188, 113–123. Montague, T., Kjelgren, R., Rupp, L., 2000. Surface energy balance affects gas exchange and growth of two irrigated landscape tree species in an arid climate. J. Am. Soc. Hortic. Sci. 125, 299–309. Nowak, D.J., Crane, D.E., 2002. Carbon storage and sequestration by urban trees in the USA. Environ. Pollut. 116, 381–389. Pinto, J.R., Marshall, J.D., Dumroese, R.K., Davis, A.S., Cobos, D.R., 2011. Establishment and growth of container seedlings for reforestation: a function of stocktype and edaphic conditions. For. Ecol. Manag. 261, 1876–1884. Radoglou, K., Raftoyannis, Y., 2002. The impact of storage, desiccation and planting date on seedling quality and survival of woody plant species. Forestry 75, 179–190. Resco, V., Ignace, D.D., Sun, W., Huxman, T.E., Weltzin, J.F., Williams, D.G., 2008. Chlorophyll fluorescence, predawn water potential and photosynthesis in precipitation pulse-driven ecosystems – implications for ecological studies. Funct. Ecol. 22, 479–483. Rietveld, W.J., 1989. Transplanting stress in bareroot conifer seedlings; its development and progression to establishment. North. J. Appl. For. 6, 99–107. Saebo, A., Popek, R., Nawrot, B., Hanslin, H.M., Gawronska, H., Gawronski, S.W., 2012. Plant species differences in particulate matter accumulation on leaf surfaces. Sci. Total Environ. 427, 347–354. Scheiber, S.M., Gilman, E.F., Paz, M., Moore, K.A., 2007. Irrigation affects landscape establishment of burford holly, Pittosporum, and sweet viburnum. HortScience 42, 344–348. Schroeder, H.W., Cannon Jr., W.N., 1983. 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establishment phase. Being able to determine for how long this program needs to persist is an important part is succeeding with tree transplanting. The results highlight that the determination of establishment depends on the used measurement methods and the chosen timeframe and that the concept of establishment can be regarded in many different ways. This confirms that the term establishment of trees needs to be more clearly defined. 5. Conclusions There are several measuring methods for determining establishment, and the results from this study indicate that these methods do not always provide the same answer to when a tree is established. One reason is that the term “establishment success” for trees has not been firmly defined. The actual aim with establishment measurements in urban environments should be to evaluate a tree’s vitality and thereby the tree’s likelihood of long-term survival. The ambition in every study of establishment is to quantify the tree’s vitality under circumstances of transplanting. From a short-term perspective, measurements of water status or nightly recovery might be better indicators of establishment because they more accurately reflect whether the trees are waterstressed or acclimated to the new growing environment compared to shoot elongation measurements. The morphological measurements seem, on the other hand, to provide the same indications on a longerterm perspective. The results from this study were based on regressions and PCA-analyses. As these methods of analysis are exploratory and may provide an overview of the area, studies of the association between the measuring methods and the establishment phenomena they attempt to quantify, must be conducted for more generalizable results. Funding This work was supported by the Swedish Farmers Foundation of Agricultural Research (SLF), the city of Malmö, the Federation of Swedish Farmers - Nursery section (GRO), and Partnerskap Alnarp – the research funding organization of the Swedish University of Agricultural Sciences (SLU). Acknowledgements This project was undertaken in collaboration with the city of Malmö and the Swedish Nursery Industry, who provided space, assistance and experience in urban tree planting projects. Dr. Jan-Eric Englund provided statistical guidance. Karin Snarf provided assistance in the field work, and the Garden Laboratory of the Swedish University of Agricultural Sciences, with Joakim Tigerschöld and Alexandra Nikolic, assisted in tree maintenance. References Akbari, H., 2002. Shade trees reduce building energy use and CO2 emission from power plants. Environ. Pollut. 116, 119–126. Beckett, K.P., Freer-Smith, P.H., Taylor, G., 2000. The capture of particulate pollution by trees at five contrasting urban sites. Arboric. J. 24, 209–230. Beeson Jr., R.C., 1994. Water relations of field-grown Quercus virginiana Mill. from preharvest through containerization and 1 year into a landscape. J. Am. Soc. Hortic. Sci. 119, 169–174. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G., Friml, J., 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602. Brouwer, R., 1983. Functional equilibrium – sense or nonsense. Neth. J. Agric. Sci. 31, 335–348. Buhler, O., Kristoffersen, P., Larsen, S.U., 2007. Growth of street trees in Copenhagen with emphasis on the effect of different establishment concepts. Arboric. Urban For. 33, 330–337. Carlson, W.C., Miller, D.E., 1990. Target seedling root-system size, hydraulic conductivity, and water-use during seedling establishment. Target Seedling Symposium: proceedings. Comb. Meet. West. For. Nurs. Assoc. 200, 53–65. Davis, A.S., Jacobs, D.F., Overton, R.P., Dumroese, R.K., 2008. Influence of irrigation method and container type on northern red oak seedling growth and media electrical
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Watson, G., Himelick, E.B., 1997. Principles and Practice of Planting Trees and Schrubs. International Society of Arboriculture, Champaign, Illinois. Williams, L.E., Araujo, F.J., 2002. Correlations among predawn leaf, midday leaf, and midday stem water potential and their correlations with other measures of soil and plant water status in Vitis vinifera. J. Am. Soc. Hortic. Sci. 127, 448–454. Woolery, P.O., Jacobs, D.F., 2014. Planting stock type and seasonality of simulated browsing affect regeneration establishment of Quercus rubra. Can. J. For. Res. 44, 732–739.
1441–1448. Summit, J., Sommer, R., 1999. Further studies of preferred tree shapes. Environ. Behav. 31, 550–576. Tranquillini, W., Havranek, W., 1970. Studies on transplanting shock in Larch. I: the growth pattern after transplanting. Zentralblatt fur das gesamte Forstwesen 87, 238–250. Turner, N.C., 1988. Measurement of plant water status by the pressure chamber technique. Irrig. Sci. 9, 289–308.
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