Tree Physiology 34, 10561068

doi:10.1093/treephys/tpu086

Research paper

Responses of gas-exchange rates and water relations to annual

fluctuations of weather in three species of urban street trees
Yoko Osone1,2,9, Satoko Kawarasaki2, Atsushi Ishida3, Satoshi Kikuchi4, Akari Shimizu1,
Kenichi Yazaki4, Shin-ichi Aikawa4,5, Masahiro Yamaguchi6,7, Takeshi Izuta8 and Genki I. Matsumoto1

Downloaded from http://treephys.oxfordjournals.org/ at New York University on April 20, 2015

1School of Social Information Studies, Otsuma Women's University, 2-7-1 Karakida, Tama, Tokyo 206-8540, Japan; 2Department of Biological Sciences, Graduate School
ofScience and Engineering, Tokyo Metropolitan University, Minamiosawa 1-1, Hachioji, Tokyo 192-0397, Japan; 3Center for Ecological Research, Kyoto University,
2-509-3 Hirano, Otsu, Shiga 520-2113, Japan; 4Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba 305-8687, Japan; 5Japan Forest Technology
Association, Chiyoda, Tokyo 102-0085, Japan; 6Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-8509, Japan; 7Graduate
School of Fisheries Science and Environmental Studies, Nagasaki University, Nagasaki 852-8521, Japan; 8Institute of Agriculture, Tokyo University of Agriculture and
Technology, Fuchu, Tokyo 183-8509, Japan; 9Corresponding author (osone.yk@gmail.com)

Received June 4, 2014; accepted September 16, 2014; published online November 11, 2014; handling Editor Marc Abrams

The frequency of extreme weather has been rising in recent years. A 3-year study of street trees was undertaken in Tokyo to
determine whether: (i) street trees suffer from severe water stress in unusually hot summer; (ii) species respond differently to
such climatic fluctuations; and (iii) street trees are also affected by nitrogen (N) deficiency, photoinhibition and aerosol pol-
lution. During the study period (201012), midsummers of 2010 and 2012 were unusually hot (2.42.8C higher maximum
temperature than the long-term mean) and dry (656% precipitation of the mean). In all species, street trees exhibited sub-
stantially decreased photosynthetic rate in the extremely hot summer in 2012 compared with the average summer in 2011.
However, because of a more conservative stomatal regulation (stomatal closure at higher leaf water potential) in the hot sum-
mer, apparent symptoms of hydraulic failure were not observed in street trees even in 2012. Compared with Prunusyedoen-
sis and Zelkova serrata, Ginkgo biloba, a gymnosperm, was high in stomatal conductance and midday leaf water potential even
under street conditions in the unusually hot summer, suggesting that the species had higher drought resistance than the other
species and was less susceptible to urban street conditions. This lower susceptibility might be ascribed to the combination of
higher soil-to-leaf hydraulic conductance and more conservative water use. Aside from meteorological conditions, N deficiency
affected street trees significantly, whereas photoinhibition and aerosol pollution had little effect. The internal CO2 and 13C
suggested that both water and N limited the net photosynthetic rate of street trees simultaneously, but water was more limit-
ing. From these results, we concluded that the potential risk of hydraulic failure caused by climatic extremes could be low in
urban street trees in temperate regions. However, the size of the safety margin might be different between species.

Keywords: carbon isotopes, extreme weather, photosynthesis, roadside trees, stomatal conductance, summer heat,
waterpotential.

Introduction etal. 2006). Even in regions with abundant natural precipitation,

extreme weather, such as intense heat in summer, causes tran-
Extreme meteorological events have rapid and widespread sient water deficits. Since plants adapted to mesic environments
impacts on the composition and productivity of vegetation are more sensitive to drought than plants adapted to xeric envi-
(Allen and Breshears 1998, Hanson and Weltzin 2000, Berg ronments (Volaire et al. 1998, Sack 2004, Engelbrecht et al.

The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com

2005), they may be affected more severely by these transient
water deficits. In mesic regions, the effects of extreme weather
may appear most prominently in urban areas where plants are
exposed to high temperature and low relative humidity caused
by heat island effects. Increasing evidence suggests that urban
greening areas play more important roles in ecosystem services
than previously expected. For example, they provide habitats
for a wide array of wildlife, mitigate the effects of heat islands
and may act as local carbon sinks (Nowak 1993, Ditchkoff et al.
2006, Rizwan et al. 2008, Niemel et al. 2010). To make urban
greening area fully perform these functions, an understanding
of the in situ physiological status of plants is required.
The hypothetical scenario for water stress in urban trees holds
that both limited water supply and excessive water demand pre-
vail in the urban environment (Whitlow et al. 1992). Water supply
to roots is decreased because paving and compacted soil prevent
percolation into the root zone. Access to ground water is often
prevented by underground obstacles. On the other hand, atmo-
spheric demand is increased because elevated temperatures and
lower humidities accentuate vapour pressure deficits. If the evap-
orative demand exceeds the water supply, strong negative tension
is imposed on the xylem and the probability of xylem cavitation
increases (e.g., Blizzard and Boyer 1980, Sperry 2000). To avoid
such hydraulic failure, plants usually decrease stomatal conduc-
tance and reduce water loss from leaves in response to water
deficits (Meinzer et al. 1992, Sperry et al. 1993). However, this
is at the expense of diminished photosynthetic rates and thereby
the increased risk of photoinhibition (Damesin and Rambal 1995,
Ishida et al. 1999, 2006, Martnez-Ferri et al. 2000).
Urban street trees may also be subject to other stress fac-
tors. One of those is nitrogen (N) deficiency caused by litter
removal and reduced microbial activity in the compacted soil
(Pulford 1991, Craul 1999, Harris et al. 2004, Scharenbroch
and Lloyd 2004). By reducing the amount of photosynthetic
enzymes, N deficiency may result in the diminished growth
and increased risk of photoinhibition in street trees (Warren
etal. 2003, Osone and Tateno 2005). In addition, aerosol par-
ticles such as sulphates and black carbon in diesel exhaust
may affect street trees. Aerosol particles could interfere with
normal gas exchange if deposited into the stomata, and may
dissolve the epicuticular wax of leaf surfaces which promotes
evaporation from leaf surfaces (Hirano et al. 1991, Burkhardt
et al. 2001). Although these factors are thought to affect urban
plants, the direct evidence is largely absent.
Responses to these stresses will be species specific. Species
selection in urban greening is generally empirical and its physi-
ological basis is unknown. Therefore, it is possible that some
species may operate narrowly on the edge of survival during
unusual weather while others may thrive with a large margin
of safety. For example, gymnosperms and angiosperms, which
have fundamental differences in habitats, xylem structure and
water-use strategy (e.g., Tyree et al. 1994, Pittermann et al.
The effects of summer heat on urban street trees1057
2006, Sperry et al. 2006, Brodribb et al. 2012, Choat et al.
2012), are expected to respond differently to water deficits
during unusual summer heat.
In the present study, we explored the species and annual
patterns of in situ physiological status of urban street trees.
For this purpose, we performed a 3-year study from 2010 to
2012 on three typical street tree species in Japan including
two angiosperms and one gymnosperm. The midsummers of
2010 and 2012 were extremely hot and dry with the highest
and the second highest average temperatures on record and
much less rainfall than average, while the midsummer of 2011
was mild with average temperatures and greater than average
seasonal rainfall. Three specific questions to be addressed are:
(i) Do street trees suffer from severe water stress in unusu-
Downloaded from http://treephys.oxfordjournals.org/ at New York University on April 20, 2015
ally hot summers?
(ii)Do species respond differently to climatic fluctuations?
(iii)Are street trees also influenced by N deficiency, photoinhi-
bition and air pollution?
Materials and methods
Tree species and study sites
Three tall tree species, including two angiosperms, Prunus
yedoensis Matsumura and Zelkova serrata (Thumb.) Makino, and
one gymnosperm, Ginkgo biloba L., were used in the present
study. Prunusyedoensis, a hybrid of a native Japanese Prunus
species, is one of the most common street trees in Tokyo. Since
it grows well in wet soils, it is often planted at the edges of rivers
and ponds as well. Similarly, Z. serrata, a plant of wet valleys or
fertile river terraces, is a common street or ornamental tree spe-
cies in urban areas. Ginkgo biloba, native to China, is also one of
the most frequently planted tree species in urban areas in Japan.
Study sites were in the cities of Tama and Machida (3560
3561N, 1394013942E), in urbanized suburbs 30km
west of central Tokyo. The population density of the area is
60007000 peoplekm2 (Municipalities of Tama and Machida)
and the daily average traffic count is 30,00040,000 vehi-
clesday1 (Road traffic research data 2011, Municipalities of
Tama and Machida). Three street sites' were set along streets
in this area, each of which supported plantings of one of the
study species. In the street sites, plants were all planted in grids
embedded in concrete or asphalt pavement. Street lamps were
present at intervals of 25m. Sample trees were selected from
those that were not adjacent to the lamps. As a control, a park
site was selected in a nearby 42.2-ha city park (Oyamada Park)
composed of several open areas surrounded by urban forests.
The park site was positioned in an open space where the three
species had been planted directly in bare soil. Street trees are
pruned every 2 years, while park trees are pruned irregularly
in a longer interval. Trees in both sites were not fertilized. Soil
samples taken by a boring stick (060cm depth) from the
Tree Physiology Online at http://www.treephys.oxfordjournals.org
 1058 Osone et al.
grids at the street sites and the soil at the park site were brown-
coloured containing little sand, stones and clay.
Observations were made over three growing seasons from
2010 to 2012. In 2010, to observe the changes in leaf proper-
ties during a growing season, stomatal conductance of water
vapour (gs, molm2s1), leaf N content, specific leaf area
(m2kg1) and leaf fall were measured monthly from June to
October in the park and street sites. To examine the effects
of climatic fluctuations on plant physiology, a set of proper-
ties related to plant water status (midday leaf potential, pre-
dawn leaf potential, hydraulic conductance from soil to leaf,
osmotic potential at full turgor, gas-exchange rate, stomatal
density, carbon isotope ratio) and related to N deficiency (gas-
exchange rate, leaf N content) was measured in both park and
street sites in early August in 2011 and 2012. Chlorophyll fluo-
rescence (in 2011 only) and parameters of aerosol (in 2012
only) were also measured in early August in both park and
street sites. These measurements were carried out on sunny
days after at least three consecutive sunny days. For all these
measurements, three individuals with similar size were used
per species per site (Table1).
Environmental conditions
Average air temperature and precipitation in 201012 and the
30-year means of 19832012 in this region were obtained
from the nearest weather station (Fuchu, Japan Meteorological
Agency). In 2010, the first year of this study, the microclimate of
each site was monitored continuously during the growing season
(late JuneOctober). Air temperature at 3m above the soil sur-
face was measured every hour by portable data loggers equipped
with a thermo sensor (TR-51i, T and D Corp., Nagano, Japan).
Soil moisture content to a depth of 25cm was measured every
hour by probes (10HS, Decagon Devices, Inc., Pullman, WA, USA)
equipped with data loggers (Em5b, Decagon Devices, Inc.).
Leaf fall
In June 2010, 10 sun-exposed shoots were randomly selected
per individual (three individuals per species and site; the same
hereafter) at a height of 34m above the soil surface and
marked. Sylleptic shoots were not included in the marked
shoots. The number of leaves of these marked shoots was
counted monthly from June to October. All marked shoots had
no leaf scars at the measurement in June indicating that all
Table1. Average height, average diameter at breast height (DBH) and size of the planting grid. Numbers in parentheses represent SD.
Height (m) DBH (cm)
P. yedoensis Park 11.0 (3.0) 40.8 (17.9)
Street 7.7 (0.6) 27.4 (5.3)
Z. serrata Park 9.0 (0.8) 43.8 (10.7)
Street 7.5 (0.4) 32.5 (2.0)
G. biloba Park 11.0 (0.8) 42.4 (4.8)
Street 9.0 (0.8) 27.7 (4.8)
Tree Physiology Volume 34, 2014
current-year leaves were still attached to the branches at this
time, and they did not produce new leaves after this. The pro-
portion of remaining leaves was calculated as the current num-
ber of leaves divided by the initial leaf count.
Gas-exchange rate
To determine the potential gas-exchange rate, both the net pho-
tosynthetic rate (A, molm2s1) and gs in midsummer were
measured with an infrared gas analyzer-leaf chamber system
(Li-6400; Li-Cor, Inc., Lincoln, NE, USA) at a photosynthetic
photon flux density of 2000molm2s1, a leaf temperature
of 26C, 6070% relative humidity and 400ppm of CO2.
Intrinsic water-use efficiency (WUE) was calculated by dividing
A by gs. All measurements were completed during the morning
(911 am) on sunny days to obtain maximum gas-exchange
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rates. In all measurements, three fully expanded, sun-exposed
leaves at a height of 34m above the soil surface near the tips
of shoots were randomly selected per individual.
Plant water relations
In early August in 2011 and 2012, to determine leaf-area based
soil-to-leaf hydraulic conductance (KS-L, mmolm2s1MPa1), gs
was measured four times in a single day from predawn to early
afternoon using a porometer (Li-1600; Li-Cor, Inc.). Immediately
following the leaf gas-exchange measurements, the leaves were
sampled and their water potentials were then determined using
a pressure chamber (Model 600, PMS Instrument Co., Corvallis,
OR, USA). In all measurements, three sun-exposed leaves at a
height of 34m above the soil surface near the tips of shoots
were randomly selected per individual. The transpiration rate per
unit leaf area (E, mmolm2s1) was then calculated from the gs
values and boundary layer conductance (gb, molm2s1) as:
E = W( gs gb /( gs + gb ))103 , (1)
where W is the leaf vapour pressure deficit calculated using the
GoffGratch formulation for saturated water vapour pressure.
Following Jones (1992), gb was determined as:
gb = 0.446(0.715( /d )0.5 )(273/(Tleaf + 273))(P /101.3), (2)

where is wind speed (ms1), d is leaf length (m) and P is air
pressure (kPa), assuming =1 and d=0.05. The possible error
Years after planting Grid size
20
25 Strips of 80cm width 7m interval between trees
Unknown
25 Strips of 80cm width 8m interval between trees
Unknown
>35 80110cm grids planted individually in a grid

in E is 20% for values between 0.1 and 1, when gs=0.2.
Assuming that the values of predawn leaf water potential (pd)
are almost in equilibrium with soil water potential and that the
transpirational flow is in the steady state, the values of KS-L were
estimated as (Wullschleger et al. 1998):
K S-L = E(pd )1 (3)
where is the leaf water potential at daytime. There are two
possible methods of calculating KS-L, the regression method
and the single-point method. In the regression method, KS-L is
obtained from the regression coefficient for E versus pd
trajectory (Schulze et al. 1985, Ishida et al. 1992). In the sin-
gle-point method, KS-L is obtained from values of pd mea-
sured at a single point in time (Cochard et al. 1996, Meinzer
et al. 1995). In P. yedoensis and Z. serrata, the E versus pd
relationships were almost linear during early to late morning,
yielding similar values for KS-L calculated by the two differ-
ent methods. However, the regression method could not be
applied in G. biloba since these relationships were curvilin-
ear. In the present study, therefore, KS-L was calculated by
the single-point method using the data obtained in the late
morning at which time the value of E was stabilizing (Scholz
et al. 2007).
Three sun-exposed shoots per individual were harvested at
the day of measurements and left overnight covered by plas-
tic bags with their cut end immersed in tap water. The next
day, leaves of these shoots were cut off, and after a freeze
and thaw, their osmotic potential () was determined with a
vapour pressure osmometer (Vapro 5520, Wescor, Inc., Logan,
UT, USA).
Leaf N content and stable carbon isotope ratio
Seven to ten discs were obtained from each leaf used for the
measurements of potential gas-exchange rate. These discs
were then oven dried at 80C for 3 days. The N content of
half of the leaf discs was determined with an N-C analyser
(Sumigraph NC-800, Sumitomo-Kagaku, Osaka, Japan). Mass-
based or area-based N concentration and photosynthetic
N-use efficiency (PNUE, maximum photosynthesis divided by
area-based N concentration) were then calculated. In 2012,
the remaining leaf discs were finely ground using a sample mill.
Then, stable carbon isotope ratios of the subsamples of 2mg
were measured with a combined system of an elemental anal-
yser (Flash 2000, Thermo Fisher Scientific K.K., Yokohama,
Japan) and an isotope mass spectrometer (Delta V advantage,
Thermo Fisher Scientific K.K.). Isotope values were corrected
using the standards (l-alanine, 13C was 23.47).
Stomatal density
In 2011 and 2012, three leaves per individual were har-
vested near the locations of the leaves from which potential
The effects of summer heat on urban street trees1059
gas-exchange rate was determined and replicas of the adaxial
surfaces were obtained by Suzuki's Universal Micro-Printing
(SUMP) method using amyl acetate and thin celluloid plates
(2cm in diameter; SUMP Laboratory, Tokyo, Japan). Micrographs
of the replicas were then acquired using a CCD camera fas-
tened to a light microscope (BX40, Olympus, Tokyo, Japan). The
number of stomata in the surface area of 0.250.35mm2 was
determined using Image J software. Stomatal density was cal-
culated as the number of stomata divided by the surface area.
Chlorophyll fluorescence
Chlorophyll fluorescence was measured with a fluorescence
meter (Mini-PAM, Walz, Effeltrich, Germany) connected to a leaf
clip holder (Model 2030-B, Walz) in 2011. Maximum fluores-
cence yield (Fm) and dark fluorescence yield (F0) in Photosystem
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II (PSII) were determined just before dawn on the same day
that the maximum A measurements were made. For the same
leaves, steady-state fluorescence (F) and maximal fluorescence
(Fm) in the light adapted state of PSII were determined during
the day. Measuring beam and flashes were applied through a
fibre optic cable adjusted to an angle of 60 to the leaf surface.
The source of actinic light was sunlight (>950molm2s1).
From these measurements, potential maximum quantum yield
of PSII (Fv/Fm=(FmF0)/Fm), effective quantum yield of PSII
(F/Fm=(FmF)/Fm) and non-photochemical quenching
coefficient (NPQ=(Fm/Fm)1) were calculated.
Aerosol pollutants
In August 2012, three shoots near the leaves used for photo-
synthetic measurements were sampled per individual. Half of
the leaves in a shoot were washed with ultrapure water, and
the quantity of SO4 in the water was determined by ion chro-
matography (DX320, Dionex, Osaka, Japan). The remaining
leaves were washed with chloroform. A subsample of the chlo-
roform was then filtered by a quartz fibre filter to collect black
carbon particles suspended in the chloroform. The absorbance
at 580nm of the quartz fibre filters was measured by a spec-
trophotometer with an integrating sphere (U-4100, Hitachi
High-Technologies Corp., Tokyo, Japan), and the amount of
black carbon was calculated following Yamaguchi et al. (2012).
The amount of epicuticular wax extracted in chloroform was
determined following Takamatsu et al. (2001).
Statistical analysis
For the traits measured in a single year, differences in means
between sites were tested by t test for each species. For the
traits measured in both 2011 and 2012, differences in means
among four combinations of the two sites and 2 years were
tested by Tukey's multiple comparison. Where possible, data
were transformed to conform to assumptions of normality and
homogeneity of variance. All statistical analyses were carried
out using R version 3.0.1.
Tree Physiology Online at http://www.treephys.oxfordjournals.org
 1060 Osone et al.

Results to September, although gs was almost constant throughout

Climate conditions
The midsummers of 2010 and 2012 were more harsh than
usual with 2.8 and 2.4C higher air temperature in August than
the average year (the highest and the second highest average
maximum temperature in recorded history, respectively) and with
656% precipitation of average year in July and August (Table2).
The 2011 season was as usual with average maximum tempera-
ture (31.0C, August) and slightly more rain (278mm, August)
than falls in an average year. Vapour pressure deficit (VPD) of
August was also higher in 2010 and 2012 than in 2011.
The meteorological conditions were different between street
and park sites (Figure1). In the street sites, daily air tempera-
ture was generally higher than that in the park sites by 23C
the season in Z. serrata in the street site (Figure2ac). In
P.yedoensis and Z. serrata, gs was lower in the street site than
in the park site during most of the growing season, and the
difference was more remarkable in the midsummer. In these
species, leaf N content per area (Na) was also lower in street
sites than in the park site (Figure2d and e). In contrast, in G.
biloba, gs and Na at the street site was similar to or even higher
than that at the park site (Figure2c and f).
In all species, leaf fall started earlier in park trees than in
street trees in the 2010 growing season (Figure2gi). Among
the species, P. yedoensis was the fastest in leaf fall: leaves
had started to fall in August in the park site and most of the
leaves had been lost by October in both sites. In other species,
leaf fall occurred much more slowly with most leaves (>70%)

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throughout the growing season. Soil water content was lower
in the street sites than in the park site at most by 60%. On the
other hand, air temperature and soil water content were similar
among street sites.
Seasonal patterns in leaf traits and leaf number
betweensites
Stomatal conductance to water vapour (gs) generally increased
from June to July reaching a peak in midsummer and decreased
remaining on the branches in October.
Water relations between sites and years
Both in 2011 and 2012, P. yedoensis decreased photosyn-
thetic capacity (A) and gs, and increased intrinsic WUE in the
street site compared with the park site (Figure3a, b and d).
Between years, A and gs were lower in hot and dry 2012 than
in milder 2011, resulting in the lowest A and gs and the h
ighest
WUE in the street trees in 2012. In Z. serrata, A and gs did

Table2. Maximum air temperature, precipitation and VPD of 201012 and 30-year means (19832012). Data on air temperature and precipitation
were derived from Fuchu weather station and VPD data were derived from the municipal of Tama city. Bold letters represent temperature >2C
above means or precipitation >50mm deficits from means. The 30-year mean was not available for VPD.

Maximum air temperature (C) Precipitation (mmmonth1) VPD (kPa)

June July August September October June July August September October June July August September October
2010 28.0 32.0 33.8 29.2 20.8 112 59 51 432 199 0.97 1.24 1.49 1.16 0.67
2011 26.4 31.2 31.0 28.3 21.8 119 244 278 337 126 0.87 1.20 1.17 1.04 0.79
2012 24.7 30.7 33.5 29.0 22.3 228 98 14 256 82 0.88 1.18 1.55 1.19 0.88
30 year mean 25.6 29.6 31.1 26.8 21.3 168 176 236 259 182

Figure1. Average daily air temperature (a) and soil water content (b) in a park site (open symbols) and in street sites (closed symbols). PY, ZS and
GB denote Prunusyedoensis, Zelkova serrata and Ginkgo biloba, respectively.

Tree Physiology Volume 34, 2014


Figure2. Time courses of stomatal conductance (ac), leaf nitrogen per area (df) and proportion of remaining leaves of the initial leaf number
in shoots (gi) for P. yedoensis, Z. serrata and G. biloba at a park site (open symbols) and in street sites (closed symbols) in the growth season in
2010. Data are means with SE (*P<0.05, **P<0.01, ***P<0.001).
not differ significantly between sites in 2011, but showed sig-
nificant decreases in street trees in 2012. In these angiosperm
species, A was strongly correlated with gs, suggesting that the
variations in A between sites and years were largely explained
by gs (Figure4a, P. yedoensis: R=0.84, P<0.001; Z. serrata:
R=0.80, P<0.001). Likewise, in G. biloba, gs tended to be
smaller in street sites than in the park site, and smaller in 2012
than in 2011 (Figure3b). However, A did not show significant
site differences within a year, which resulted in a weaker cor-
relation between A and gs in this species (Figure4a, R=0.63,
P<0.01). Across species, G. biloba, a gymnosperm, was gener-
ally higher in gs and lower in WUE than the two angiosperms in
both sites and years (Figure3b and d). As a result, the lowest
gs value in G. biloba (street trees in 2012) was still higher than
those of the angiosperms except in only one case (P.yedoensis
The effects of summer heat on urban street trees1061
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in the park site in 2011). The low WUE in G.biloba can be also
seen in Figure4a, where the Ags relationship of G. biloba was
shifted towards the right side of the angiosperms, resulting in a
higher leaf internal CO2 of G. biloba (Figure3f).
Stomatal density did not vary significantly between sites and
years in P. yedoensis and G. biloba suggesting that the changes in
gs were not controlled by the number of stomata in these species
(Figure3c). However, Z. serrata decreased stomatal density in the
street site in both 2011 and 2012. Among the species, G. biloba,
which was the highest in gs, was the lowest in stomatal density.
Although intrinsic WUE varied substantially in P. yedoensis
and Z. serrata between sites (Figure3d), 13C, an index of WUE
over the long term, varied little between sites in these species
(Figure3e). Between years, P. yedoensis in the street site and
Z. serrata showed more negative 13C in hot and dry 2012 than
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 1062 Osone et al.

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Figure3. Parameters related to gas-exchange rates for P. yedoensis, Z. serrata and G. biloba. (a) Photosynthetic rate; (b) stomatal conductance; (c)
stomatal density; (d) intrinsic WUE; (e) carbon isotope ratio; (f) intercellular CO2 concentration; (g) nitrogen content per unit leaf area; (h) PNUE.
Data are means with SE. Different letters indicate the significant differences of the mean values among sites and research years in a species
(P<0.05).

Tree Physiology Volume 34, 2014

 The effects of summer heat on urban street trees1063

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Figure4. Relationships between photosynthesis and stomatal conductance (a) and leaf nitrogen per area (b) in P. yedoensis, Z. serrata and G.biloba.

Table3. Parameters of plant water relations in a city park (Park) and along streets (Street). Mean values (SD) are presented. Different letters
indicate the significant differences of the mean values among sites and research years for a species (P<0.05).

Species Sites md of leaves (MPa) pd of leaves (MPa) (MPa1) KS-L (mmolm2s1MPa1)

2011 2012 2011 2012 2011 2012 2011 2012

P. yedoensis Park 1.34 (0.07)a 0.68 (0.09)b 0.26 (0.10)a 0.12 (0.03)b 1.78 (0.07)a 1.61 (0.03)b 7.80 (0.80)a 7.21 (1.26)a
Street 1.48 (0.05)a 0.86 (0.17)b 0.27 (0.10)a 0.36 (0.02)a 1.85 (0.05)a 1.60 (0.02)b 6.27 (1.32)b 6.69 (1.62)a
Z. serrata Park 1.75 (0.10)a 0.87 (0.03)c 1.05 (0.65)a 0.11 (0.03)b 1.84 (0.10)a 1.51 (0.05)b 5.32 (2.05)a 4.92 (0.85)a
Street 1.63 (0.06)a 1.16 (0.22)b 1.13 (0.15)a 0.38 (0.08)c 1.74 (0.06)a 1.46 (0.15)b 5.75 (0.62)a 3.67 (0.92)c
G. biloba Park 1.33 (0.85)a 0.50 (0.13)b 0.48 (0.06)a 0.15 (0.09)b 1.65 (0.06)a 1.43 (0.03)b 8.93 (0.85)a 9.25 (1.54)a
Street 1.49 (0.36)b 0.53 (0.36)b 0.38 (0.06)a 0.34 (0.09)a 1.67 (0.02)a 1.52 (0.07)b 6.84 (0.42)b 9.70 (0.28)a

in 2011, which also contradicted the pattern found in intrinsic
WUE and expected by the environmental conditions.
Compared with these gas-exchange properties, parameters
related to water availability in plants varied less between sites
(Table3). In all species, midday water potential of leaves (md)
tended to be more negative in the street sites than in the park
site, but the differences were small or statistically insignificant.
Predawn water potential of leaves (pd) also showed significant
decreases in the street sites in all species in 2012, but even in
these cases, pd did not fall below 0.5MPa. An exception was
Z. serrata in 2011 where pd fell to 1MPa. Osmotic potential
() did not differ significantly between sites, either. Likewise,
leaf hydraulic conductance from soil-to-leaf (KS-L) did not differ
or decreased slightly in the street sites. Unlike the site differ-
ences, these parameters showed more consistent differences
between years except KS-L, which decreased significantly only
in Z. serrata in 2012. There was an overall trend for md and
to be slightly higher in 2012 than in 2011. The higher md in
2012 was accompanied by a lower gs than in 2011 (Figure5a),
suggesting that stomatal closure occurred at a higher md in
2012. Across species, G. biloba, which was the highest in KS-L,
was the highest both in gs and pd in either years, while Z. ser-
rata was the lowest in KS-L, gs and pd (Figure5a and b).
Nitrogen deficiency between sites and years
Leaf N content per unit area (Na) was significantly lower at the
street sites than at the park site in P. yedoensis and Z. serrata
(Figure3g). In G. biloba, Na tended to be lower at the street
sites in both years, but the difference was not statistically sig-
nificant. In contrast to parameters related to water stress, Na did
not show a consistent difference between years in either spe-
cies. A was significantly correlated with Na in P. yedoensis and
Z. serrata but the correlation was weaker than that between A
and gs (Figure4b, P. yedoensis: R=0.77, P<0.001; Z. serrata:
R=0.64, P<0.05; G. biloba: R=0.33, P=0.17).
Effects of photoinhibition and aerosol pollution
betweensites
Midday quantum yield of PSII (F/Fm) was significantly lower
at the street sites than at the park site in P. yedoensis and
Z. serrata. However, in these species, the predawn quantum
yield (Fv/Fm) at the street site was well over 0.75 (Table4).

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 1064 Osone et al.

Downloaded from http://treephys.oxfordjournals.org/ at New York University on April 20, 2015

Figure5. Relationships between stomatal conductance and leaf water potential (a), and stomatal conductance and hydraulic conductance (b). PY,
ZS and GB denote P. yedoensis, Z. serrata and G. biloba, respectively. The symbols located at the origins of the arrows are data from park sites and
the symbols at the ends of the arrows are data from the street sites. Open symbols, 2011; closed symbols, 2012.

Table4. PAM and aerosol parameters of the three study species planted in a city park (Park) and along streets (Street). PAM parameters were
measured in 2011 and aerosol parameters were measured in 2012. Mean values (SD) are presented. Asterisks indicate the significant differences
of the mean values between sites in a species (*P<0.05, **P<0.01, ***P<0.001).

Species Sites PAM Aerosol

Fv/Fm F/Fm NPQ SO4 (mmolm2) Black carbon (gmm2) Wax (mgm2)
P. yedoensis Park 0.82 (0.02) 0.42 (0.02)*** 1.86 (0.40) 0.131 (0.05) 15.75 (2.53) 0.544 (0.057)
Street 0.82 (0.01) 0.37 (0.02) 2.13 (0.27) 0.123 (0.02) 14.89 (4.16) 0.544 (0.057)
Z. serrrata Park 0.83 (0.00)*** 0.33 (0.02)* 3.14 (0.41)*** 0.179 (0.06) 6.25 (1.55) 0.313 (0.018)
Street 0.79 (0.01) 0.29 (0.04) 2.01 (0.30) 0.178 (0.13) 6.38 (0.82) 0.315 (0.128)
G. biloba Park 0.78 (0.01) 0.22 (0.03)** 2.92 (0.49)** 0.172 (0.09) 5.86 (2.78) 0.416 (0.125)
Street 0.78 (0.01) 0.26 (0.02) 2.23 (0.53) 0.122 (0.05) 7.87 (4.91) 0.418 (0.034)

Non-photochemical quenching, which was associated with the
amount of excess excitation energy dissipated as heat, did not
show significant increases at the street sites in all species.
The amount of sulphate and black carbon that was attached
to the leaf surface did not differ significantly between the sites
for all species (Table4), neither did the amount of epicuticular
wax on the leaves.
Discussion
Water stress differed between years
All species decreased their A and gs more or less in street sites in
both years, but the decrease was larger in the unusually hot and
dry 2012 summer than in the average 2011 summer (Figure3).
These results suggest that street trees were subjected to more
severe water stress in the 2012 summer than average year.
However, even in the unusually hot and dry summer, street trees
in P. yedoensis and G. biloba exhibited no apparent symptoms of
hydraulic failure (loss of nocturnal recovery of water potential, a
large decline in KS-L and gas-exchange rate), indicating that the
potential risk of hydraulic failure caused by climatic extremes is
low in these species (Figures3 and 5, Table3). Only Z. ser-
rata showed a significant reduction in KS-L in 2012, but nocturnal
recovery of pd suggests that this is not a fatal hydraulic failure.
Similar to the present study, Whitlow et al. (1992), who monitored
water relations (gs and water potentials) in street trees in eastern
North America for 3years, also reported no evidence of unusual
water stress in the year of least rainfall of the record. The summer
of 2012 marked air temperature as much as 2.4C above normal
(the second highest August temperature in the history) and had
rainfall of 656% of the usual summer. One may think that these
conditions were not extreme enough to cause apparent hydrau-
lic failure in street trees. However, in the European heatwave in
2003, a similar degree of heat and drought (temperatures 2C

Tree Physiology Volume 34, 2014


above long-term means and 50% rainfall deficits, an average
from 14 sites) was reported (Ciais et al. 2005). Therefore, the
climatic condition in 2012 might be a realistic extreme that trees
in temperate regions would experience.
The species showed differential stomatal regulations depend-
ing on whether the drought they experienced was caused by
street conditions or by climatic fluctuations. When subjected
to street conditions, species decreased md slightly or kept
constant while decreasing gs (Figure5a, Table3, comparison
between sites). This was a common response that plants exhibit
during moderate drought (Abrams 1990, Arndt 2000, Poulos et
al. 2007). In contrast, during hot and dry summers, trees even
increased md by decreasing gs by a large amount (Figure5a,
Table3, comparison between years). This means that plants ini-
tiated stomatal closure at higher md in the hot summer than in
the usual summer. Plants under dry soil conditions sometimes
keep their gs low even if leaf water potential is high enough for
gas exchange (Davies and Zhang 1991). Although this is a less
common response, Whitlow et al. (1992) also reported a lower
gs but higher md in unirrigated street trees than irrigated street
trees. Why the same species responded differently to drought
caused by street conditions and by climatic fluctuations was
not known. However, closing stomata at higher md appears
to be a more conservative responsekeeping the demand for
water well below levels that would challenge supply. Therefore,
it may be that the drought stress caused by climatic fluctua-
tions was so influential as to make plants change the sensitiv-
ity of stomata to VPD or to water availability of roots in the
hot summer. It is generally thought that patterns of stomatal
regulation are related to the species strategy or plant functional
group (i.e., gymnosperms vs angiosperm, trees vs herbs). So,
there are studies that reported differential stomatal regulations
among species from different habitats (i.e., seric vs mesic) or
from different functional groups (Abrams 1990, Arndt 2000,
Sperry 2004, Poulos et al. 2007). However, few studies have
reported so far that the same species showed differential sto-
matal regulation to drought.
The lower 13C in 2012 than in 2011 in P. yedoensis and
Z. serrata appears to contradict the hotter and drier midsummer
in 2012. This can be explained by the fact that 13C reflects Ci
over the long term. Although the environmental conditions in
2011 were milder in the midsummer, they were more severe
during the rainy season (from June to middle of July) with less
rainfall and higher temperatures than in 2012 (Table2). In 2011,
therefore, plants might have been subjected to stronger water
stress in this period and had increased uptake of 13C at this time,
which resulted in a rise of 13C of leaf tissues. Similarly, was
slightly lower in 2012 than in 2011, which also contradicted our
expectation (Table3). However, plants regulated the stomata to
keep higher md in 2012 than in 2011. Therefore, they did not
need to decrease . It is also possible that osmotic regulations
had not been fully completed by the time of measurement (early
The effects of summer heat on urban street trees1065
August) in 2012, since an increase in osmolytes in response to
water deficits is a process that takes several hours and weeks
depending on species (Morgan 1984).
Sensitivity to street conditions differed between species
Compared with P. yedoensis and Z. serrata, G. biloba, a gymno-
sperm, was less affected by street conditions keeping high gs,
md and KS-L even under adverse conditions (Figures3 and 5,
Table 3). These results suggest that G. biloba was the least
sensitive to urban street conditions of the three species. The
most sensitive species might be Z. serrata, which decreased gs
and KS-L substantially in the street sites in 2012. What were the
causes of these species differences, then? Ginkgo biloba was
generally high in KS-L, which enabled the species to keep their
gs higher than other species without reducing md. On the other
Downloaded from http://treephys.oxfordjournals.org/ at New York University on April 20, 2015
hand, Z.serrata was low in KS-L even under a preferable condi-
tion, suggesting that it is intrinsically low in whole-plant hydraulic
conductance (Table3, Figure5b). To ensure gs with the low KS-L,
Z. serrata decreased md more than the other species in all sites
and years (Figure5a). However, the decreased md increased
the probability of cavitation, which could be the cause of the
decline in KS-L observed in 2012 (Table3, Figure5b). Therefore,
the susceptibility to drought in Z. serrata can be ascribed to the
combination of a lower whole-plant hydraulic conductance and a
riskier stomatal regulation. Regardless of KS-L, a riskier stomatal
regulation or a lower safety margin to hydraulic failure is likely
an intrinsic property that angiosperms have in common (Sperry
2004, Choat et al. 2012). The higher KS-L in G. biloba might appear
to be inconsistent with the classic view that gymnosperms with
their narrow tracheids are less efficient in water transport than
angiosperms with large vessels (Bond 1989, Rundel and Yoder
1998, Pammenter etal. 2004). However, recent close scrutiny
of the ultrastructure of tracheids and vessels revealed that gym-
nosperms were no less hydraulically efficient than angiosperms
(Hacke et al. 2004, Brodribb et al. 2012), and there are studies
showing higher whole-plant hydraulic conductance and transpira-
tion rates of some gymnosperms than of angiosperms (Kull and
Herbig 1994, Becker et al. 1999, Becker 2000).
Street trees are also subjected to N deficiency
Nm and Na were generally lower at the street sites than at
the park site for the three study years (Figures 2df and 3g),
supporting the notion that N availability is limited in urban
environments (Pulford 1991, Craul 1999, Harris et al. 2004,
Scharenbroch and Lloyd 2004). Although comparable data
were limited, Tanaka-Oda et al. (2009) showed that on a
university campus in Tokyo, Na was 1.52.0gm2 in decidu-
ous trees planted in grids embedded in pavements and 2.0
3.3gm2 in bare soil. These ranges largely overlapped with
those obtained at the street sites (1.321.95gm2) and the
park site (1.892.63gm2) in the present study, respectively.
However, a meta-analysis of 2500 vascular plant species in
Tree Physiology Online at http://www.treephys.oxfordjournals.org
 1066 Osone et al.

natural vegetation showed that the 595 percentile range of
Na of non-fixing plants was 0.83.5gm2 (Wright et al. 2005),
which covers the ranges for trees in pavements. Street trees
were therefore not likely to experience unusually low N avail-
ability, compared with trees in natural vegetation.
In P. yedoensis and Z. serrata, street trees exhibited symp-
toms of both water and N deficiency. An intriguing question is
whether water (gs) or N deficiency (Na) limited A more strongly
in the street trees. In these species, A was correlated signifi-
cantly with both gs and Na, but the correlation was stronger
between A and gs than between A and Na (Figure4). However,
if stomatal conductance alone limits A largely, Ci should
decrease in the street site, but this did not occur in the present
study (Figure3f). Rather, Ci was quite conservative between
sites, indicating that the decreased supply of CO2 caused by
stresses at street sites could impair the physiological func-
tions of leaves. However, despite the apparent signs of water
deficiency in the street sites, leaves of street trees were more
durable than those of trees in the park (Figure2gi). This may
be partly explained by retarded leaf aging in street trees. In
temperate deciduous trees, seasonal leaf aging progresses as
air temperatures decrease in autumn (Brgger et al. 2003). In
the streets where the air temperature was higher than in the
park, this aging process can be retarded, reducing leaf fall in
the late growing season. Similar to these results, Matsumoto
etal. (2003) reported retarded leaf fall in G. biloba in an urban-
ized area of Japan. However, the substantial leaf loss found in
P. yedoensis during midsummer in the park cannot be ascribed
to the faster autumnal leaf aging. This might be related to her-
bivory by insects. Leaves of P. yedoensis are sometimes subject

Downloaded from http://treephys.oxfordjournals.org/ at New York University on April 20, 2015

the lowered gs was balanced by the decreased uptake of inter-
nal CO2 by photosynthetic enzymes (N deficiency) in the street
sites. Therefore, in these species, it is likely that water defi-
ciency limited A more strongly but N deficiency also contrib-
uted substantially to the decreases in A.
Street trees did not suffer from photoinhibition or aerosol
pollution
A low photosynthetic rate that results from drought or N
deficiency increases the risk of photoinhibition because it
increases the amount of excess light energy that leaves cannot
use. Indeed, P. yedoensis and Z. serrata, which decreased A
in the street sites, had a lower quantum yield of PSII (F/Fm,
Table4) in the sites. However, they showed a nocturnal recov-
ery of predawn quantum yield of PSII (Fv/Fm>0.7) and did not
show significant increases in NPQ. These results suggest that
neither chronic photoinhibition nor induction of photoprotec-
tive processes (Ishida et al. 1999, 2006, Martnez-Ferri et al.
2000) occurred in these species in the street sites, despite
the apparent reduction in A. In the present case, the reduction
in A might have not been large enough to cause chronic photo-
inhibition and induction of photoprotective processes.
The emission standards for diesel cars in Japan are less
strict than those of Europe. For example, the standard for SO4
emission is <500ppm in Japan, while it is <50ppm in Europe.
Consequently, SO4 and black carbon emitted by diesel cars
could be major sources of aerosol particles in Japan. However,
there was no evidence for significant influences of aerosols on
the street trees (Table4). Since the street sites and park site
were only a few kilometres apart and aerosol nanoparticles
can be readily diffused in the atmosphere, the differences in
the effects of aerosol particles might be negligible between
the sites.
Leaves of street trees were more durable
We had expected that street trees would lose more leaves than
park trees during a growing season, because environmental
to severe herbivory by larvae of multiple moth species in July
to September. Indeed, we found much more intensive herbivory
of P. yedoensis leaves in the park than in the street sites (data
not shown), which could have caused the substantial loss of the
leaves in summer. Trees in the park may have been more prone
to herbivory because the high leaf N content of park trees
created a preferred food source for larvae (Minkenberg and
Fredrix 1989). Whatever the causes might be, however, pro-
longed persistence of leaves in street trees is interesting from
the perspective of annual carbon balance since the carbon gain
brought by these leaves in early autumn can compensate for
their decreased carbon gain in midsummer in the street trees.
Conclusions
Street trees suffered from more severe drought stress in the
unusually hot and dry summer in 2012 than in the usual sum-
mer in 2011. However, because of a more conservative stoma-
tal regulation (stomatal closure at higher leaf water potential),
apparent symptoms of hydraulic failure could be avoided even
in the hot and dry summer. Among species, G. biloba, a gymno-
sperm, was less susceptible to the drought under urban street
conditions than P. yedoensis and Z. serrata. The lower suscep-
tibility could be explained by the higher intrinsic KS-L and more
conservative stomatal regulation of the species. Street trees
were also subjected to N deficiency, which reduced carbon
assimilation rates, together with the decreases in gs. However,
effects of photoinhibition and aerosol pollution on street trees
were not observed.
Acknowledgments
The authors thank Drs Hiroyuki Sase, Masaharu Sakai and
Yuko Ito and Shoji Hashimoto for their valuable advice and sup-
port in data collection. Municipality of Tama, Municipality of
Machida and Oyamada Park provided us with valuable informa-
tion on research sites.

Tree Physiology Volume 34, 2014


Conflict of interest
None declared.
Funding
This research was supported by Grant-in-Aid for Scientific
research (20120010, 23570032, 24370009) from the Ministry
of Education, Culture, Sports, Science and Technology, Japan.
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