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Environmental Research Letters

Environ. Res. Lett. 9 (2014) 044012 (8pp) doi:10.1088/1748-9326/9/4/044012

Impact of heat stress on crop yield—on the


importance of considering canopy
temperature
Stefan Siebert1, Frank Ewert1, Ehsan Eyshi Rezaei1, Henning Kage2 and
Rikard Graß2
1
Institute of Crop Science and Resource Conservation, University of Bonn, Katzenburgweg 5, D-53115
Bonn, Germany
2
Institute of Crop Science and Plant Breeding, Agronomy and Crop Science Department,
Christian-Albrechts-Universität zu Kiel, Hermann-Rodewald-Str. 9, D-24118 Kiel, Germany

E-mail: s.siebert@uni-bonn.de

Received 21 February 2014, revised 25 March 2014


Accepted for publication 28 March 2014
Published 1 May 2014

Abstract
Increasing crop productivity while simultaneously reducing the environmental footprint of crop
production is considered a major challenge for the coming decades. Even short episodes of heat
stress can reduce crop yield considerably causing low resource use efficiency. Studies on the
impact of heat stress on crop yields over larger regions generally rely on temperatures measured
by standard weather stations at 2 m height. Canopy temperatures measured in this study in field
plots of rye were up to 7 °C higher than air temperature measured at typical weather station
height with the differences in temperatures controlled by soil moisture contents. Relationships
between heat stress and grain number derived from controlled environment studies were only
confirmed under field conditions when canopy temperature was used to calculate stress thermal
time. By using hourly mean temperatures measured by 78 weather stations located across
Germany for the period 1994–2009 it is estimated, that mean yield declines in wheat due to heat
stress during flowering were 0.7% when temperatures are measured at 2 m height, but yield
declines increase to 22% for temperatures measured at the ground. These results suggest that
canopy temperature should be simulated or estimated to reduce uncertainty in assessing heat
stress impacts on crop yield.
S Online supplementary data available from stacks.iop.org/ERL/9/044012/mmedia

Keywords: heat stress, crop yield, temperature, soil moisture, modelling, wheat, rye

1. Introduction tunnels controlling temperature during crop growth [4–9], the


negative impacts of heat stress on yield has recently been
As sustainably meeting increasing world food demand is a confirmed for actual production conditions at large spatial
major challenge for humanity [1–3], it is important to scales by the interpretation of field trials, statistical analyses
understand factors constraining crop yields and resource use of large scale observational datasets and the application of
efficiency. Evidence of the negative impact of heat stress on crop models [10–20].
major world food crop yields is considered increasingly Heat and drought have multiple, negative impacts on
robust. Formerly studied in climate chambers or plastic crop yields, including reducing leaf photosynthesis and
enhancing leaf senescence rates. More critically for yield
Content from this work may be used under the terms of the determination, however, are the reported effects of decreasing
Creative Commons Attribution 3.0 licence. Any further grain number when heat stress occurs before or around
distribution of this work must maintain attribution to the author(s) and the
title of the work, journal citation and DOI. anthesis and reduced grain weight when it occurs during grain

1748-9326/14/044012+08$33.00 1 © 2014 IOP Publishing Ltd


Environ. Res. Lett. 9 (2014) 044012 S Siebert et al

filling [6, 21–24]. While drought represents a process that


develops and intensifies slowly, heat stress can occur very
abruptly and even short episodes of high temperature can
cause a severe decline in grain yields. This reality that both
heat stress and drought occur together, makes it difficult to
assess the unique impact of heat stress on crop yields under
field conditions and bares the risk of confounding effects [23].
Previous work, has used statistical methods to analyze the
relationship between high temperature and crop yields for
different crops and regions [15, 20], though such methods are
not able to identify nor explain the specific processes
responsible for yield losses [16, 25]. Process-based crop
models are increasingly used to quantify the impact of heat
and drought on crop yield but differ with respect to the
stresses and processes considered [26–28]. A remaining
challenge is to implement relationships into crop models
describing the impact of heat stress around flowering [29, 30].
Reported relationships between heat stress and grain yield or
grain number indentified under controlled environment con-
ditions may not hold under field conditions as temperatures in
the canopy close to the flowers may diverge considerably
from weather station measurements [31], where air tempera-
ture is typically measured above a grass canopy at 2 m height.
Further, the degree of deviation of canopy and flower tem- Figure 1. Schematic illustration of the temperature measurements
peratures from weather station measurements is likely used in this study. Tc is canopy temperature in rye measured by two
dependent on crop type, cultivar and crop management. As infrared radiometers placed about 50 cm above the canopy while the
other measurements refer to air temperature measured at a height of
such, the uncertainties in assessments of heat stress impacts 350 cm (T350), 200 cm (T200), 20 cm (T20) above ground or at the
on crop yield due to air temperature measurements are not ground (Tg).
well reported. The objectives of this study were (i) to deter-
mine differences between air temperature at 2 m height and
canopy temperature under field conditions, (ii) to evaluate the
relationship between stress thermal time around flowering replications (1920 test plots, SI figure 1(c)) and accounted
calculated from temperatures measured at different heights therefore for a considerable part of the heterogeneity in
and grain number or grain yield, and (iii) to estimate the varieties, soils and water management as observed under real
uncertainty in heat stress assessments caused by the missing field conditions. The test plots of 1.25 m times 4 m size were
information on canopy temperature. The study was performed arranged in a rectangular setup with gaps of 0.1 m between
in Germany but the findings are of general relevance for the plots. Measurements were conducted under clear sky
cereal cultivation in temperate regions. conditions in the period 10 AM to 2 PM. Plant height varied
between 70 cm and 150 cm with the majority of plants with a
height of about 115 cm (irrigated) and 95 cm (rainfed). In
addition, air temperature (T200), humidity, wind speed and
2. Materials and methods
global radiation were measured at 200 cm height above
ground on a grass canopy by a nearby standard weather sta-
2.1. Experimental setup to determine differences between
tion. Temperatures measured at the standard weather station
canopy temperature and air temperature above the canopy
at 200 cm height were in good agreement to the measure-
To determine the range of differences between canopy tem- ments taken at 350 cm height at the rye fields but on average
perature and air temperature under field conditions, tem- 0.6 K lower during the measurement period (SI figure 1(b)).
perature was measured in 1920 rye plots on field trials of Mean wind speed during the measurement period was 2.0
KWS LOCHOW GmbH located at Wohlde (52.80 °N, m s−1, global radiation ranged between 526 W m−2 and 969
10.02 °E, 80 m a.s.l.) in northern Germany on 30th of May W m−2 and relative humidity between 40% and 54%. The soil
2012 (anthesis). Canopy temperature Tc was measured by two properties differed between an area in the southeast char-
infrared radiometers (Campbell IR 120) fixed to a carrier at acterized by sandy soil texture (Su3, 69% sand, 26% silt, 5%
50 cm on average above the canopy while air temperature clay) and a loamy part in the northwest (Su4, 53% sand, 41%
T350 was measured using a band-gap temperature sensor silt, 6% clay). Soil water content was measured by an FDR
(Campbell CS 215) at 350 cm above ground or about 250 cm probe (Sentek Diviner 2000) to a depth of 85 cm (measure-
above the rye canopy (figure 1, SI figure 1(a)). The test site ments every 10 cm, 8 different depths) for 19 loamy rainfed
consisted of 480 inbred lines and hybrids of rye grown under plots, 20 loamy irrigated plots, 12 sandy rainfed plots, and 20
rainfed and irrigated conditions on loamy or sandy soil in 2 sandy irrigated plots. Mean plant available water content in

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Environ. Res. Lett. 9 (2014) 044012 S Siebert et al

the root zone was 17% for the rainfed sandy soil, 24% for the heat stress was applied was 5–12 days in some experiments
rainfed loamy soil, 67% for the irrigated sandy soil, and 59% [5, 34] but other reports indicate that the sensitive period may
for the irrigated loamy soil. The experiment at Wohlde was be longer [24, 35, 36]. Teixeira et al [36] for example,
however not suitable to test relationships between temperature assumed a thermal-sensitive period of 30 days centered in the
measured at different height and grain number or grain yield mid-point of the reproductive phase. To account for the cul-
because the temperature differences were measured on one tivar differences in heading date and the typical length of the
day only. period between heading and flowering at the test sites it was
decided to use a constant sensitive period of 18 days for this
2.2. Impact of heat stress on winter wheat grain number and study. STT20 and STT200 was then compared to mean grain
yield number per ear and relative yields Yrel (-) computed as ratio
We tested the relationship between stress thermal time around between the yield in a specific year and maximum yield
anthesis STT (°C minutes), computed as the accumulated observed at the research site during the period 2001–2011.
temperature sum above a threshold of 31 °C [6], and grain
number per ear or grain yield at winter wheat variety trials in
Saxony (Eastern Germany) during period 2001–2011. The 2.3. Uncertainty of heat stress impact around anthesis on
trials, performed by the State Office of Environment, Agri- winter wheat in Germany
culture and Geology of the federal state of Saxony (http://
To estimate the uncertainty in STT arising from unknown
www.smul.sachsen.de/lfulg), are designed to test the perfor-
mance of cultivars registered for commercial growing in canopy temperatures for other locations in Germany, we
Germany at test sites representing the range of climate and computed STT around flowering of winter wheat by using
soil conditions found in this federal state. Annual reports have hourly mean temperatures measured at the ground (Tg, °C)
been available for the period 2001–2011 and contained data or at 200 cm height (T200, °C) for 78 weather stations located
for 7 test sites in Saxony. The number of varieties tested in across Germany and period 1994–2009. We estimated the
these trials varied between locations and years with a mini- corresponding relative crop yield by applying an equation
mum of 37 cultivars grown in year 2009 and a maximum of obtained from data collected under a controlled environment
45 cultivars tested in year 2005. For each year and test site the
mean of cultivar specific heading dates, grain number per ear Yrel ‒ heat = 1 − 0.000164 STT (2)
and grain yield was computed from the observations. While
heading date and grain yield was available for every year, where Yrel-heat was grain yield reduced by the effect of heat
data on grain number per ear were missing for the years 2004 stress around flowering [37]. Tg and T200 were extracted
and 2011. Hourly mean of air temperature measured by agro- from a database providing observations for all weather sta-
climatic stations at the variety test sites at 20 cm height (T20, tions that are maintained by the German Meteorological
°C) and at 200 cm height (T200, °C) were extracted from the Service [38]. We selected 78 weather stations located on—or
database of the agro-meteorological service of the state of close to—areas classified as cropland according to the
Saxony [32]. The automated weather stations were placed Corine land cover classification 2006 [39] with complete
above a short grass canopy. The sites Christgrün (50.58 °N, data coverage for the thermal sensitive phase around flow-
12.21 °E, 430 m), Nossen (51.06 °N, 13.27 °E, 255 m), and ering (18 days starting with heading of winter wheat) within
Roda (51.05 °N, 12.62 °E, 224 m) were selected for further the period 1994–2009 and calculated stress thermal time at
analysis because there was complete data coverage for both, 200 cm height (STT200, °C min) and stress thermal time at
weather data and crop data, within the period 2001–2011. The
the ground (STTg, °C min). Heading day at each weather
soil type at the test sites was sandy loam (Christgrün) or loam
station and each year was calculated by linear interpolation
(Nossen, Roda). Long-term annual precipitation sum was
(inverse distance weighting method with 12 neighbours
722 mm yr−1 at Christgrün, 711 mm yr−1 at Roda and 643
mm yr−1 at Nossen, while long-term annual mean temperature and power of 2) of phenological observations provided by
was 7.4 °C at Christgrün, 8.6 °C at Roda and 8.1 °C at Nos- the WebWerdis database [38]. The observations of the
sen. Stress thermal time STT (°C minutes) was computed beginning of heading of winter wheat extracted from the
from hourly mean temperature Th (°C) measured at 20 cm data base of the German Meteorological Service were first
height (STT20, °C minutes) and at 200 cm height (STT200, °C filtered to exclude potential outliers or suspect data from the
minutes) by accumulating temperature sums above a thresh- analysis [40]. The number of heading day observations used
old Tcrit set to 31 °C for an 18-day period starting at the day of as input into the interpolation after application of this fil-
heading: tering procedure varied between 502 in year 2007 and 1373
in year 1995. From the STT computed at the 2 different
STT = ∑ 60 MAX ( Th − Tcrit ; 0) (1)
heights, 78 stations and the period 1994–2009 we then
Experiments undertaken before in climate chambers or computed the annual mean across observation sites and the
plastic tunnels showed that temperatures above this threshold mean across years for each station. In addition, the fre-
cause a reduction of grain number and grain yield of wheat quency of years with heat stress around flowering of winter
[6, 33]. The length of the period around flowering in which wheat was compared.

3
Environ. Res. Lett. 9 (2014) 044012 S Siebert et al

3. Results

3.1. Comparison of canopy and air temperatures measured at


anthesis

Canopy temperature Tc was 19.5 °C–33.5 °C while air tem-


perature measured above the rye canopy T350 varied between
22.0 °C and 26.0 °C (figure 2(a)). In irrigated treatments, Tc
was on average 2 °C lower than T350 while in rainfed treat-
ments Tc was up to 7.5 °C higher than T350. The difference
between Tc and T350 was mainly controlled by soil moisture
(figure 2(a)) and net radiation (figure 2(b)). On sandy rainfed
plots, which had the lowest soil moisture content, Tc was
higher than T350 for almost all measurements. The tempera-
ture difference was low in the morning hours with low net
radiation and increased then to 3–7 °C in the hours with the
highest sun elevation and highest net radiation (figure 2(b)).
The critical temperature threshold of 31 °C reported for wheat
and other temperate cereals [5, 6, 41], was already surpassed
at a T350 of about 25 °C (figure 2(a)). In contrast, Tc was lower
than T350 for almost all measurements at irrigated plots with
largest differences of up to 6 °C in the morning hours
(figure 2(b)). In the period around midday with net radiation
between 400 and 700 W m−2, the temperature difference at
irrigated plots was 0–2 °C (figure 2(b)). Under irrigated
conditions, the canopy temperature Tc was always lower than
26 °C and thus well below the critical threshold of 31 °C.

3.2. Relationship between stress thermal time and grain yield

The decline in grain number per ear with increasing STT,


reported from experiments under controlled conditions
[5, 22, 41], was reproduced well when temperatures mea-
sured at 20 cm height were used to compute STT (figure 3)
while there was no relationship when standard air tempera-
ture measurements at 200 cm height were used (figure 3). A
similar result was obtained when STT was related to relative
crop yield (SI figure 2), which indicates that the decline in Figure 2. Relationship between air temperature 350 cm above
grain number caused by heat stress around anthesis was not ground T350 and canopy temperature Tc (a) and between the
difference Tc − T350 and net radiation at the time of measurement (b)
compensated for in later growing stages. T20 at the three in irrigated (filled symbols) and rainfed (unfilled symbols)
sites in Saxony was up to 7 °C higher than T200 with annual treatments, for sandy (squares) and loamy (circles) soil. Measure-
means of the temperature difference of 1.0–4.7 °C in periods ments are shown for 1920 test plots of 480 inbred lines and hybrids
with a T20 larger than 31 °C (SI figure 2). Consequently, of rye at Wohlde (Germany) on 30 May 2012 (flowering).
Regression lines: loamy irrigated (solid), sandy irrigated (dashed),
STT20 was much higher than STT200 (figure 3 and SI figure loamy rainfed (dotted), sandy rainfed (dotdashed). Depending on
2). Air temperature in the period around anthesis of winter plant height, T350 was measured 200–280 cm above the canopy.
wheat exceeded 31 °C in 5–7, depending on the site, out of
12 years when it was measured at 20 cm height but only in
3.3. Uncertainty in estimates of heat stress impact on wheat
2–3, depending on the site, out of 12 years when it was
yield from air temperatures
measured at 200 cm height (SI figure 2). Linear trends of
relative yield on STT20 were in good agreement to relative We found that mean STT across all stations and years was
yield calculated by applying equation (2) which was derived only 44 °C min when temperature measurements at 200 cm
from experiments under controlled conditions [37]. The height were used but 1366 °C min when temperature was
slope of the trend lines for the three sites in Saxony, indi- measured at the ground, with corresponding declines in crop
cating the yield reduction per °C minutes of STT, was yield estimated by 0.7% and 22.4%, respectively. The mean
−0.000 134 for Christgrün, −0.000 224 for Nossen, and number of years with heat stress across all stations was 2.8
−0.000 335 for Roda. (out of 16 years) when temperature at 200 cm height was used

4
Environ. Res. Lett. 9 (2014) 044012 S Siebert et al

derived stress thermal time and corresponding yield reduction may


not be representative for the whole wheat growing area of Germany.
Heat stress with a canopy temperature of more than 31 °C
typically occurs in the early afternoon on warm days with
clear sky. Standard weather stations are placed on a short
grass so that the ground will heat up in this period resulting in
a temperature gradient of high temperature at the ground (Tg)
to lower temperature at 200 cm height (T200) and intermediate
temperature at 20 cm height (T20) which is also reduced by
the cooling effect of transpiration of the grass vegetation. The
results presented in sections 3.2 and 3.3 suggest that T20
measured on grass might be a better indicator of heat stress in
wheat than T200 or Tg. Unfortunately, T20 is only measured by
Figure 3. Relationship between mean grain number per ear and stress
thermal time calculated from hourly temperature measurements at agro-meteorological stations in Germany so that the data
20 cm height STT20 (°C min) and at 200 cm height STT200 (°C min) coverage for regional scale analyses is very limited.
of winter wheat at three sites in Saxony (Germany). Stress thermal Our results from the field experiment at Wohlde (sec-
time was computed for a period of 18 days starting at heading of tion 3.1) show that canopy temperature can differ sub-
winter wheat by using a temperature threshold of 31 °C, only years stantially from the temperature measured at 200 cm height,
with heat stress during flowering (stress thermal time > 0 °C min) are
shown. which is typically used to assess the impact of the heat stress
on agricultural crops. This is consistent to results of previous
research [13, 43, 44]. The magnitude of the difference
but 11.1 when temperature was measured at the ground between these temperatures depends on weather variables like
(figure 4). Inter-annual variability in STT was large with the incoming radiation, wind speed or humidity, on canopy
highest STT computed for year 2003 and the lowest in year properties like canopy roughness, plant height or LAI, and on
2001. The relative yield reduction due to heat stress estimated actual soil moisture [13, 43, 44]. Under rainfed conditions,
for year 2003 was 75% when using data for temperature that are typical for Germany, we propose that the impact of
measured at the ground and 3% when temperature measured heat stress during flowering would be underestimated for
at 200 cm height was used (figure 4(a)). In addition, we found major cereals like rye and wheat when air temperature mea-
large spatial differences in STT with almost no heat stress sured at 200 cm height was used.
along the coastline and in higher altitudes and hot spots of We suggest that crop models should be improved by
heat stress with highest STT in the river valleys in Southern simulating canopy temperature instead of relying on 200 cm
Germany and in the lowlands of the southern part of Eastern air temperature measured at standard weather stations. An
Germany (figure 4(b)). In contrast to the large uncertainty in alternative might be to use surface temperatures derived by
the magnitude of STT, its spatial pattern was found to be in satellite imagery [45]. Interestingly, remote sensing products
good agreement to means of daily maximum temperature in are used to predict patterns of actual evapotranspiration and
months May and June, measured at 200 cm height corresponding drought stress based on differences in surface
(figure 4(b), SI figure 3). temperature, e.g. by using the SEBAL or METRIC methods
[46–48]. However, currently available sensors do not have the
temporal and spatial resolution required for heat stress
4. Discussion assessments at field scale but may be used to determine the
soil moisture status around flowering at large extent. Because
Due to the thermal gradient in the canopy and typical crop heights of of the dependency of canopy temperature on soil moisture this
German winter wheat between 70 cm and 100 cm, STT computed by information may be well suited to inform models simulating
using ground temperature measured in a short grass canopy (e.g. canopy temperature.
used in section 3.3) will likely represent an overestimate while using Another alternative to account for the difference between
air temperature measured at 200 cm height will underestimate STT canopy temperature and 200 cm air temperature may be to use
and corresponding yield losses, as shown in the previous section. air temperature measured at 200 cm height but to reduce the
According to the German agricultural statistics [42], the lowest winter critical temperature threshold determined by pot experiments
wheat yield in period 1994–2009 was recorded in year 2003 (6.55 under controlled conditions (Tcrit in equation (1)) when cal-
t ha−1) representing a 20% decline to the highest yield reported for culating the heat stress effect. Previous heat stress assess-
year 2004 (8.21 t ha−1), while mean yield reduction across all sites ments performed at the large scale used a wide range of
due to heat stress estimated in this study for year 2003 was 75% thresholds for the critical temperature when heat stress starts,
when using data for Tg and 3% when T200 was used (figure 3). e.g. for wheat a range of 27–31 °C when daily maximum
However, the weather stations, considered in section 3.3, were temperatures were considered [5, 14, 49] or lower thresholds
selected based on the completeness of hourly temperature data of 22–28 °C when mean daytime temperature or mean tem-
resulting in dense station coverage in heat affected regions of Ger- perature in a season were considered [18, 36]. Reducing the
many but low station coverage in the more humid and less heat temperature threshold in the calculation of stress thermal time
affected north-western part of Germany (SI figure 3). Therefore the represents however a simplification which does not account

5
Environ. Res. Lett. 9 (2014) 044012 S Siebert et al

Figure 4. Stress thermal time (STT) during flowering of winter wheat at 78 weather stations across Germany in the period 1994–2009 (°C
minutes). Mean STT across sites and respective mean relative yield reduction according to Ferris et al (2000) [37] computed from hourly
temperatures measured at 200 cm height T200 (open circles) and temperature at the ground Tg (filled circles) (a), mean STT across years and
number of years with a STT > 0 computed from T200 (left) or Tg (right) (b).

for the soil moisture status and other impacts on canopy temperature threshold of 31 °C and STT200 with a threshold
temperature and will thus tend to produce less precise results. ranging between 27 °C and 31 °C for the site Christgrün (SI
We demonstrate this by comparing STT20 calculated with a figure 4). To derive a STT200 similar to STT20 it would be

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Environ. Res. Lett. 9 (2014) 044012 S Siebert et al

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