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LETTERS
                                                                           PUBLISHED ONLINE: 29 JANUARY 2012 | DOI: 10.1038/NCLIMATE1356




Extreme heat effects on wheat senescence in India
David B. Lobell1 *, Adam Sibley1 and J. Ivan Ortiz-Monasterio2

An important source of uncertainty in anticipating the effects               than average, even without differences in precipitation2 . Similarly,
of climate change on agriculture is limited understanding                    wheat-yield variations in India are widely attributed to temperature
of crop responses to extremely high temperatures1,2 . This                   effects, with yields in 2010 reportedly hampered owing to a sudden
uncertainty partly reflects the relative lack of observations                 rise in temperature causing forced maturity12 .
of crop behaviour in farmers’ fields under extreme heat. We                       Although crop-simulation models typically include equations
used nine years of satellite measurements of wheat growth                    to model the effects of temperature on both development and
in northern India to monitor rates of wheat senescence                       grain-filling rates, models differ in exactly how these mechanisms
following exposure to temperatures greater than 34 ◦ C. We                   are treated, particularly for extreme temperatures. For example, the
detect a statistically significant acceleration of senescence                 Agricultural Production Systems Simulator (APSIM) model used in
from extreme heat, above and beyond the effects of increased                 ref. 2 includes a separate equation to speed up senescence for tem-
average temperatures. Simulations with two commonly used                     peratures above 34 ◦ C, which results in a decline in photosynthesis
process-based crop models indicate that existing models                      and grain-filling rates, whereas models such as the widely used Crop
underestimate the effects of heat on senescence. As the                      Environment Resource Synthesis (CERES) model do not13 .
onset of senescence is an important limit to grain filling, and                   Model differences such as this arise because responses to extreme
therefore grain yields, crop models probably underestimate                   heat have been investigated in only a small number of experimental
yield losses for +2 ◦ C by as much as 50% for some sowing                    trials. These trials vary in many aspects, including the variety used,
dates. These results imply that warming presents an even                     air humidity, soil moisture, the speed at which temperatures are
greater challenge to wheat than implied by previous modelling                increased from ambient levels, and the timing, severity and duration
studies, and that the effectiveness of adaptations will depend               of heat exposure in the life cycle1,7,14,15 . Such differences make it hard
on how well they reduce crop sensitivity to very hot days.                   to interpret the often large spread in observed effects of extreme
   Wheat is harvested annually on more than 220 million hectares             heat on grain size, development, senescence or yield. For example,
of cropland, making it the most widely grown crop in the world.              studies carried out in greenhouses can experience unusually high
As a crop that prefers relatively cool temperatures, wheat is sown           levels of humidity, which inhibit transpiration and cause canopy
throughout much of the world in late autumn or early winter                  temperatures to rise markedly above ambient temperatures14 . As
and harvested before early summer. The temperature profile of the            a result of these and other confounding factors, modellers are
wheat growing season in many regions therefore rises towards the             understandably unclear on whether certain processes are important
end, with the hottest conditions experienced during grain filling1 .         enough to include and, if so, how to include them.
   High temperatures affect crop growth at many stages of devel-                 The treatment of extreme heat effects becomes especially impor-
opment and through several different mechanisms. Grain yields                tant when models are used to project the impacts of climate change.
are affected both by changes in grain number, which is determined            The occurrence of extreme heat events is already increasing in many
from 30 days before flowering (or anthesis) until shortly after              parts of the world16 , and will continue to do so throughout the next
anthesis, and grain size, which is determined during grain filling.          few decades regardless of changes in policies affecting greenhouse-
Towards the end of the season, when hot conditions are common                gas emissions17 . Even changes that were once considered rather ex-
in many regions, the most pronounced effect of warming is to                 treme scenarios, such as a 4 ◦ C increase in global mean temperature
shorten the duration of grain filling3,4 . High temperatures can also        over pre-industrial levels (with much larger warming in many crop-
increase the rate of grain filling, but only slightly at temperatures        ping regions), could happen as soon as the early 2060s (ref. 18).
above 20 ◦ C, which fails to compensate for the shortened duration               The high frequency of heat events in plausible future scenarios
and leads to an overall reduction in grain size1,2,5,6 . Above 30 ◦ C,       underscores the importance of understanding crop responses
warming can slow grain-filling rates, in part because the leaf               to extreme temperatures. Additional experiments are certainly
photosynthetic apparatus can be damaged at extreme canopy                    needed, but alternative approaches can also be helpful. Here, we
temperatures, resulting in an acceleration of senescence7–11 .               introduce one such approach, which uses satellite data to develop
   In response to these factors, farmers typically select varieties          a large data set on wheat phenology and daily temperatures in the
that possess a maturity rating well suited to the local climate.             Indo-Gangetic Plains (IGP) in India. This data set is then used
That is, they maximize the period of growth during favourable                to identify the unique effects of extreme heat on wheat through
temperatures while maturing in time to escape excessive heat.                regression analysis. Predictions from the regression model for the
Despite the selection of suitable varieties, however, temperature            effects of different amounts of warming are then compared with
fluctuations from year to year can cause significant changes in              predictions from two process-based crop models, CERES-Wheat
yields. For example, recent simulations of wheat yield in Australia          and APSIM. These comparisons are used to explore whether
found that a growing season that is 2 ◦ C warmer than average has            past projections of wheat responses to warming in this region,
yields that are typically less than 50% of those in years 2 ◦ C cooler       which generally ignore the effects of extreme heat, have accurately



1 Department  of Environmental Earth System Science and Program on Food Security and the Environment, Stanford University, Stanford, California 94305,
USA, 2 International Maize and Wheat Improvement Center (CIMMYT), Global Conservation Agriculture Program, Apdo. Postal 6-641, 06600 Mexico
D.F., Mexico. *e-mail: dlobell@stanford.edu.

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                                                       © 2012 Macmillan Publishers Limited. All rights reserved.
LETTERS                                                                                              NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1356

    a                                      b                    34                                                       c 34

                Punjab
                Haryana                                         32                                                                      32
                   Uttar Pradesh




                                               Latitude (° N)




                                                                                                                       Latitude (° N)
                                                                30                                                                      30


                                                                28                                                                      28


                                                                26                                                                      26

                                                                     74        76       78      80        82   84                            74    76         78      80        82         84
                                                                                        Longitude (° E)                                                       Longitude (° E)

                                                                             310     320 330 340 350 360                                          80       100     120      140      160
                                                                                    Green-up date (day of year)                                        Green-season length (no. days)

Figure 1 | The study region of the IGP in northern India. a, The location of the main study area (outlined) and names of three primary states. b, The
green-up date (day of year) estimated by MODIS for harvest year 2001. c, The green-season length (days from green-up to senescence) estimated by
MODIS for the same year. White areas indicate grid cells with less than 40% wheat, which were not included in this study. A total of 1,638,127 individual
estimates of green-up and season length were used over the study period.

captured the implications of climate change for the future viability                                photosynthetic cells and reductions in photosynthetic rates and
of wheat production in the region.                                                                  viable leaf area when plants are exposed to extreme heat after
                                                                                                    anthesis, for example, refs 10,11. However, these experimental
Results and discussion                                                                              studies provide limited guidance on the quantitative effects of
The study focused on the portion of the IGP in India (Fig. 1a), which                               extreme heat, because they investigate a small number of treatments
is one of the most intensive wheat growing regions in the world, with                               that are difficult to relate to field conditions. The geospatial data
nearly 100% of the wheat area irrigated and average fertilizer rates                                sets used here reflect the behaviour of the wheat varieties grown at
of 145 kg N ha−1 (ref. 19). Patterns of wheat green-up and green                                    present in actual field conditions under actual farmer management.
season length (GSL) derived from the Moderate Resolution Imaging                                    They therefore serve as a valuable confirmation of past experiments,
Spectroradiometer (MODIS) satellite data (Fig. 1) agreed well with                                  and provide a basis for quantifying potential responses to future
previous ground-based studies of sow-date gradients in the study                                    changes in extreme heat.
region20,21 . In particular, wheat is sown earlier in the northwest state                               The MODIS-based regression models for GSL indicate that
of Punjab, and later by a month or more at the eastern edge of Uttar                                warming the region by 2 ◦ C would shorten the photosynthetically
Pradesh and into Bihar (Supplementary Fig. S1 shows a distribution                                  active part of the growing season by roughly nine days, with
of sow dates across the region for all years). The successive delays                                slight variations depending on sow date (Fig. 3a). Simulations with
as one moves eastwards results from several factors, including                                      CERES-Wheat and APSIM indicate significantly less shortening
later sowing and harvesting of rice and slow drainage of fields in                                  of the season, particularly for later sowing dates. For example,
low-lying areas22,23 . Estimates of GSL indicated that later-sown areas                             with 2 ◦ C warming and a sow date of 25 November, the MODIS
tended to have shorter growing cycles, resulting in a much narrower                                 regression shortens the season by roughly nine days compared with
range of harvest dates than sowing dates. This is expected on the                                   six for CERES and only three for APSIM. For the sow date of
basis of previous work showing that wheat develops more quickly                                     10 December, the APSIM season actually becomes longer for a 2 ◦ C
in the warmer temperatures experienced for later sowing, and that                                   warming, which is surprising given that the model contains specific
day length and vernalization sensitivities cause most cultivars grown                               equations to accelerate senescence for extreme heat. This unusual
in the region to develop more slowly when sown earlier24 .                                          behaviour is driven by the thermal-time calculations in APSIM,
    The effects of temperature were assessed by a regression of GSL                                 which like the original version (but unlike the present version)
on measures of cumulative exposure to normal-growing-degree                                         of CERES-Wheat has a triangular response of thermal time to
days (GDD; between 0 and 30 ◦ C) and extreme-growing-degree                                         temperature, with a peak value at 26 ◦ C. Temperatures above 26 ◦ C
days (EDD; above 34 ◦ C). To control for the fact that day length                                   at any point in the season cause a slowing of overall development in
influences development rates, separate regressions were carried                                     APSIM, and in warming scenarios a significant portion of the season
out for early, middle and late sowing dates. A simple plot of the                                   is above this value. Similar artefacts have recently been observed for
average GSL for high and low values of EDD at each value of                                         simulations of rice development at high temperatures that are above
GDD illustrates that GSL is shortened by both high GDD and EDD                                      those for which the crop models are calibrated25 . This erroneous
(Fig. 2a). Regressions for each of the three common dates resulted                                  slowing of development is probably one reason why CERES-Wheat
in a statistically significant effect of both GDD and EDD on GSL,                                   now maintains thermal-time accumulation at maximum rates for
with higher values of each leading to shorter seasons (Fig. 2b).                                    temperatures up to 50 ◦ C.
The coefficients were larger in absolute value for EDD than GDD,                                        The underestimations of season shortening imply that both
indicating that a further degree of warming has a stronger effect on                                CERES and APSIM are underestimating potential yield losses
GSL as temperatures exceed 34 ◦ C. All coefficients were statistically                              for warming in this region, given that reduced season length
significant even after accounting for spatial correlation (p < 0.05),                               is a key mechanism of yield loss under warming. In particular,
consistent across the use of two satellite data sets (Supplementary                                 extreme heat exposure in this region occurs towards the end of
Fig. S3), and robust to the inclusion of rainfall and district-level                                the cycle (Supplementary Fig. S2), which shortens grain-filling
fixed effects in the regression (Supplementary Table S1).                                           duration and slows photosynthesis and grain-filling rates. Using
    The inferred acceleration of senescence is consistent with                                      the relationship between season length and yield change in our
various greenhouse experiments that have documented damage to                                       CERES simulations, we estimated the yield losses associated with

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                                                                          © 2012 Macmillan Publishers Limited. All rights reserved.
NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1356                                                                                                                                                      LETTERS
     a                                                                                                          a
                                      135
                                                                                                                                                                                                            MODIS
                                                                                                                                                                                                            CERES




                                                                                                                         Shortening of season length (no. days)
                                     130                                                                                                                                                                    APSIM
                                                                                                                                                                   8
              Season length (days)




                                      125
                                                                                                                                                                   6
                                     120

                                                                                                                                                                  4
                                      115


                                      110     EDD quartile
                                                                                                                                                                   2
                                                    First
                                                    Fourth
                                     105
                                                                                                                                                                  0
                                            2,200    2,300   2,400   2,500   2,600   2,700    2,800                                                                    10 November   25 November   10 December
                                                                     GDD                                                                                                               Sow date
     b                                                                                                          b
                                                                                                                                                                                                            MODIS
                                                                                                                                                                  20                                        CERES
                                                                                                                                                                                                            APSIM
                                       0
         Coefficient estimates




                                                                                                                                                                  15




                                                                                                                    Yield loss (%)
                                     ¬0.1
                                                                                                                                                                  10


                                     ¬0.2
                                                    GDD                                                                                                            5
                                                    EDD
                                                    PRE

                                     ¬0.3                                                                                                                         0
                                               26 November         11 December       26 December                                                                       10 November   25 November     10 December
                                                      Centre of green-up values (one week)                                                                                              Sow date

Figure 2 | The effects of GDD and EDD on GSL in the study area for                                         Figure 3 | Comparison of MODIS-based responses to crop models.
2000–2009. a, Average GSL for grid cells with green-up on the week                                         a, Estimated response of season length to +2 ◦ C warming based on
centred on 11 December, shown for different GDD and for the top (red) and                                  regression coefficients from MODIS analysis (shown in Fig. 2b) and two
bottom (blue) quartile of EDD at each GDD. High GDD shortens GSL (up to                                    common crop models (CERES-Wheat and APSIM-Wheat). b, The same as
∼2,600 ◦ C per day), and high EDD results in further shortening. Shading                                   in a but showing percentage estimated yield losses. As we did not estimate
indicates ±2σ . b, Estimated coefficients for GDD, EDD and growing season                                   yields directly with MODIS, the yield losses for MODIS were based on the
precipitation (PRE) in a regression to predict GSL for three common                                        relationship between season-length shortening and yield loss as simulated
green-up dates using MODIS data. Error bars indicate 5–95% confidence                                       by CERES. Error bars in both panels show 5–95% confidence interval based
interval, which accounts for heteroskedatic and spatially autocorrelated                                   on 1,000 bootstrap samples for MODIS estimates and 5–95% interval for
errors. Coefficients for GDD and EDD remained significantly negative                                         27 simulations (three sites, nine years) for the crop models.
(p < 0.05) after including district-level fixed effects (Supplementary
Table S1) or using an alternative satellite data set (Supplementary Fig. S3).                              general point exemplified by this study is that phenology patterns
Number of observations (n) = 209,391, n = 253,767 and n = 165,257 for the                                  captured in satellite data over the past decade provide a useful
three respective dates.                                                                                    new data set with which to evaluate the performance of existing
                                                                                                           crop models. Although these models have traditionally been tested
the predicted shortening from the regression model (Fig. 3b).                                              with greenhouse or field-level data, the use of satellite data is
Compared with both CERES and APSIM, losses predicted from the                                              especially relevant to the broader scale questions that crop models
MODIS regression were significantly larger for the two later sow                                           are increasingly used to address.
dates. At the most common sowing date at present of 25 November,
                                                                                                           Methods
for instance, the median yield decline for a +2 ◦ C scenario was 14%                                       Estimates of green-up and senescence dates and GSL across the IGP were obtained
for CERES and 10% for APSIM, whereas the MODIS regression                                                  using vegetation index products derived from two remote-sensing platforms in
indicated a yield loss of 20%. Differences were less pronounced                                            conjunction with established phenology metrics (see Supplementary Information).
for the earlier sowing date, which tended to occur in the western                                          We restricted our analysis to land areas in India above 24◦ N that have at least 40%
portion of the study region where there is less exposure to extreme                                        area sown with wheat according to a global map of wheat-harvested area26 .
                                                                                                                Daily minimum and maximum temperatures (Tmin and Tmax ) were estimated
heat in the growing season (Supplementary Fig. S2).                                                        at each 1-km grid cell using a combination of the Global Summary of the Day
   Overall, the response of wheat senescence to warming evident                                            (GSOD) data set from the National Climate Data Center (http://www.ncdc.noaa.
in the MODIS data indicate greater sensitivities of season length                                          gov/cgi-bin/res40.pl?page=gsod.html) and the high-resolution maps of climatology
and wheat yield to warming than implied by two commonly used                                               provided in the WorldClim database (http://worldclim.org). WorldClim Tmin
crop models. Whether these results hold beyond the crop and region                                         and Tmax maps provide long-term average values on a monthly basis, which we
                                                                                                           interpolated to daily values by fitting a cosine curve at each grid cell. From these
considered in this study is a question for future research to address,                                     daily climatology values we compute daily Tmin and Tmax anomalies for each GSOD
and will probably depend on the degree to which warming results                                            station across India. The anomalies are then interpolated to 1-km grid cells using a
in increased exposure to heat above critical thresholds. A more                                            thin-plate spline with latitude (◦ ), longitude (◦ ) and elevation (km) as covariates.


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                                                                                      © 2012 Macmillan Publishers Limited. All rights reserved.
LETTERS                                                                                   NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1356

Anomalies are interpolated rather than actual station measurements to minimize            8. Harding, S. A., Guikema, J. A. & Paulsen, G. M. Photosynthetic decline from
the effects of missing data27 .                                                               high temperature stress during maturation of wheat: I. Interaction with
     GDD was calculated from hourly temperature values obtained by fitting a sine             senescence processes. Plant Physiol. 92, 648–653 (1990).
curve to daily Tmin and Tmax .                                                            9. Reynolds, M. P., Balota, M., Delgado, M. I. B., Amani, I. & Fischer, R. A.
                                                          if Tt < Tbase                       Physiological and morphological traits associated with spring wheat yield
                                                                          
                        N                      0                          
       GDDbase,opt =       DDt ,  DD =      T − Tbase if Tbase ≤ Tt ≤ Topt                    under hot, irrigated conditions. Aust. J. Plant Physiol. 21, 717–730 (1994).
                      t =1
                                        
                                           Topt − Tbase   if Tt > Topt
                                                                                         10. Al-Khatib, K. & Paulsen, G. M. Mode of high temperature injury to wheat
                                                                                              during grain development. Physiol. Plant. 61, 363–368 (1984).
where t represents the hourly time step, N is the total number of hours in the            11. Al-Khatib, K. & Paulsen, G. M. High-temperature effects on photosynthetic
season and DD represents degree days. We used a base temperature of 0 ◦ C and                 processes in temperate and tropical cereals. Crop Sci. 39, 119–125 (1999).
a maximum temperature of 30 ◦ C. Furthermore, we computed the accumulation                12. Gupta, R. et al. Wheat productivity in indo-gangetic plains of India during
of degree days over 34 ◦ C (Tbase = 34 ◦ C, Topt = ∞), termed EDD. N was based                2010: Terminal heat effects and mitigation strategies. PACA Newsletter 14,
on the average length of GSL for a given sowing date, rather than the GSL of                  1–11 (2010).
each individual pixel, as the latter would lead to endogeneity in an analysis of          13. Wilkens, P. & Singh, U. in Modeling Temperature Response in Wheat and Maize
GDD and EDD effects on GSL (that is, shorter seasons would have lower GDD by                  (ed. White, J. W.) 1–7 (CIMMYT, 2001).
construction). For simplicity, we present results for three representative green-up       14. Stone, P. & Nicolas, M. Wheat cultivars vary widely in their responses of grain
windows: the weeks centred on days 330, 345 and 360 of the year, which span a                 yield and quality to short periods of post-anthesis heat stress. Funct. Plant Biol.
large fraction of the green-up dates in the region (Supplementary Fig. S1). Each              21, 887–900 (1994).
pixel/year combination that fell into one of these three weeks was segregated into a      15. Ferris, R., Ellis, R., Wheeler, T. & Hadley, P. Effect of high temperature stress
separate group, for which average and standard deviation of senescence dates were             at anthesis on grain yield and biomass of field-grown crops of wheat. Ann. Bot.
calculated. The period from average green-up date to average senescence plus one              82, 631–639 (1998).
standard deviation was used as the interval in which to calculate GDD and EDD             16. Zwiers, F. W., Zhang, X. & Feng, Y. Anthropogenic influence on long
for every pixel in the group.                                                                 return period daily temperature extremes at regional scales. J. Clim. 24,
     To estimate effects of heat on GSL, a linear regression was applied to each of           881–892 (2011).
the three aforementioned groups of green-up dates:                                        17. Meehl, G. A. et al. in IPCC Climate Change 2007: The Physical Science Basis
                                                                                              (eds Solomon, S. et al.) (Cambridge Univ. Press, 2007).
                      GSL = β0 + βG GDD + βE EDD + βR RAIN                                18. Betts, R. A. et al. When could global warming reach 4 ◦ C? Phil. Tran. R. Soc. A
                                                                                              369, 67–84 (2011).
Total rainfall for the growing season (RAIN) was included because rainfall might          19. Food and Agriculture Organization of the United Nations. Fertilizer Use by
be correlated with extreme heat and could alleviate moisture stress and therefore             Crop in India (FAO, 2005).
delay senescence. RAIN was estimated using gridded rainfall from NASA (http://            20. Randhawa, A., Dhillon, S. & Singh, D. Productivity of wheat varieties as
power.larc.nasa.gov/). To account for the effects of autocorrelation among the                influenced by the time of sowing. J. Res. Punjab Agr. Univ. 18, 227–233 (1981).
1-km pixels in our study, standard errors for the regression coefficients were            21. Aggarwal, P. K. & Kalra, N. Analyzing the limitations set by climatic factors,
computed using a heteroskedasticity and autocorrelation consistent covariance                 genotype, and water and nitrogen availability on productivity of wheat. 2.
matrix, following the procedure in ref. 28. As an additional robustness check, the            Climatically potential yields and management strategies. Field Crop. Res. 38,
regression was also carried out using district fixed effects to avoid the influence           93–103 (1994).
of omitted variables related to location, such as fertilizer rates or variety selection   22. Chandna, P. et al. Increasing the Productivity of Underutilized Lands by Targeting
(Supplementary Table S1).                                                                     Resource Conserving Technologies-A GIS/Remote Sensing Approach: A Case
      To explore the possible effects of climate change on GSL, using both our                Study of Ballia District, Uttar Pradesh, in the Eastern Gangetic Plains 43
regression model and existing crop models, we selected three sites from each group            (CIMMYT, 2004).
of planting dates. From each group one site was drawn from the fifth, fiftieth and        23. Fujisaka, S., Harrington, L. & Hobbs, P. Rice-wheat in South Asia: Systems
ninety-fifth percentiles in EDD accumulation to ensure that our sites represent               and long-term priorities established through diagnostic research. Agr. Syst. 46,
the full range of possible extreme heat exposure. Daily temperatures at every site            169–187 (1994).
were raised by 1 ◦ C, and GDD and EDD recomputed. The regression equations                24. Ortiz-Monasterio, J. I., Dhillon, S. S. & Fischer, R. A. Date of sowing effects
were then used to predict change in GSL relative to baseline. This process was                on grain-yield and yield components of irrigated spring wheat cultivars and
repeated for 2–4 ◦ C warming.                                                                 relationships with radiation and temperature in Ludhiana, India. Field Crop.
      Finally, using these same sites and temperature records, we ran CERES-Wheat             Res. 37, 169–184 (1994).
and APSIM to obtain process-based model estimates of season shortening and yield          25. van Oort, P. A. J., Zhang, T., de Vries, M. E., Heinemann, A. B. & Meinke, H.
loss. Models were run without nitrogen or water stress. In CERES we used cultivar             Correlation between temperature and phenology prediction error in rice
parameters developed for a similar wheat-growing region of Mexico29 . For APSIM               (Oryza sativa L.). Agr. Forest Meteorol. 151, 1545–1555 (2011).
we chose one of the default cultivars, Zippy, as Zippy vernalization and photoperiod      26. Monfreda, C., Ramankutty, N. & Foley, J. A. Farming the planet: 2. Geographic
sensitivity parameters are reasonable for the area. To be consistent with our method          distribution of crop areas, yields, physiological types, and net primary
of obtaining GSL from satellite data, we used daily model outputs in both cases to            production in the year 2000. Glob. Biogeochem. Cycles 22, GB1022 (2008).
identify the dates when 10% of maximum leaf area was reached on each end of the           27. Mitchell, T. D. & Jones, P. D. An improved method of constructing a
growing season. We also compared the yield outputs for baseline and elevated tem-             database of monthly climate observations and associated high-resolution grids.
perature to calculate percentage yield loss for each year and location in our sample          Int. J. Climatol. 25, 693–712 (2005).
set. Regressing these yield losses against growing season shortening gives an estimate    28. Hsiang, S. M. Temperatures and cyclones strongly associated with economic
of the amount of yield one might expect to lose for each day of shortening in GSL.            production in the Caribbean and Central America. Proc. Natl Acad. Sci. USA
                                                                                              107, 15367–15372 (2010).
Received 11 August 2011; accepted 1 December 2011;                                        29. Lobell, D. B. et al. Analysis of wheat yield and climatic trends in Mexico.
published online 29 January 2012                                                              Field Crop. Res. 94, 250–256 (2005).

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                                                              © 2012 Macmillan Publishers Limited. All rights reserved.
SUPPLEMENTARY INFORMATION
                                                                                                                   DOI: 10.1038/NCLIMATE1356

      Supplementary Information for

      “Extreme heat effects on wheat senescence in India” by Lobell, Sibley, and Ortiz-Monasterio



      Satellite Data Processing Methods:

               We obtained two time series of vegetation index (VI) products spanning the study area for 2000-
      2009. The first was obtained by combining the MOD13A2 (Terra) and MYD13A2 (Aqua) MODIS products
      (available at https://lpdaac.usgs.gov). Each gives the maximum value of the enhanced VI (EVI) over a 16
      day composite window, with an eight day offset between the two products, yielding EVI estimates at
      eight day intervals. A contemporaneous time series of 10 day composite normalized difference VI (NDVI)
      data from the SPOT VEGETATION sensor (available at http://free.vgt.vito.be) was used as a secondary
      source, to ensure that results were robust to the choice of instrument record. Both products cover the
      entire study area at a spatial resolution of 1km.

               For both VI time series we fit double logistic functions to each time series on a pixel-by-pixel
      basis using the Timesat software 1. The double logistic curve has been used extensively to model
      vegetation phenology as its shape closely resembles the VI signature of plants during a growing season 2.
      From our fitted functions we define green-up in each year as the point when the fitted curve reaches
      10% of its maximum amplitude for that year; senescence was defined as the equivalent point on the
      declining portion of the function. Green season length (GSL) was computed each year as the number of
      days between green-up and senescence.

      References:

      1          Jönsson, P. & Eklundh, L. TIMESAT--a program for analyzing time-series of satellite sensor data*
                 1. Computers & Geosciences 30, 833-845 (2004).
      2          Fischer, A. A Simple-Model For the Temporal Variations of Ndvi At Regional- Scale Over
                 Agricultural Countries - Validation With Ground Radiometric Measurements. International
                 Journal of Remote Sensing 15, 1421-1446 (1994).




NATURE CLIMATE CHANGE | www.nature.com/natureclimatechange	                                                                                    1

                                                       © 2012 Macmillan Publishers Limited. All rights reserved.
Table S1. Regression coefficients for models with and without district fixed-effects for three different
green-up dates. Values in parentheses indicate standard errors, and stars indicate statistical significance
(**: p< 0.05). Standard errors were computed to account for heteroskedatic and spatially auto-
correlated errors.

             Standard Regression                                      Fixed Effects Model
             GDD           EDD                   Precip               GDD            EDD              Precip
Day 330      -0.03**         -0.122**            0.013**              -0.017**             -0.131**   0.017**

             (0.002)         (0.034)             (0.063)              (0.003)              (0.029)    (0.006)

Day 345      -0.031**        -0.216**            -0.009**             -0.007**             -0.24**    0.004

             (0.003)         (0.05)              (0.055)              (0.004)              (0.038)    (0.008)

Day 360      -0.04**         -0.151**            -0.057**             -0.262**             -0.25**    0.008

             (0.004)         (0.042)             (0.063)              (0.004)              (0.04)     (0.01)




                                       © 2012 Macmillan Publishers Limited. All rights reserved.
Supplementary Figure Captions:

   1. Histogram of green-up dates estimated from MODIS for harvest years 2000-2009. Shaded bars
      indicate three 7-day windows used for regression analysis.

   2. Average number of days within each month of the growing season when maximum daily
      temperatures exceeded 34 °C for 2000-2009 in study region. No areas experienced 34 °C during
      December-February (top right). Extreme heat occurs mainly during the grain filling period of
      wheat, in March and April.

   3. Estimate of regression coefficients for GDD, EDD, and growing season rainfall in a model to
      predict GSL for three common green-up dates using SPOT-VGT data. Error bars indicate 5-95%
      confidence interval, and were computed to account for heteroskedatic and spatially auto-
      correlated errors. (Same as Figure 2b in main paper but for SPOT-VGT instead of MODIS data)




                                  © 2012 Macmillan Publishers Limited. All rights reserved.
Figure S1. Histogram of green-up dates estimated from MODIS for harvest years 2000-2009. Shaded bars
indicate three 7-day windows used for regression analysis.




                                  © 2012 Macmillan Publishers Limited. All rights reserved.
Figure S2. Average number of days within each month of the growing season when maximum daily
temperatures exceeded 34 °C for 2000-2009 in study region. No areas experienced 34 °C during
December-February (top right). Extreme heat occurs mainly during the grain filling period of wheat, in
March and April.




                                    © 2012 Macmillan Publishers Limited. All rights reserved.
Figure S3. Estimate of regression coefficients for GDD, EDD, and growing season rainfall in a model to
predict GSL for three common green-up dates using SPOT-VGT data. Error bars indicate 5-95%
confidence interval, and were computed to account for heteroskedatic and spatially auto-correlated
errors. (Same as Figure 2b in main paper but for SPOT-VGT instead of MODIS data)




                                    © 2012 Macmillan Publishers Limited. All rights reserved.

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Lobell etal 2012_nclimate1356

  • 1. LETTERS PUBLISHED ONLINE: 29 JANUARY 2012 | DOI: 10.1038/NCLIMATE1356 Extreme heat effects on wheat senescence in India David B. Lobell1 *, Adam Sibley1 and J. Ivan Ortiz-Monasterio2 An important source of uncertainty in anticipating the effects than average, even without differences in precipitation2 . Similarly, of climate change on agriculture is limited understanding wheat-yield variations in India are widely attributed to temperature of crop responses to extremely high temperatures1,2 . This effects, with yields in 2010 reportedly hampered owing to a sudden uncertainty partly reflects the relative lack of observations rise in temperature causing forced maturity12 . of crop behaviour in farmers’ fields under extreme heat. We Although crop-simulation models typically include equations used nine years of satellite measurements of wheat growth to model the effects of temperature on both development and in northern India to monitor rates of wheat senescence grain-filling rates, models differ in exactly how these mechanisms following exposure to temperatures greater than 34 ◦ C. We are treated, particularly for extreme temperatures. For example, the detect a statistically significant acceleration of senescence Agricultural Production Systems Simulator (APSIM) model used in from extreme heat, above and beyond the effects of increased ref. 2 includes a separate equation to speed up senescence for tem- average temperatures. Simulations with two commonly used peratures above 34 ◦ C, which results in a decline in photosynthesis process-based crop models indicate that existing models and grain-filling rates, whereas models such as the widely used Crop underestimate the effects of heat on senescence. As the Environment Resource Synthesis (CERES) model do not13 . onset of senescence is an important limit to grain filling, and Model differences such as this arise because responses to extreme therefore grain yields, crop models probably underestimate heat have been investigated in only a small number of experimental yield losses for +2 ◦ C by as much as 50% for some sowing trials. These trials vary in many aspects, including the variety used, dates. These results imply that warming presents an even air humidity, soil moisture, the speed at which temperatures are greater challenge to wheat than implied by previous modelling increased from ambient levels, and the timing, severity and duration studies, and that the effectiveness of adaptations will depend of heat exposure in the life cycle1,7,14,15 . Such differences make it hard on how well they reduce crop sensitivity to very hot days. to interpret the often large spread in observed effects of extreme Wheat is harvested annually on more than 220 million hectares heat on grain size, development, senescence or yield. For example, of cropland, making it the most widely grown crop in the world. studies carried out in greenhouses can experience unusually high As a crop that prefers relatively cool temperatures, wheat is sown levels of humidity, which inhibit transpiration and cause canopy throughout much of the world in late autumn or early winter temperatures to rise markedly above ambient temperatures14 . As and harvested before early summer. The temperature profile of the a result of these and other confounding factors, modellers are wheat growing season in many regions therefore rises towards the understandably unclear on whether certain processes are important end, with the hottest conditions experienced during grain filling1 . enough to include and, if so, how to include them. High temperatures affect crop growth at many stages of devel- The treatment of extreme heat effects becomes especially impor- opment and through several different mechanisms. Grain yields tant when models are used to project the impacts of climate change. are affected both by changes in grain number, which is determined The occurrence of extreme heat events is already increasing in many from 30 days before flowering (or anthesis) until shortly after parts of the world16 , and will continue to do so throughout the next anthesis, and grain size, which is determined during grain filling. few decades regardless of changes in policies affecting greenhouse- Towards the end of the season, when hot conditions are common gas emissions17 . Even changes that were once considered rather ex- in many regions, the most pronounced effect of warming is to treme scenarios, such as a 4 ◦ C increase in global mean temperature shorten the duration of grain filling3,4 . High temperatures can also over pre-industrial levels (with much larger warming in many crop- increase the rate of grain filling, but only slightly at temperatures ping regions), could happen as soon as the early 2060s (ref. 18). above 20 ◦ C, which fails to compensate for the shortened duration The high frequency of heat events in plausible future scenarios and leads to an overall reduction in grain size1,2,5,6 . Above 30 ◦ C, underscores the importance of understanding crop responses warming can slow grain-filling rates, in part because the leaf to extreme temperatures. Additional experiments are certainly photosynthetic apparatus can be damaged at extreme canopy needed, but alternative approaches can also be helpful. Here, we temperatures, resulting in an acceleration of senescence7–11 . introduce one such approach, which uses satellite data to develop In response to these factors, farmers typically select varieties a large data set on wheat phenology and daily temperatures in the that possess a maturity rating well suited to the local climate. Indo-Gangetic Plains (IGP) in India. This data set is then used That is, they maximize the period of growth during favourable to identify the unique effects of extreme heat on wheat through temperatures while maturing in time to escape excessive heat. regression analysis. Predictions from the regression model for the Despite the selection of suitable varieties, however, temperature effects of different amounts of warming are then compared with fluctuations from year to year can cause significant changes in predictions from two process-based crop models, CERES-Wheat yields. For example, recent simulations of wheat yield in Australia and APSIM. These comparisons are used to explore whether found that a growing season that is 2 ◦ C warmer than average has past projections of wheat responses to warming in this region, yields that are typically less than 50% of those in years 2 ◦ C cooler which generally ignore the effects of extreme heat, have accurately 1 Department of Environmental Earth System Science and Program on Food Security and the Environment, Stanford University, Stanford, California 94305, USA, 2 International Maize and Wheat Improvement Center (CIMMYT), Global Conservation Agriculture Program, Apdo. Postal 6-641, 06600 Mexico D.F., Mexico. *e-mail: dlobell@stanford.edu. NATURE CLIMATE CHANGE | ADVANCE ONLINE PUBLICATION | www.nature.com/natureclimatechange 1 © 2012 Macmillan Publishers Limited. All rights reserved.
  • 2. LETTERS NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1356 a b 34 c 34 Punjab Haryana 32 32 Uttar Pradesh Latitude (° N) Latitude (° N) 30 30 28 28 26 26 74 76 78 80 82 84 74 76 78 80 82 84 Longitude (° E) Longitude (° E) 310 320 330 340 350 360 80 100 120 140 160 Green-up date (day of year) Green-season length (no. days) Figure 1 | The study region of the IGP in northern India. a, The location of the main study area (outlined) and names of three primary states. b, The green-up date (day of year) estimated by MODIS for harvest year 2001. c, The green-season length (days from green-up to senescence) estimated by MODIS for the same year. White areas indicate grid cells with less than 40% wheat, which were not included in this study. A total of 1,638,127 individual estimates of green-up and season length were used over the study period. captured the implications of climate change for the future viability photosynthetic cells and reductions in photosynthetic rates and of wheat production in the region. viable leaf area when plants are exposed to extreme heat after anthesis, for example, refs 10,11. However, these experimental Results and discussion studies provide limited guidance on the quantitative effects of The study focused on the portion of the IGP in India (Fig. 1a), which extreme heat, because they investigate a small number of treatments is one of the most intensive wheat growing regions in the world, with that are difficult to relate to field conditions. The geospatial data nearly 100% of the wheat area irrigated and average fertilizer rates sets used here reflect the behaviour of the wheat varieties grown at of 145 kg N ha−1 (ref. 19). Patterns of wheat green-up and green present in actual field conditions under actual farmer management. season length (GSL) derived from the Moderate Resolution Imaging They therefore serve as a valuable confirmation of past experiments, Spectroradiometer (MODIS) satellite data (Fig. 1) agreed well with and provide a basis for quantifying potential responses to future previous ground-based studies of sow-date gradients in the study changes in extreme heat. region20,21 . In particular, wheat is sown earlier in the northwest state The MODIS-based regression models for GSL indicate that of Punjab, and later by a month or more at the eastern edge of Uttar warming the region by 2 ◦ C would shorten the photosynthetically Pradesh and into Bihar (Supplementary Fig. S1 shows a distribution active part of the growing season by roughly nine days, with of sow dates across the region for all years). The successive delays slight variations depending on sow date (Fig. 3a). Simulations with as one moves eastwards results from several factors, including CERES-Wheat and APSIM indicate significantly less shortening later sowing and harvesting of rice and slow drainage of fields in of the season, particularly for later sowing dates. For example, low-lying areas22,23 . Estimates of GSL indicated that later-sown areas with 2 ◦ C warming and a sow date of 25 November, the MODIS tended to have shorter growing cycles, resulting in a much narrower regression shortens the season by roughly nine days compared with range of harvest dates than sowing dates. This is expected on the six for CERES and only three for APSIM. For the sow date of basis of previous work showing that wheat develops more quickly 10 December, the APSIM season actually becomes longer for a 2 ◦ C in the warmer temperatures experienced for later sowing, and that warming, which is surprising given that the model contains specific day length and vernalization sensitivities cause most cultivars grown equations to accelerate senescence for extreme heat. This unusual in the region to develop more slowly when sown earlier24 . behaviour is driven by the thermal-time calculations in APSIM, The effects of temperature were assessed by a regression of GSL which like the original version (but unlike the present version) on measures of cumulative exposure to normal-growing-degree of CERES-Wheat has a triangular response of thermal time to days (GDD; between 0 and 30 ◦ C) and extreme-growing-degree temperature, with a peak value at 26 ◦ C. Temperatures above 26 ◦ C days (EDD; above 34 ◦ C). To control for the fact that day length at any point in the season cause a slowing of overall development in influences development rates, separate regressions were carried APSIM, and in warming scenarios a significant portion of the season out for early, middle and late sowing dates. A simple plot of the is above this value. Similar artefacts have recently been observed for average GSL for high and low values of EDD at each value of simulations of rice development at high temperatures that are above GDD illustrates that GSL is shortened by both high GDD and EDD those for which the crop models are calibrated25 . This erroneous (Fig. 2a). Regressions for each of the three common dates resulted slowing of development is probably one reason why CERES-Wheat in a statistically significant effect of both GDD and EDD on GSL, now maintains thermal-time accumulation at maximum rates for with higher values of each leading to shorter seasons (Fig. 2b). temperatures up to 50 ◦ C. The coefficients were larger in absolute value for EDD than GDD, The underestimations of season shortening imply that both indicating that a further degree of warming has a stronger effect on CERES and APSIM are underestimating potential yield losses GSL as temperatures exceed 34 ◦ C. All coefficients were statistically for warming in this region, given that reduced season length significant even after accounting for spatial correlation (p < 0.05), is a key mechanism of yield loss under warming. In particular, consistent across the use of two satellite data sets (Supplementary extreme heat exposure in this region occurs towards the end of Fig. S3), and robust to the inclusion of rainfall and district-level the cycle (Supplementary Fig. S2), which shortens grain-filling fixed effects in the regression (Supplementary Table S1). duration and slows photosynthesis and grain-filling rates. Using The inferred acceleration of senescence is consistent with the relationship between season length and yield change in our various greenhouse experiments that have documented damage to CERES simulations, we estimated the yield losses associated with 2 NATURE CLIMATE CHANGE | ADVANCE ONLINE PUBLICATION | www.nature.com/natureclimatechange © 2012 Macmillan Publishers Limited. All rights reserved.
  • 3. NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1356 LETTERS a a 135 MODIS CERES Shortening of season length (no. days) 130 APSIM 8 Season length (days) 125 6 120 4 115 110 EDD quartile 2 First Fourth 105 0 2,200 2,300 2,400 2,500 2,600 2,700 2,800 10 November 25 November 10 December GDD Sow date b b MODIS 20 CERES APSIM 0 Coefficient estimates 15 Yield loss (%) ¬0.1 10 ¬0.2 GDD 5 EDD PRE ¬0.3 0 26 November 11 December 26 December 10 November 25 November 10 December Centre of green-up values (one week) Sow date Figure 2 | The effects of GDD and EDD on GSL in the study area for Figure 3 | Comparison of MODIS-based responses to crop models. 2000–2009. a, Average GSL for grid cells with green-up on the week a, Estimated response of season length to +2 ◦ C warming based on centred on 11 December, shown for different GDD and for the top (red) and regression coefficients from MODIS analysis (shown in Fig. 2b) and two bottom (blue) quartile of EDD at each GDD. High GDD shortens GSL (up to common crop models (CERES-Wheat and APSIM-Wheat). b, The same as ∼2,600 ◦ C per day), and high EDD results in further shortening. Shading in a but showing percentage estimated yield losses. As we did not estimate indicates ±2σ . b, Estimated coefficients for GDD, EDD and growing season yields directly with MODIS, the yield losses for MODIS were based on the precipitation (PRE) in a regression to predict GSL for three common relationship between season-length shortening and yield loss as simulated green-up dates using MODIS data. Error bars indicate 5–95% confidence by CERES. Error bars in both panels show 5–95% confidence interval based interval, which accounts for heteroskedatic and spatially autocorrelated on 1,000 bootstrap samples for MODIS estimates and 5–95% interval for errors. Coefficients for GDD and EDD remained significantly negative 27 simulations (three sites, nine years) for the crop models. (p < 0.05) after including district-level fixed effects (Supplementary Table S1) or using an alternative satellite data set (Supplementary Fig. S3). general point exemplified by this study is that phenology patterns Number of observations (n) = 209,391, n = 253,767 and n = 165,257 for the captured in satellite data over the past decade provide a useful three respective dates. new data set with which to evaluate the performance of existing crop models. Although these models have traditionally been tested the predicted shortening from the regression model (Fig. 3b). with greenhouse or field-level data, the use of satellite data is Compared with both CERES and APSIM, losses predicted from the especially relevant to the broader scale questions that crop models MODIS regression were significantly larger for the two later sow are increasingly used to address. dates. At the most common sowing date at present of 25 November, Methods for instance, the median yield decline for a +2 ◦ C scenario was 14% Estimates of green-up and senescence dates and GSL across the IGP were obtained for CERES and 10% for APSIM, whereas the MODIS regression using vegetation index products derived from two remote-sensing platforms in indicated a yield loss of 20%. Differences were less pronounced conjunction with established phenology metrics (see Supplementary Information). for the earlier sowing date, which tended to occur in the western We restricted our analysis to land areas in India above 24◦ N that have at least 40% portion of the study region where there is less exposure to extreme area sown with wheat according to a global map of wheat-harvested area26 . Daily minimum and maximum temperatures (Tmin and Tmax ) were estimated heat in the growing season (Supplementary Fig. S2). at each 1-km grid cell using a combination of the Global Summary of the Day Overall, the response of wheat senescence to warming evident (GSOD) data set from the National Climate Data Center (http://www.ncdc.noaa. in the MODIS data indicate greater sensitivities of season length gov/cgi-bin/res40.pl?page=gsod.html) and the high-resolution maps of climatology and wheat yield to warming than implied by two commonly used provided in the WorldClim database (http://worldclim.org). WorldClim Tmin crop models. Whether these results hold beyond the crop and region and Tmax maps provide long-term average values on a monthly basis, which we interpolated to daily values by fitting a cosine curve at each grid cell. From these considered in this study is a question for future research to address, daily climatology values we compute daily Tmin and Tmax anomalies for each GSOD and will probably depend on the degree to which warming results station across India. The anomalies are then interpolated to 1-km grid cells using a in increased exposure to heat above critical thresholds. A more thin-plate spline with latitude (◦ ), longitude (◦ ) and elevation (km) as covariates. NATURE CLIMATE CHANGE | ADVANCE ONLINE PUBLICATION | www.nature.com/natureclimatechange 3 © 2012 Macmillan Publishers Limited. All rights reserved.
  • 4. LETTERS NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE1356 Anomalies are interpolated rather than actual station measurements to minimize 8. Harding, S. A., Guikema, J. A. & Paulsen, G. M. Photosynthetic decline from the effects of missing data27 . high temperature stress during maturation of wheat: I. Interaction with GDD was calculated from hourly temperature values obtained by fitting a sine senescence processes. Plant Physiol. 92, 648–653 (1990). curve to daily Tmin and Tmax . 9. Reynolds, M. P., Balota, M., Delgado, M. I. B., Amani, I. & Fischer, R. A. if Tt < Tbase Physiological and morphological traits associated with spring wheat yield   N  0  GDDbase,opt = DDt , DD = T − Tbase if Tbase ≤ Tt ≤ Topt under hot, irrigated conditions. Aust. J. Plant Physiol. 21, 717–730 (1994). t =1  Topt − Tbase if Tt > Topt  10. Al-Khatib, K. & Paulsen, G. M. Mode of high temperature injury to wheat during grain development. Physiol. Plant. 61, 363–368 (1984). where t represents the hourly time step, N is the total number of hours in the 11. Al-Khatib, K. & Paulsen, G. M. High-temperature effects on photosynthetic season and DD represents degree days. We used a base temperature of 0 ◦ C and processes in temperate and tropical cereals. Crop Sci. 39, 119–125 (1999). a maximum temperature of 30 ◦ C. Furthermore, we computed the accumulation 12. Gupta, R. et al. Wheat productivity in indo-gangetic plains of India during of degree days over 34 ◦ C (Tbase = 34 ◦ C, Topt = ∞), termed EDD. N was based 2010: Terminal heat effects and mitigation strategies. PACA Newsletter 14, on the average length of GSL for a given sowing date, rather than the GSL of 1–11 (2010). each individual pixel, as the latter would lead to endogeneity in an analysis of 13. Wilkens, P. & Singh, U. in Modeling Temperature Response in Wheat and Maize GDD and EDD effects on GSL (that is, shorter seasons would have lower GDD by (ed. White, J. W.) 1–7 (CIMMYT, 2001). construction). For simplicity, we present results for three representative green-up 14. Stone, P. & Nicolas, M. Wheat cultivars vary widely in their responses of grain windows: the weeks centred on days 330, 345 and 360 of the year, which span a yield and quality to short periods of post-anthesis heat stress. Funct. Plant Biol. large fraction of the green-up dates in the region (Supplementary Fig. S1). Each 21, 887–900 (1994). pixel/year combination that fell into one of these three weeks was segregated into a 15. Ferris, R., Ellis, R., Wheeler, T. & Hadley, P. Effect of high temperature stress separate group, for which average and standard deviation of senescence dates were at anthesis on grain yield and biomass of field-grown crops of wheat. Ann. Bot. calculated. The period from average green-up date to average senescence plus one 82, 631–639 (1998). standard deviation was used as the interval in which to calculate GDD and EDD 16. Zwiers, F. W., Zhang, X. & Feng, Y. Anthropogenic influence on long for every pixel in the group. return period daily temperature extremes at regional scales. J. Clim. 24, To estimate effects of heat on GSL, a linear regression was applied to each of 881–892 (2011). the three aforementioned groups of green-up dates: 17. Meehl, G. A. et al. in IPCC Climate Change 2007: The Physical Science Basis (eds Solomon, S. et al.) (Cambridge Univ. Press, 2007). GSL = β0 + βG GDD + βE EDD + βR RAIN 18. Betts, R. A. et al. When could global warming reach 4 ◦ C? Phil. Tran. R. Soc. A 369, 67–84 (2011). Total rainfall for the growing season (RAIN) was included because rainfall might 19. Food and Agriculture Organization of the United Nations. Fertilizer Use by be correlated with extreme heat and could alleviate moisture stress and therefore Crop in India (FAO, 2005). delay senescence. RAIN was estimated using gridded rainfall from NASA (http:// 20. Randhawa, A., Dhillon, S. & Singh, D. Productivity of wheat varieties as power.larc.nasa.gov/). To account for the effects of autocorrelation among the influenced by the time of sowing. J. Res. Punjab Agr. Univ. 18, 227–233 (1981). 1-km pixels in our study, standard errors for the regression coefficients were 21. Aggarwal, P. K. & Kalra, N. Analyzing the limitations set by climatic factors, computed using a heteroskedasticity and autocorrelation consistent covariance genotype, and water and nitrogen availability on productivity of wheat. 2. matrix, following the procedure in ref. 28. As an additional robustness check, the Climatically potential yields and management strategies. Field Crop. Res. 38, regression was also carried out using district fixed effects to avoid the influence 93–103 (1994). of omitted variables related to location, such as fertilizer rates or variety selection 22. Chandna, P. et al. Increasing the Productivity of Underutilized Lands by Targeting (Supplementary Table S1). Resource Conserving Technologies-A GIS/Remote Sensing Approach: A Case To explore the possible effects of climate change on GSL, using both our Study of Ballia District, Uttar Pradesh, in the Eastern Gangetic Plains 43 regression model and existing crop models, we selected three sites from each group (CIMMYT, 2004). of planting dates. From each group one site was drawn from the fifth, fiftieth and 23. Fujisaka, S., Harrington, L. & Hobbs, P. Rice-wheat in South Asia: Systems ninety-fifth percentiles in EDD accumulation to ensure that our sites represent and long-term priorities established through diagnostic research. Agr. Syst. 46, the full range of possible extreme heat exposure. Daily temperatures at every site 169–187 (1994). were raised by 1 ◦ C, and GDD and EDD recomputed. The regression equations 24. Ortiz-Monasterio, J. I., Dhillon, S. S. & Fischer, R. A. Date of sowing effects were then used to predict change in GSL relative to baseline. This process was on grain-yield and yield components of irrigated spring wheat cultivars and repeated for 2–4 ◦ C warming. relationships with radiation and temperature in Ludhiana, India. Field Crop. Finally, using these same sites and temperature records, we ran CERES-Wheat Res. 37, 169–184 (1994). and APSIM to obtain process-based model estimates of season shortening and yield 25. van Oort, P. A. J., Zhang, T., de Vries, M. E., Heinemann, A. B. & Meinke, H. loss. Models were run without nitrogen or water stress. In CERES we used cultivar Correlation between temperature and phenology prediction error in rice parameters developed for a similar wheat-growing region of Mexico29 . For APSIM (Oryza sativa L.). Agr. Forest Meteorol. 151, 1545–1555 (2011). we chose one of the default cultivars, Zippy, as Zippy vernalization and photoperiod 26. Monfreda, C., Ramankutty, N. & Foley, J. A. Farming the planet: 2. Geographic sensitivity parameters are reasonable for the area. To be consistent with our method distribution of crop areas, yields, physiological types, and net primary of obtaining GSL from satellite data, we used daily model outputs in both cases to production in the year 2000. Glob. Biogeochem. Cycles 22, GB1022 (2008). identify the dates when 10% of maximum leaf area was reached on each end of the 27. Mitchell, T. D. & Jones, P. D. An improved method of constructing a growing season. We also compared the yield outputs for baseline and elevated tem- database of monthly climate observations and associated high-resolution grids. perature to calculate percentage yield loss for each year and location in our sample Int. J. Climatol. 25, 693–712 (2005). set. Regressing these yield losses against growing season shortening gives an estimate 28. Hsiang, S. M. Temperatures and cyclones strongly associated with economic of the amount of yield one might expect to lose for each day of shortening in GSL. production in the Caribbean and Central America. Proc. Natl Acad. Sci. USA 107, 15367–15372 (2010). Received 11 August 2011; accepted 1 December 2011; 29. Lobell, D. B. et al. Analysis of wheat yield and climatic trends in Mexico. published online 29 January 2012 Field Crop. Res. 94, 250–256 (2005). References Acknowledgements 1. Wardlaw, I. & Wrigley, C. Heat tolerance in temperate cereals: An overview. We thank the APSIM team for providing their model and S. Hsiang for providing the Aust. J. Plant Physiol. 21, 695–703 (1994). code to estimate heteroskedasticity- and autocorrelation-consistent standard errors. This 2. Asseng, S., Foster, I. & Turner, N. C. The impact of temperature variability on work was supported by the Rockefeller Foundation and NASA New Investigator grant wheat yields. Glob. Change Biol. 17, 997–1012 (2011). no. NNX08AV25G to D.B.L. 3. Ritchie, J. T. & NeSmith, D. S. in Modeling Plant and Soil Systems Vol. 31 (eds Hanks, J. & Ritchie, J. T.) 5–29 (American Society of Agronomy, 1991). 4. Tashiro, T. & Wardlaw, I. F. A comparison of the effect of high temperature on Author contributions grain development in wheat and rice. Ann. Bot. 64, 59–65 (1989). D.B.L. conceived the study, D.B.L. and A.S. analysed data, A.S. carried out crop model 5. Wardlaw, I. & Moncur, L. The response of wheat to high temperature following simulations, and D.B.L., A.S. and J.I.O-M. interpreted results and wrote the paper. anthesis. I. The rate and duration of kernel filling. Funct. Plant Biol. 22, 391–397 (1995). 6. Sofield, I., Evans, L., Cook, M. & Wardlaw, I. Factors influencing the rate and Additional information duration of grain filling in wheat. Funct. Plant Biol. 4, 785–797 (1977). The authors declare no competing financial interests. Supplementary information 7. Zhao, H., Dai, T., Jing, Q., Jiang, D. & Cao, W. Leaf senescence and grain filling accompanies this paper on www.nature.com/natureclimatechange. Reprints and affected by post-anthesis high temperatures in two different wheat cultivars. permissions information is available online at http://www.nature.com/reprints. Plant Growth Regul. 51, 149–158 (2007). Correspondence and requests for materials should be addressed to D.B.L. 4 NATURE CLIMATE CHANGE | ADVANCE ONLINE PUBLICATION | www.nature.com/natureclimatechange © 2012 Macmillan Publishers Limited. All rights reserved.
  • 5. SUPPLEMENTARY INFORMATION DOI: 10.1038/NCLIMATE1356 Supplementary Information for “Extreme heat effects on wheat senescence in India” by Lobell, Sibley, and Ortiz-Monasterio Satellite Data Processing Methods: We obtained two time series of vegetation index (VI) products spanning the study area for 2000- 2009. The first was obtained by combining the MOD13A2 (Terra) and MYD13A2 (Aqua) MODIS products (available at https://lpdaac.usgs.gov). Each gives the maximum value of the enhanced VI (EVI) over a 16 day composite window, with an eight day offset between the two products, yielding EVI estimates at eight day intervals. A contemporaneous time series of 10 day composite normalized difference VI (NDVI) data from the SPOT VEGETATION sensor (available at http://free.vgt.vito.be) was used as a secondary source, to ensure that results were robust to the choice of instrument record. Both products cover the entire study area at a spatial resolution of 1km. For both VI time series we fit double logistic functions to each time series on a pixel-by-pixel basis using the Timesat software 1. The double logistic curve has been used extensively to model vegetation phenology as its shape closely resembles the VI signature of plants during a growing season 2. From our fitted functions we define green-up in each year as the point when the fitted curve reaches 10% of its maximum amplitude for that year; senescence was defined as the equivalent point on the declining portion of the function. Green season length (GSL) was computed each year as the number of days between green-up and senescence. References: 1 Jönsson, P. & Eklundh, L. TIMESAT--a program for analyzing time-series of satellite sensor data* 1. Computers & Geosciences 30, 833-845 (2004). 2 Fischer, A. A Simple-Model For the Temporal Variations of Ndvi At Regional- Scale Over Agricultural Countries - Validation With Ground Radiometric Measurements. International Journal of Remote Sensing 15, 1421-1446 (1994). NATURE CLIMATE CHANGE | www.nature.com/natureclimatechange 1 © 2012 Macmillan Publishers Limited. All rights reserved.
  • 6. Table S1. Regression coefficients for models with and without district fixed-effects for three different green-up dates. Values in parentheses indicate standard errors, and stars indicate statistical significance (**: p< 0.05). Standard errors were computed to account for heteroskedatic and spatially auto- correlated errors. Standard Regression Fixed Effects Model GDD EDD Precip GDD EDD Precip Day 330 -0.03** -0.122** 0.013** -0.017** -0.131** 0.017** (0.002) (0.034) (0.063) (0.003) (0.029) (0.006) Day 345 -0.031** -0.216** -0.009** -0.007** -0.24** 0.004 (0.003) (0.05) (0.055) (0.004) (0.038) (0.008) Day 360 -0.04** -0.151** -0.057** -0.262** -0.25** 0.008 (0.004) (0.042) (0.063) (0.004) (0.04) (0.01) © 2012 Macmillan Publishers Limited. All rights reserved.
  • 7. Supplementary Figure Captions: 1. Histogram of green-up dates estimated from MODIS for harvest years 2000-2009. Shaded bars indicate three 7-day windows used for regression analysis. 2. Average number of days within each month of the growing season when maximum daily temperatures exceeded 34 °C for 2000-2009 in study region. No areas experienced 34 °C during December-February (top right). Extreme heat occurs mainly during the grain filling period of wheat, in March and April. 3. Estimate of regression coefficients for GDD, EDD, and growing season rainfall in a model to predict GSL for three common green-up dates using SPOT-VGT data. Error bars indicate 5-95% confidence interval, and were computed to account for heteroskedatic and spatially auto- correlated errors. (Same as Figure 2b in main paper but for SPOT-VGT instead of MODIS data) © 2012 Macmillan Publishers Limited. All rights reserved.
  • 8. Figure S1. Histogram of green-up dates estimated from MODIS for harvest years 2000-2009. Shaded bars indicate three 7-day windows used for regression analysis. © 2012 Macmillan Publishers Limited. All rights reserved.
  • 9. Figure S2. Average number of days within each month of the growing season when maximum daily temperatures exceeded 34 °C for 2000-2009 in study region. No areas experienced 34 °C during December-February (top right). Extreme heat occurs mainly during the grain filling period of wheat, in March and April. © 2012 Macmillan Publishers Limited. All rights reserved.
  • 10. Figure S3. Estimate of regression coefficients for GDD, EDD, and growing season rainfall in a model to predict GSL for three common green-up dates using SPOT-VGT data. Error bars indicate 5-95% confidence interval, and were computed to account for heteroskedatic and spatially auto-correlated errors. (Same as Figure 2b in main paper but for SPOT-VGT instead of MODIS data) © 2012 Macmillan Publishers Limited. All rights reserved.