OENO One Resilience of grapevine yield in response to warming Sadras VO * 1 Moran MA 1 Petrie PR 1 2 1 1South Australian Research and Development Institute, Waite Campus, Australia2Australian Wine Research Institute, Waite Campus, Australia Abstract

Aim : To evaluate the effect of elevated temperature on the yield of Shiraz vines in the Barossa Valley of Australia.

Methods and r esults: We compiled and analysed 37 pair-wise yield comparisons between heated and control vines spaning seven consecutive vintages from 2009-10. Heating with open-top chambers increased daily average temperature by approx. 2 °C above ambient in realistic vineyard conditions, in comparison to 0.9 to 2.9 °C projected warming for south-eastern Australia (2030-2070). The combination of seasons, varieties, fruit loads, pruning times, and water regimes returned an 8.5-fold variation in the yield of unheated vines. Warming had no statistically significant effect on yield in 32 out of 37 comparisons, reduced yield in 2 and increased yield in 3.

Conclusion: Projected warming is unlikely to cause widespread reduction of yield in environments with thermal regimes similar to Barossa Valley; extrapolation to cooler or warmer regions is not warranted.

Significance and impact of the study: The relevance of this finding is three-fold. First, it demonstrates vine resilience against the target of the Paris Agreement setting a long-term goal of holding global warming below 2 °C. Second, further research on adaptation to warming needs to focus on logistic issues such as early harvest, and fruit composition with implications for wine quality, rather than yield. Third, this summary data set is a robust reference to benchmark time-series and modelling analysis of vine yield in response to warming.

Key words: projected warming, grapevine, yield, modelling analysis, adaptation

Introduction

As with most horticultural crops, the growers of premium wine grapes regulate yields to achieve higher quality and profit (Lentz, 1998); management practices to regulate grapevine yield (Clingeleffer, 2010) need to be considered in the context of global warming. Evidence from time-series analysis of realised warming, experiments, and modelling projections into future climates indicate the potential for elevated temperature to affect yield, fruit traits and wine attributes (Barnuud et al., 2014; Bergqvist et al., 2001; Bindi et al., 1996; Bonada et al., 2013; Bonada et al., 2015; Bowen et al., 2004; Hannah et al., 2013; Rienth et al., 2016; Sadras and Moran, 2012; Sadras and Moran, 2013; Sadras et al., 2013a; Sadras et al., 2013b; Santos et al., 2013; van Leeuwen et al., 2013). Different approaches and assumptions used in modelling and time-series studies lead to results of varying reliability, as reviewed by Bonada and Sadras (2015). These authors also emphasised two distinct effects of global warming: the gradual increase in background temperature, and the increasing incidence of heat waves; this paper deals with the former.

As a perennial, the fruit yield of grapevines is determined by the conditions over successive seasons, where multiple developmental stages are responsive to the environment, genotype, management, and their interactions (Dry, 2000; Dunn, 2005; Vasconcelos et al., 2009). Generally higher temperature increases the number of bunches and the number of berries per bunch, hence increasing yield (Srinivasan and Mullins, 1981). However, most of these relationships are non-linear (Buttrose, 1974) and at some developmental stages high temperature can reduce yield components; for example, high temperature immediately prior to budburst can reduce flower number (Petrie and Clingeleffer, 2005). Intra-specific variation in thermal adaptation in grapevine is large; for example, increasing temperature from 20 to 30 °C increased the weight of bunch primordia 4-fold in Riesling, but did not change the size of bud primordia in Shiraz (Dunn, 2005). Canopy growth, mostly driven by water availability and management practices such as pruning, interacts with the environment to influence yield (Dry, 2000).

In comparison to annual crops where robust models are used routinely in studies of climate change (e.g. Asseng et al., 2013), we have a limited ability to predict yield and its responses to temperature in long-lived perennials including grapevine, where models are less developed (Bindi et al., 1996; Santos et al., 2011). Hence, the experimental quantification of the effect of high temperature on yield is particularly important in perennials.

We have devised open-top chambers (Figure 1ab) to increase daily average temperature by approx. 2 °C above ambient in realistic vineyard conditions (Sadras and Soar, 2009; Sadras et al., 2012a). This compares with the range from 0.9 to 2.9 °C for projected global warming depending on the time frame (2030, 2070) and modelling scenario (Webb et al., 2013). Using these systems, we measured and reported yield response to warming from three experiments comprising 20 pair-wise comparisons between heated and control treatments in the vintages 2009-10 to 2011-12 (Sadras and Moran, 2013). The aim of this article is to consolidate this data set, and expand it to 37 pair-wise comparisons including four additional vintages from 2012-13 to 2015-16. First, we compare actual and long-term temperature records to identify potential bias in the environments sampled during the experiments; for example, actual temperatures below long-term average would bias results in the direction of more likely positive warming effect on yield. Then, we analyse the pair-wise yields of heated and control vines for the whole data set in the seven vintages from 2009-10.

Background temperature

Way and Oren (2010) reviewed the response to temperature of trees in a meta-analysis showing enhanced growth in deciduous more than in evergreen trees and in temperate and boreal species more than in their tropical counterparts. This highlights the differential impact of elevated temperature depending on the background temperature; 2 °C warming, for example, is more likely to return positive effects in a cool viticultural region, and more likely to return negative effects in an already hot region (Bentzen and Smith, 2009; Deluze, 2010; Jones et al., 2005).

To account for background temperature in our trials, we compared the long-term climate records and the actual temperature during the seven vintages when we measure yield (Figure 1c). The experiments spanned the climatic range from percentiles 10th to 90th at the beginning (September) and end of the season (March). The core of the season, from October to February, was mostly close to or above the median long-term temperatures. October 2013 and 2014, November 2009 and 2012, and December 2015 were particularly hot, with monthly means above the 90th percentile. In only one out of seven seasons, January temperature was below median, and February temperature was never below median. The prevailing warmer-than-median conditions during the experiments (Figure 1c) indicates that bias, if any, was in the direction of over-estimating the negative impact of the heating treatment.

Measured yield response to warming

We conducted four experiments, where two thermal regimes (heated, control) were combined with either: (1) four varieties over three seasons (2009-10 to 2011-12), (2) two fruit loads over two seasons (2010-11, 2011-12), (3) two water regimes over six seasons (2010-11 to 2015-16), and (4) three pruning times over three seasons (2014-15 to 2015-16). Experiment 1 included Cabernet franc, Shiraz, Semillon and Chardonnay, and experiments 2-4 were with Shiraz. Clones and rootstocks, planting pattern, vineyard practices, experimental design and detail of thermal regimes and vine water status have been presented previously (Sadras et al., 2012b).

The combination of seasons, varieties, fruit loads, pruning times, and water regimes returned an 8.5-fold variation in the yield of unheated vines (Figure 1d). Figure 1e shows the pair-wise comparisons for all these combinations. Warming had no significant effect on yield in 32 out of 37 cases, reduced yield in 2 and increased yield in 3 (P = 0.05). Reductions in yield were 22% for Shiraz in 2010 (exp. 1), and 34% for vines pruned at budburst in 2016 (exp. 4). Warming increased yield 2.0-2.8 fold in both irrigated and water-deficit vines in 2012 (exp. 3), and 1.5 fold in winter-pruned vines in 2014 (exp. 4). This asymmetry, whereby the magnitude of yield enhancement was larger than the magnitude of reduction, was noticed and discussed previously (Sadras and Moran, 2013).

Interpretation of our results and extrapolation to other sites needs caution because plant responses to warming are influenced by background temperature, as discussed before, and other factors such as water and nutrient availability and interactions with pathogens (Ac et al., 2015; Downey, 2012; Ko et al., 2010; Piedallu et al., 2016; Sadras and Moran, 2013; Xu and Zhou, 2005). Our trials were limited to a red brown earth (Northcote, 1979) on a single site; this may restrict conclusions for other soils, particularly important to capture interactions between temperature and water availability. Experiment 3, however, combined thermal and water regimes over six seasons, where yield was reduced from 2.6-8.9 kg/plant in irrigated vines to 1.8-4.6 kg/plant under water deficit (Figure 1d). Despite these severe water restrictions, warming did not reduce yield in five seasons, and substantially increased yield in both irrigated and water-deficit vines in 2012 (Figure 1e, blue symbols). Wet weather in 2010-11 favoured fungal diseases in south-eastern Australia, and vines under elevated temperature showed lower incidence of Botrytis bunch rot (Botrytis spp) in the Barossa Valley (Sadras and Moran, 2013) and lower incidence of downy mildew (Plasmopara viticola) in the trials at Sunraysia (Downey, 2012) in comparison to vines under ambient temperature.

We conclude that projected warming is unlikely to be detrimental for vine yield in environments with thermal regimes similar to Barossa Valley (Figure 1c) for vineyards in a range from 1.2 to 10.5 kg/plant (Figure 1d). Occasional yield reductions are likely to be compensated by yield enhancement, depending on seasonal conditions. The relevance of this finding is three-fold. First, it demonstrates vine resilience (sensu Doring et al., 2015) against the target of the Paris Agreement setting a long-term temperature goal of holding the global average temperature increase to well below 2 °C (Schleussner et al., 2016). Second, research effort on adaptation to warming needs to focus on logistic issues such as early harvest, and fruit composition with implications for wine, rather than yield. Third, this summary data set is a useful reference to benchmark time-series and modelling analysis of vine yield in response to warming, and more broadly, the yield response of long-lived perennial plants. Extrapolation to cooler or warmer regions is not warranted.

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Figure 1 - Resilience of grapevine yield in response to warming.

(a, b). Large-scale open-top chambers used in experiments 1, 2 and 4 (a), and 3 (b). (c) Comparison of actual mean monthly temperature in seven growing seasons (points) and long-term (1957-2016) monthly temperature (lines) in the Barossa Valley, Australia. Lines are, from bottom to top, 10th, 25th, 50th, 75th and 90th percentiles. (d) Yield of unheated controls, and (e) difference between heated and control treatments in experiments where two thermal regimes (heated, control) were combined with either: (exp. 1, black symbols) four varieties over three seasons (2009-10 to 2011-12), (exp. 2, green symbols) two fruit loads over two seasons (2010-11, 2011-12), (exp. 3, blue symbols) two water regimes over six seasons (2010-11 to 2015-16), and (exp. 4, grey symbols) three pruning times over three seasons (2014-15 to 2015-16). Error bars are two standard deviations and asterisks indicate significant warming effect (t-test, P ≤ 0.05). Sources: (a) Sadras and Soar (2009); (b) Sadras et al. (2012a); (c) Queensland Government SILO Climate Data (www.longpaddock.qld.gov.au/silo/); (d-e) Sadras et al. (2013a, b); Sadras et al. (2014); Sadras et al. (2015); Moran, Petrie and Sadras (unpublished).

Figure 1 - Resilience of grapevine yield in response to warming.

(a, b). Large-scale open-top chambers used in experiments 1, 2 and 4 (a), and 3 (b). (c) Comparison of actual mean monthly temperature in seven growing seasons (points) and long-term (1957-2016) monthly temperature (lines) in the Barossa Valley, Australia. Lines are, from bottom to top, 10th, 25th, 50th, 75th and 90th percentiles. (d) Yield of unheated controls, and (e) difference between heated and control treatments in experiments where two thermal regimes (heated, control) were combined with either: (exp. 1, black symbols) four varieties over three seasons (2009-10 to 2011-12), (exp. 2, green symbols) two fruit loads over two seasons (2010-11, 2011-12), (exp. 3, blue symbols) two water regimes over six seasons (2010-11 to 2015-16), and (exp. 4, grey symbols) three pruning times over three seasons (2014-15 to 2015-16). Error bars are two standard deviations and asterisks indicate significant warming effect (t-test, P ≤ 0.05). Sources: (a) Sadras and Soar (2009); (b) Sadras et al. (2012a); (c) Queensland Government SILO Climate Data (www.longpaddock.qld.gov.au/silo/); (d-e) Sadras et al. (2013a, b); Sadras et al. (2014); Sadras et al. (2015); Moran, Petrie and Sadras (unpublished).

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Acknowledgements: Our work was funded by Wine Australia and the Department of Agriculture.

Ac A. Malenovsky Z. , Olejnickova J. , Galle A. , Rascher U. and Mohammed G. (2015) . Meta-analysis assessing potential of steady-state chlorophyll fluorescence for remote sensing detection of plant water, temperature and nitrogen stress. Remote Sensing of Environment, 420-436. doi:10./j.rse..07.022, 168. Asseng S. , Ewert F. , Rosenzweig C. , Jones J. W. , Hatfield J. L. , Ruane A.C. and Wolf J. (2013) . Uncertainty in simulating wheat yields under climate change. Nature Climate Change, 827-832. doi:10./nclimate, 3(9). Barnuud N.N. , Zerihun A. , Gibberd M. and Bates B. (2014) . Berry composition and climate: responses and empirical models. International Journal of Biometeorology, -. doi:10./s4-013--2, 58(6). Bentzen J. and Smith V. (2009) . Wine production in Denmark. Do the characteristics of the vineyards affect the chances for awards? Aarhus University, Working Paper 09-21. . Bergqvist J. , Dokoozlian N. and Ebisuda N. (2001) . Sunlight exposure and temperature effects on berry growth and composition of Cabernet-Sauvignon and Grenache in the central San Joaquin Valley of California. American Journal of Enology and Viticulture, 52(1), 1-7. . Bindi M. , Fibbi L. , Gozzini B. , Orlandini S. and Miglietta F. (1996) . Modelling the impact of future climate scenarios on yield and yield variability of grapevine. Climate Research, 213-224. doi:10./cr13, 7(3). Bonada M. and Sadras V.O. (2015) . Review: critical appraisal of methods to investigate the effect of temperature on grapevine berry composition. Australian Journal of Grape and Wine Research, 1-17. doi:10./ajgw.2, 21(1). Bonada M. , Sadras V. , Moran M. and Fuentes S. (2013) . Elevated temperature and water stress accelerate mesocarp cell death and shrivelling, and decouple sensory traits in Shiraz berries. Irrigation Science, -. doi:10./s1-013--z, 31(6). Bonada M. , Jeffery D.W. Petrie P R. , Moran M. A. and Sadras V.O. (2015) . Impact of elevated temperature and water deficit on the chemical and sensory profiles of Barossa Shiraz grapes and wines. Australian Journal of Grape and Wine Research, 240-253. doi:10./ajgw.2, 21(2). Bowen P.A. , Bogdanoff C.P. and Estergaard B. (2004) . Impacts of using polyethylene sleeves and wavelength selective mulch in vineyards. II. Effects on growth, 555-568. doi:10./P03-094, leaf gas exchange, 84(2). Buttrose M.S. (1974) . Climatic factors and fruitfulness in grapevines. Horticultural Abstracts, 44, 319-326. . Clingeleffer and P. R. (2010) . Plant management research: status and what it can offer to address challenges and limitations. Australian Journal of Grape and Wine Research, 25-32. doi:10./j.-..5.x, 16(s1). Deluze A. (2010) . What future for the Champagne industry? American Association of Wine Economists, Working Paper 64. . Doring T.F. , Vieweger A. , Pautasso M. , Vaarst M. , Finckh M.R. and Wolfe M.S. (2015) . Resilience as a universal criterion of health. Journal of the Science of Food and Agriculture, 455-465. doi:10./jsfa, 95(3). Downey M.O. (2012) . Strategies to maintain productivity and quality in a changing environment - Impacts of global warming on grape and wine production. Final report to the GWRDC. . Dry P.R. (2000) . Canopy management for fruitfulness. Australian Journal of Grape and Wine Research, 109-115. doi:10./j.-..tb8.x, 6(2). Dunn G.M. (2005) . Factors that control flower formation in grapevines. Paper presented at the Australian Society for Viticulture and Oenology Workshop Proceedings - Transforming Flowers to Fruit, Mildura, Australia. . Hannah L. , Roehrdanz P.R. , Ikegami M. , Shepard A.V. , Shaw M.R. , Tabor G. and Hijmans R.J. (2013) . Climate change, wine, and conservation. Proceedings of the National Academy of Sciences of the United States of America, -. doi:10./pnas.10, 110(17). Jones G.V. , White M.A. , Cooper O.R. and Storchmann K. (2005) . Climate change and global wine quality. Climatic Change, 319-343. doi:10./s4-005--2, 73(3). Ko J. , Ahuja L. , Kimball B. , Anapalli S. , Ma L.W. , Green T.R. and Bader D.A. (2010) . Simulation of free air CO2 enriched wheat growth and interactions with water, nitrogen, and temperature. Agricultural and Forest Meteorology, -. doi:10./j.agrformet..06.004, 150(10). Lentz W. (1998) . Model applications in horticulture: a review. Scientia Horticulturae, 151-174. doi:10./S-(98)5-5, 74(1-2). Northcote K. (1979) . A factual key for the recognition of Australian soils. Rellim Technical Publications: Glenside, S.A. Petrie P.R. and Clingeleffer P.R. (2005) . Effects of temperature and light (before and after budburst) on inflorescence morphology and flower number of Chardonnay grapevines (Vitis vinifera L. ). Australian Journal of Grape and Wine Research, 59-65. doi:10./j.-..tb9.x, 11(1). Piedallu C. , Gegout J.C. , Lebourgeois F. and Seynave I. (2016) . Soil aeration, water deficit, nitrogen availability, acidity and temperature all contribute to shaping tree species distribution in temperate forests. Journal of Vegetation Science, 387-399. doi:10./jvs.0, 27(2). Rienth M. , Torregrosa L. , Sarah G. , Ardisson M. , Brillouet J.-M. and Romieu C. (2016) . Temperature desynchronizes sugar and organic acid metabolism in ripening grapevine fruits and remodels their transcriptome. BMC Plant Biology, 1-23. doi:10./s0-016--0, 16(1). Sadras V.O. and Soar C.J. (2009) . Shiraz vines maintain yield in response to a 2-4 degrees C increase in maximum temperature using an open-top heating system at key phenostages. European Journal of Agronomy, 250-258. doi:10./j.eja..09.004, 31(4). Sadras V.O. and Moran M.A. (2012) . Elevated temperature decouples anthocyanins and sugars in berries of Shiraz and Cabernet Franc. Australian Journal of Grape and Wine Research, 115-122. doi:10./j.-..0.x, 18(2). Sadras V.O. and Moran M.A. (2013) . Asymmetric warming effect on the yield and source:sink ratio of field-grown grapevine. Agricultural and Forest Meteorology, 116-126. doi:10./j.agrformet..12.005, 173. Sadras V.O. , Bubner R. and Moran M.A. (2012) . a. A large-scale, 187-194. doi:10./j.agrformet..11.005, 154-155. Sadras V.O. , Moran M.A. and Petrie P.R. (2012) . b. A window into hotter and drier futures: phenological shifts and adaptive practices. Final report to the GWRDC. . Sadras V.O. , Moran M.A. , and Bonada M. (2013) . a. Effects of elevated temperature in grapevine. I. Berry sensory traits. Australian Journal of Grape and Wine Research, 95-106. doi:10./ajgw.7, 19(1). Sadras V.O. and Petrie P.R.and Moran M.A. (2013) . b. Effects of elevated temperature in grapevine. II. Juice pH, 107-115. doi:10./ajgw.1, titratable acidity and wine sensory attributes. Australian Journal of Grape and Wine Research, 19(1). Sadras V.O. , Petrie P.R. and Moran M.A. (2014) . Yield of Shiraz in response to warming and late pruning. Australian and New Zealand Grapegrower & Winemaker, 605(June), 38-39. . Sadras V.O. , Petrie P.R. and Moran M.A. (2015) . Delayed pruning shifted Shiraz maturity by two weeks in . Australian and New Zealand Grapegrower & Winemaker, 617(June), 66-67. . Santos J.A. , Malheiro A.C. , Karremann M.K. and Pinto J.G. (2011) . Statistical modelling of grapevine yield in the Port Wine region under present and future climate conditions. International Journal of Biometeorology, 119-131. doi:10./s4-010--0, 55(2). Santos J.A. , Gratsch S.D. , Karremann M.K. , Jones G.V. and Pinto J.G. (2013) . Ensemble projections for wine production in the Douro Valley of Portugal. Climatic Change, 211-225. doi:10./s4-012--x, 117(1-2). Schleussner C.-F. , Rogelj J. , Schaeffer M. , Lissner T. , Licker R. , Fischer E.M. and Hare W. (2016) . Science and policy characteristics of the Paris Agreement temperature goal. Nature Climate Change, 827-835. doi:10./nclimate, 6(9). Srinivasan C. and Mullins M.G. (1981) . Physiology of flowering in the grapevine - A review. American Journal of Enology and Viticulture, 32, 47-63. . van Leeuwen C. , Schultz H.R. , Garcia de Cortazar-Atauri I. , Duchêne E. , Ollat N. , Pieri P. and Delrot S. (2013) . Why climate change will not dramatically decrease viticultural suitability in main wine-producing areas by . Proceedings of the National Academy of Sciences of the United States of America, E-E. doi:10./pnas.10, 110(33). Vasconcelos M.C. , Greven M. , Winefield C.S. , Trought M.C.T. and Raw V. (2009) . The flowering process of Vitis vinifera: a review. American Journal of Enology and Viticulture, 60, 411-434. . Way D.A. and Oren R. (2010) . Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiology, 669-688. doi:10./treephys/tpq015, 30(6). Webb L.B. , Watterson I. , Bhend J. , Whetton P.H. and Barlow E.W.R. (2013) . Global climate analogues for winegrowing regions in future periods: projections of temperature and precipitation. Australian Journal of Grape and Wine Research, 331-341. doi:10./ajgw.5, 19(3). Xu Z.Z. and Zhou G.S. (2005) . Effects of water stress and high nocturnal temperature on photosynthesis and nitrogen level of a perennial grass Leymus chinensis. Plant and Soil, 131-139. doi:10./s4-004--y, 269(1-2).