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Range Size and Growth Temperature Influence Eucalyptus Species Responses to an Experimental Heatwave

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Macquarie University PURE Research Management System This is the peer reviewed version of the following article: Aspinwall, M.J., Pfautsch, S., Tjoelker, M.G., et al. (2019), Range size and growth temperature influence Eucalyptus species responses to an experimental heatwave. Global Change Biology, vol. 25, no. 5, pp. 1665– 1684. which has been published in final form at: https://doi.org/10.1111/gcb.14590 This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. 1 DR. MICHAEL J ASPINWALL (Orcid ID : 0000-0003-0199-2972) DR. JOHN E DRAKE (Orcid ID : 0000-0003-1758-2169) DR. OWEN K ATKIN (Orcid ID : 0000-0003-1041-5202) Article type : Primary Research Articles Range size and growth temperature influence Eucalyptus species responses to an experimental heatwave Running title: mechanisms of tree heatwave tolerance Michael J. Aspinwall1,2*, Sebastian Pfautsch1, Mark G. Tjoelker1, Angelica Vårhammar1, Malcolm Possell3, John E. Drake1,4, Peter B. Reich1,5, David T. Tissue1, Owen K. Atkin6, Paul D. Rymer1, Siobhan Dennison7, Steven C. Van Sluyter7 1Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith NSW 2751, Australia 2Department of Biology, University of North Florida, 1 UNF Drive, Jacksonville FL 32224 USA 3School of Life and Environmental Sciences, University of Sydney, Sydney, NSW 2006, Australia 4Forest and Natural Resources Management, SUNY-ESF, 1 Forestry Drive, Syracuse, NY, 13210 USA. 5Department of Forest Resources, University of Minnesota, 1530 Cleveland Ave N., St Paul, MN 55108, USA 6Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia 7Department of Biological Science, Macquarie University, North Ryde, NSW 2109 Australia *Corresponding author:Author Manuscript email: [email protected], phone: +1-904-620-5626 This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/GCB.14590 This article is protected by copyright. All rights reserved 2 This article is protected by copyright. All rights reserved 3 Abstract Understanding forest tree responses to climate warming and heatwaves is important for predicting changes in tree species diversity, forest C uptake, and vegetation – climate interactions. Yet, tree species differences in heatwave tolerance and their plasticity to growth temperature remain poorly understood. In this study, populations of four Eucalyptus species, two with large range sizes and two with comparatively small range sizes, were grown under two temperature treatments (cool, warm) before being exposed to an equivalent experimental heatwave. We tested whether the species with large and small range sizes differed in heatwave tolerance, and whether trees grown under warmer temperatures were more tolerant of heatwave conditions than trees grown under cooler temperatures. Visible heatwave damage was more common and severe in the species with small rather than large range sizes. In general, species that showed less tissue damage maintained higher stomatal conductance, lower leaf temperatures, larger increases in isoprene emissions and less photosynthetic inhibition than species that showed more damage. Species exhibiting more severe visible damage had larger increases in heat shock proteins (HSPs) and respiratory thermotolerance (Tmax). Thus, across species, increases in HSPs and Tmax were positively correlated, but inversely related to increases in isoprene emissions. Integration of leaf-gas exchange, isoprene emissions, proteomics, and respiratory thermotolerance measurements provided new insight into mechanisms underlying variability in tree species heatwave tolerance. Importantly, warm-grown seedlings were, surprisingly, more susceptible to heatwave damage than cool-grown seedlings, which could be associated with reduced enzyme concentrations in leaves. We conclude that species with restricted range sizes, along with trees growing under climate warming, may be more vulnerable to heatwaves of the future. Keywords: forests, heat shock proteins (HSPs), heat stress, isoprene, photosynthesis, thermal acclimation Introduction Extreme climatic events (i.e., drought, heatwaves, floods) are the hallmark of contemporary climate change (Collins et al., 2013; Meehl & Tebaldi, 2004). These extreme events are expected to exert stronger selective pressures on organisms than gradual changes in mean climatic conditions (Gutschick & BassiriRad, 2003; Parmesan, 2006; Reyer et al., 2013). Heatwaves, This article is protected by copyright. All rights reserved 4 loosely defined as a period of consecutive (>3) excessively hot days (Perkins & Alexander, 2013), are extreme climatic events that could negatively impact the function and survival of organisms; in some regions, the frequency, intensity, and duration of heatwaves are increasing (Coumou & Robinson, 2013; Seneviratne, Donat, Mueller & Alexander, 2014). The potential for heatwaves to negatively impact the persistence of species, and the diversity and function of ecosystems, underscores the need for determining the patterns and mechanisms underlying variation in organismal responses to heatwaves (Buckley & Huey, 2016). Plant species with large geographic range sizes may cope better with climate change and extreme events than species with smaller range sizes (Aitken, Yeaman, Holliday, Wang & Curtis-McLane, 2008; González-Orozco et al., 2016; Pacifi et al., 2015; Thuiller, Lavorel & Araújo, 2005). This prediction is based on the expectation that species with broad climatic distributions possess wider environmental tolerances, thereby allowing them to inhabit a broader range of habitats (Hamrick, Godt & Sherman-Broyles,1992; Leimu, Mutikainen, Koricheva & Fischer, 2006; Morin & Thuiller, 2009; Slayter, Hirst & Sexton, 2013). Yet, predicting species responses to climate change based on range size alone has its limitations (Pacifi et al., 2015; Pearson & Dawson, 2003), and empirical tests of the relationship between species range size and vulnerability to climate change are rare (Fensham, Fraser, Macdermott & Firn, 2015; Lacher & Schwartz, 2016). Heatwaves are also occurring under background temperatures that are, on average, warmer (Collins et al., 2013). It is not clear how plants growing and existing in warmer climates will respond to heatwaves. Plants often acclimate photosynthetic and respiratory rates in response to long-term warming (Aspinwall et al., 2016; Atkin & Tjoelker, 2003; Gunderson, Norby & Wullschleger, 2000; Slot & Kitajima, 2015), yet the role of thermal acclimation in conferring high-temperature tolerance is not known. A few studies have shown that trees exposed to short-term warming or high temperature events (minutes, hours) exhibit less tissue damage and physiological stress when exposed to extended heatwaves, compared to trees with no such history (Colombo & Timmer, 1992; Daas, Montpied, Hanchi & Dreyer, 2008; Ghouil et al., 2003; Niinemets, 2010). Yet, Drake et al. (2018) found that Eucalyptus parramattensis trees grown at ambient and warmed (+3 °C) temperatures showed equivalent physiological responses and coped equally well with an experimental heatwave of four consecutive days with This article is protected by copyright. All rights reserved 5 temperatures > 43 °C. Additional studies are needed to assess how trees living in a warmed climate will respond to heatwaves of the future. Prolonged exposure to excessively high temperatures can impact plant performance at multiple scales (shown conceptually in Figure 1). High air temperatures directly affect leaf temperature (Tleaf), and along with associated increases in vapor pressure deficit of the atmosphere (VPD) influence stomatal conductance (gs), which in union with VPD modifies Tleaf via the extent of transpirational cooling. As Tleaf increases beyond the optimum temperature of photosynthesis, net photosynthesis (A) is reduced by several related processes (Lin, Medlyn & Ellsworth, 2012) including reduced gs, increased photo- and mitochondrial (i.e. dark) respiration (R, von Caemmerer & Quick, 2000; Peñuelas & Llusià, 2002), inhibition of Rubisco activase and deactivation of Rubisco (Hozain, Salvucci, Fokar & Holaday, 2010; Law & Crafts-Brandner, 1999; Salvucci & Crafts-Brandner, 2004), as well as damage to photosystem II (Allakhverdiev et al., 2008; Wise, Olson, Schrader & Sharkey, 2004). Excessively high Tleaf also (i) stimulates the synthesis of isoprene (Is) (among isoprene emitting species) which may help stabilize thylakoid membranes (Monson et al., 1992; Pollastri, Tsonev & Loreto, 2014; Singaas, Lerdau, Winter & Sharkey, 1997; Velikova et al., 2011; Vickers, Gershenzon, Lerdau & Loreto, 2009), and (ii) can increase production of heat shock proteins (HSPs) that act as chaperonins for other proteins, protect against oxidative damage, and stabilize cellular membranes (Figure 1, Heckathorn, Downs, Sharkey & Coleman, 1998; Mittler, 2002; Vierling, 1991). A few studies have demonstrated that tree species may vary in their physiological and biochemical responses to heatwaves (Ameye et al., 2012; Guha, Han, Cummings, McLennan & Warren, 2018; Wujeska-Klause, Bossinger & Tausz, 2015). Even when high temperatures reduce A, some tree species maintain high gs (and transpiration) which
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