Where and when does stem cellulose δ18O reflect a leaf water enrichment signal?

Early studies of oxygen isotope composition (δO) of cellulose noted strong relationships with mean annual temperature and humidity (Libby et al. 1976, Burk and Stuiver 1981). Since then the δO signals in plant materials have become increasingly important for the reconstruction of paleoclimates and plant physiological responses to environmental variation. Many researchers have contributed to advancing how we understand the primary controls on the δO composition of plant materials, but arguably the most influential of these were experimental and modeling studies (Sternberg et al. 1986, Yakir and DeNiro 1990, Roden et al. 2000). Thereafter, many studies have clarified various controls over leaf water enrichment and the subsequent incorporation of these δO signals in cellulose (Barbour et al. 2004, Kahmen et al. 2011, Voelker et al. 2014, Cernusak et al. 2016). In parallel to these advancements was the wider application of δO for analyses of tree-rings. For example, tree-ring δO has been used to reconstruct precipitation δO in relatively humid locations (Miller et al. 2006, Brienen et al. 2012, Boysen et al. 2014), whereas in other locations tree-ring δO often reflects evaporative demand—some combination of vapor pressure deficit, relative humidity and sunshine (Roden and Ehleringer 2007, Labuhn et al. 2014, Xu et al. 2011, Hartl-Meier et al. 2015). Where tree-ring δO clearly reflects more than one driving variable, it can often still be used to improve paleoclimatic signals within a multi-proxy framework (Loader et al. 2008, Etien et al. 2009, Berkelhammer and Stott 2012, Johnstone et al. 2013, Schollaen et al. 2013, Voelker et al. 2014, 2015). Finally, treering cellulose δO used within a mechanistic modeling framework has elucidated patterns in leaf temperature (Helliker and Richter 2008, Song et al. 2011), and when combined with carbon isotope variation of the same plant materials, has been used to infer how environmental variation has impacted stomatal conductance versus photosynthetic assimilation rates (Scheidegger et al. 2000, Brooks and Coulombe 2009, Barnard et al. 2012, Guerrieri et al. 2016, Jennings et al. 2016). The original Roden et al. (2000) mechanistic model of cellulose δO lacks some complexities that could potentially modify our conventional interpretations of climatic signals imprinted upon tree-ring δO (Sternberg and Ellsworth 2011, Gessler et al. 2014, Song et al. 2014). In this issue of Tree Physiology, Cheesman and Cernusak (2017) reveal yet another layer of complexity that is vexing to the conventional knowledge of controls on tree-ring δO. In their study, stem water and leaf and branch cellulose of five Eucalyptus and three Corymbia species were sampled across 11 sites representing a strong aridity gradient across northeastern Australia. The difference between leaf cellulose δO and source water δO could largely be explained using a slightly modified version of the conventional steady state models for leaf water and cellulose δO (i.e., Roden et al. 2000, Barbour et al. 2004). However, the difference between stem cellulose δO and source water δO was not affected by aridity as expected. In essence, their data, when combined with those of two other studies (Cooper and Solis 2003, Kahmen et al. 2011), suggest that the leaf water enrichment signal can be almost completely obscured by a post-photosynthetic process that is strongly correlated in space with relative humidity (Figure 1). If this were a generalizable phenomenon it would be contrary to many studies using stem cellulose δO as a record of evaporative enrichment within the now commonly applied