The foliar physiognomic methods discussed here (leaf margin analysis, CLAMP (Climate–Leaf Analysis Multivariate Program) and digital leaf physiognomy; Wolfe, 1979, 1993; Royer et al., 2005) estimate MAT from average scores or proportions of leaf morphological traits for the woody dicot species. These approaches have been applied only from the Cretaceous to the Neogene, as they rely on angiosperms. Other foliar physiognomic proxies of various climatic or other environmental parameters (e.g. Christophel & Greenwood, 1989; Wilf et al., 1998; Spicer et al., 2003, 2004) are not considered.
Leaf margin analysis is based on the proportion of species with entire leaf margins present within sites (Fig. 1a). The concept originated with Bailey & Sinnott (1915), and was converted into a quantitative proxy using calibration sets from the Northern Hemisphere (Wolfe, 1979; Wilf, 1997; Traiser et al., 2005; Adams et al., 2008; Su et al., 2010). Different temperature–leaf margin relationships have been established for parts of the Southern Hemisphere (Kennedy et al., 2002; Kowalski, 2002; Greenwood et al., 2004; Hinojosa et al., 2011).
CLAMP (Wolfe, 1993, 1995) makes estimates of MAT and other climatic and environmental parameters from multivariate analyses of leaf size, shape and margin type. CLAMP is based on a suite of variables representing the presence/absence of categories of the size, margins and shape of leaves (see http://clamp.ibcas.ac.cn/). These data have mostly been analysed using ordination followed by regression of MAT on the resulting axes (Fig. 1b), with some attempts at the multiple regression of raw data (Greenwood & Wing, 1995; Gregory-Wodzicki, 2000; Teodoridis et al., 2011). The principal datasets are largely made up of sites in the USA, Canada, China and Japan (http://clamp.ibcas.ac.cn/). Regions outside this geographical range have been sampled using the same protocols, but these data have not been incorporated into the main datasets and models.
Digital leaf physiognomy (Huff et al., 2003; Royer et al., 2005; Peppe et al., 2011), like CLAMP, estimates MAT and other climatic parameters from multivariate analyses of leaf form. It employs digitally measured, continuous variables and analyses them using multiple regression (Huff et al., 2003; Royer et al., 2005; Peppe et al., 2011). The most recent dataset uses many CLAMP sites, but includes other sites that give a more global representation than CLAMP (Peppe et al., 2011).
1. Underlying traits and control of foliar physiognomic traits
Leaf margin analysis, CLAMP and digital foliar physiognomy are all strongly empirical. This is because leaf margin type dominates the estimates of MAT from all of these methods (Wolfe, 1995; Wilf, 1997; Peppe et al., 2011), and no current explanation for the incidence of leaf teeth implies a direct relationship with MAT. Royer & Wilf (2006) argued that leaf teeth may be sites of elevated photosynthesis during leaf expansion, so that teeth may be favoured in cold climates where rapid expansion during spring is essential. Wolfe (1993) argued that teeth may increase transpiration, thus helping to maintain sap flow in expanding leaves. In addition, leaf teeth release root pressure through guttation from hydathode tissue inside leaf teeth (Feild et al., 2005).
Leaf teeth and other aspects of foliar physiognomy are under strong genotypic control. Potts & Jordan (1994) showed strong quantitative genetic control of leaf shape and size characteristics in a eucalypt. Although Royer et al. (2009b) presented evidence that temperature change induced a plastic response in leaf margin characters in Acer rubrum, the response was only c. 15% of that expected from the temperature differences (allowing for up to c. 85% genetic control of these characters). Indeed, the key trait of the presence/absence of toothed leaf margins appears to be more or less fixed for given genotypes. Thus, species and even major groups of species often either have toothed leaf margins or not, regardless of climate. For instance, all species of Myrtaceae have entire margined leaves, even though they occur across a range of MAT of 23°C or more (Kubitzki, 2007). More generally, the phylogenetic composition of a flora strongly influences the incidence of species with toothed leaves even within regions (Little et al., 2011). The phylogenetic effect may be even greater between broad regions, as some lineages are unique to, or more common in, major regions. As a result, the observed leaf margin–climate relationship appears to be largely a consequence of community assembly processes bringing together the balance of species that creates the relationship.
2. Genetic and environmental impacts on the relationship
Large regional effects show that foliar physiognomy fails the validation test of comparing regional relationships. Temperate floras of different continents have markedly different leaf–climate relationships (Stranks & England, 1997; Gregory-Wodzicki, 2000; Greenwood et al., 2004; Aizen & Ezcurra, 2008; Steart et al., 2010; Hinojosa et al., 2011), resulting in differences in predicted MAT of as much as 5°C or more (Jordan, 1997b). Even within broad regions, relationships can vary (Adams et al., 2008), and responses to MAT arising from altitude can differ from those arising from latitude (Halloy & Mark, 1996; Jordan, 1997b).
Variation in current environments may contribute to regional differences in the leaf–climate relationship. For instance, Southern Hemisphere temperate floras contain fewer deciduous species than floras at comparable northern latitudes (Axelrod, 1966; McGlone et al., 2004), and two of these southern regions (South Africa and Australia) are famous for the predominance of sclerophyllous plants with long-lived, evergreen leaves. These differences may be a result of thermal equability and typically low soil nutrient levels favouring long-lived, evergreen leaves (Turner, 1994; Wright et al., 2004a) in the Southern Hemisphere. Given that cool-climate deciduous species have a greater incidence of leaf teeth for a given climate than do evergreen leaves, these environmentally driven effects on morphology could have induced major differences in leaf–climate relationships between northern and southern floras (Jordan, 1997b; Peppe et al., 2011).
The second potential cause for regional variation in the leaf–climate relationship is a historical genetic signal (Jordan, 1997b). Such signals include phylogenetic effects, in which regional variation in the leaf–climate relationship is attributed to differences in historically determined lineage composition (Greenwood et al., 2004; Little et al., 2011). Thus, the entire margined family, Myrtaceae, dominates many Australian nonarid habitats (Groves, 1999). However, biases resulting from a strong phylogenetic influence on leaf–climate relationships and marked regional differences in lineage composition may be damped to some degree by the way in which foliar physiognomic approaches employ averages across many lineages. In addition, the phylogenetic differences in leaf form may be at least partly associated with differences in habitat through ecological lineage sorting, as discussed by Westoby et al. (1995). Thus, even in the extreme example given above, Myrtaceae are rare or absent from very cold environments, therefore limiting the bias induced by their entire margined leaves on estimates of palaeotemperature.
It has been argued that problems of regional variation in the leaf–climate relationship can be avoided by the use of geographically local physiognomic models (Stranks & England, 1997; Kowalski, 2002; Spicer, 2007; Hinojosa et al., 2011). Indeed, some models are implicitly geographically local – for example, the CLAMP dataset is strongly focused on the northern temperate zone (Wolfe, 1993, 1995; http://clamp.ibcas.ac.cn/). However, I next argue that the utility of local models is limited because they are inconsistent with the assumption that the leaf–climate relationship has remained constant. This limitation becomes progressively greater with the greater age of fossils, regardless of whether the regional variation in the leaf–climate relationship is a result of historical genetic effects or regional differences in environment.
The historical genetic contribution to interhemispheric variation in the leaf–climate relationship has, at times, been explained by putative Gondwanan origins of the Southern Hemisphere floras, compared with the more Laurasian heritage for the northern floras (e.g. Hinojosa et al., 2006). If this was the main factor, then regional models could arguably be extended back to Gondwanan times. However, as noted by Jordan (1997b) and Peppe et al. (2011), this view does not allow for compelling evidence of more recent and profound changes in the phylogenetic composition of temperate floras worldwide in response to climate change, landscape evolution and immigration of species from other regions (Momohara, 1994; Graham, 1999; Lee et al., 2001; Tiffney & Manchester, 2001; Hill, 2004; Hinojosa et al., 2006; Svenning & Skov, 2007; Sniderman & Jordan, 2011).
If geographical variation in the modern leaf–climate relationship is a result of regional differences in current environment, regional leaf–climate relationships cannot have remained constant through time. For example, if thermal equability or soil nutrients influence foliar physiognomy, it is perilous to extend Northern Hemisphere-specific models to the pre-Quaternary, when the Northern Hemisphere had more equable climates (Wing & Greenwood, 1993) and possibly poorer soils before the soil renewing effects of Pleistocene glaciation. Given that prevailing leaf physiognomic models are largely Northern Hemisphere local models, Quaternary climates may have induced fundamental biases. Analogous problems apply across all regions.
3. Analytical, taphonomic and other biases
Multivariate proxies can incorporate aspects of leaf morphology that compensate for biases in univariate relationships. However, Peppe et al. (2010) showed that the use of categorical variables can result in significant systematic errors in CLAMP-based estimates. In addition, the correspondence analysis methodologies employed by CLAMP can distort relationships between dependent and independent variables (Minchin, 1987), which has the potential to bias the results. The alternative approach (multiple regression) can be biased if the relationships between leaf and environmental traits are not linear (as occurs within the CLAMP dataset; Wolfe, 1995).
Taphonomic effects on foliar physiognomic proxies are relatively large, but difficult to quantify (Greenwood, 1992; Spicer et al., 2005; Dilcher et al., 2009). Greenwood (1992) argued that taphonomic processes alone may have added an uncertainty of c.± 1°C to physiognomic temperature estimates using leaf size, although it is less clear how strong the effects would be on other traits. Some broad principles have become apparent. Fossil assemblages are biased towards riparian species, certain taxonomic groups over others (Tegelaar et al., 1991; Briggs, 1999) and, possibly, some morphotypes over others. Post-depositional processes may also be important, but are poorly studied for leaves. However, shrinkage caused by drying and heating (Cleal & Shute, 2007) may affect some important physiognomic features, such as leaf dimensions, size of teeth and numbers of teeth per length of leaf margin, but will have little or no effect on dimensionless measures of leaf shape, such as ratios and the presence/absence of toothed margins.
4. Overall uncertainties
Large uncertainties are associated with current leaf proxies of past climates. Even assuming no biases, globally calibrated leaf physiognomic proxies for temperature have standard errors of c. 4°C (Peppe et al., 2011). This broad uncertainty must widen when the application of the proxy to the past is considered. Phylogenetic, habitat-related, taphonomic, diagenetic and sampling effects can all introduce biases of several degrees and add uncertainty to the proxies (Burnham et al., 2001; Kowalski & Dilcher, 2003; Greenwood, 2005; Royer et al., 2009a,b; Little et al., 2011).
The degree to which phylogenetic and environmental impacts on the leaf–climate relationships affect estimates of past MAT can be expected to be time related. If regional differences in the leaf–climate relationship are mainly phylogenetic, Neogene estimates from geographically local models will be biased by Quaternary floristic restructuring. The biases will be even greater for the Palaeogene and Cretaceous fossils. If regional differences are mainly environmental, the environmental changes over the same periods will also induce biases. This means that, although geographically local models show smaller standard errors within their strict inference spaces than the global model mentioned above, such local models will become progressively less useful for pre-Quaternary periods.