Our study provides the most extensive comparat-ive data set for seasonally dry tropical areas, an area that has been largely neglected by ecophysiological researchers (Niinemets 2001). The results highlight the importance of including studies from a wide range of biomes, and habitats within biomes, in order to derive globally applicable relationships between ecosystem function and leaf attributes. While our mean values for Amass, LMA, leaf density, leaf thickness and water content are similar to those reported in the global meta-analysis of Niinemets (1999), we found that Amass and Aarea were generally larger than found by Reich et al. (1999), who studied shrubs and herbs as well as trees, and sampled from biomes ranging from alpine tundra to tropical rainforest. Average leaf N, on either an area or a mass basis, was similar to that reported by Niinemets (1999) and Reich et al. (1999). This was unexpected, given the generally very infertile soils in northern Australia. Niinemets (1999) also derived a linear relationship between leaf thickness and annual average temperature, and attributed this to higher photosynthetic rates and shorter payback times at near-optimal temperatures. Leaf thickness measured in our study is only half what would be expected from this linear relationship; it is also lower in the few other studies where mean annual temperature exceeded 20 °C. It therefore appears that the leaf thickness–temperature relationship levels out, and perhaps even declines, at temperatures above 20 °C. Our leaf density and LMA values are also smaller than would be expected from regressions against precipitation in the three driest months (Niinemets 2001). The Darwin region is more seasonal in terms of rainfall, with both a drier 3-month period (total mean rainfall is 8 mm for June to August inclusive), and a higher maximum monthly rainfall (426 mm in January), than any included in the Niinemets (2001) study. An alternative measure of water availability that incorporates potential evapotranspiration and soil water storage would be more appropriate when such seasonal sites are included (Eamus 2003).
Reich et al. (1999) showed that there were similar slopes, but often different intercepts, in the equations relating pairs of leaf attributes from the six different biomes they studied. Our findings for the four habitats within one biome (tropical savanna) were generally consistent with this, except that the slopes varied with habitat for LMA vs Nmass. For any given value of any attribute except Pmass, Amass was larger in the dry monsoon forest than in the other habitats (Fig. 1). By contrast, differences found by Reich et al. (1999) between biomes were not so consistent; for a given LMA, Amass was highest in desert shrub species, but for a given life span, Amass was highest in humid temperate and tropical forests.
Relationships found in this study among LMA, leaf life span, Nmass, Amass and Aarea are similar to those found by Reich and co-workers (Reich et al. 1992; Reich et al. 1999). As in their studies, correlations with life span, Nmass and LMA were stronger for Amass than Aarea. Niinemets (1999) found that Amass was negatively correlated with LMA because of the negative correlation between Amass and leaf density, while there was little relationship between Amass and leaf thickness. In our study, however, Amass was more strongly correlated with leaf thickness than density (Table 3). The components of LMA, leaf thickness and density were not significantly correlated with each other, as has been found in other studies (Witkowski & Lamont 1991; Niinemets 1999). The strong negative correlation between leaf density and water content can be explained by the observation of Roderick et al. (1999) that, if a leaf has a high liquid content, then it cannot have a large volumetric fraction of dry matter and will thus have a low density.
Leaf P has seldom been included in studies such as ours, which is surprising given its suggested role in characterizing sclerophyllous vegetation (Loveless 1961). Our study found a stronger correlation between Pmass and Amass than any reported by Wright, Reich & Westoby (2001) in southern Australia, and contrasts with that of Tuohy, Prior & Stewart (1991), who found no correlation between these attributes in Zimbabwean tree species. We also found a closer correlation between Nmass and Pmass than found by Wright et al. (2001).
We found that evergreen species had larger LMA, leaf thickness and leaf life span, and smaller Nmass and Pmass than deciduous species, but there was no significant difference in Amass. (Differences in Amass were significant if trees, rather than species, were considered the experimental unit.) Smaller LMA and leaf thickness in deciduous compared with evergreen tree species have been reported in a range of woody species (Castro-Díez, Puyravaud & Cornilessen 2000), but these have generally been accompanied by larger Amass (Chabot & Hicks 1982; Sobrado 1991; Prado & Moraes 1997; Eamus & Prichard 1998). In Eurasian tree species, Nmass and Pmass are smaller in evergreen than in deciduous trees (Chabot & Hicks 1982). The longer life span of evergreen compared with deciduous leaves offsets their higher construction costs (Chabot & Hicks 1982; Sobrado 1991; Eamus & Prichard 1998). Given difficulties in precisely defining phenological categories, it is more useful to classify trees according to leaf life span than leaf phenology (Reich et al. 1992). In this study there was considerable overlap in leaf life span between the phenological guilds, especially between evergreen and semi-deciduous species (Table 4; Fig. 4). Median leaf life span varied between 3 and 12 months, and was shorter on average than in a Malaysian rainforest (Osada et al. 2001), a Mexican cloud forest (Williams-Linera 2000), Venezuelan rainforest (Reich, Walters & Ellsworth 1991), or in five of the six biomes studied by Reich et al. (1999). Our findings are consistent with those of Myers et al. (1998), who reported that leaf life span of the Eucalyptus/Corymbia group appears to be shorter in northern than in southern Australia.
There were significant differences among species in all attributes studied, and these differences were larger when expressed on a mass than on an area basis. For example, area per leaf varied 13-fold, LMA 4·5-fold, and Amass varied sevenfold, while Aarea varied only twofold. These interspecific variations were smaller than found by Reich et al. (1999). Callitris intratropica was included in this study because there have been few physiological measurements made on tropical or Southern Hemisphere conifers. In common with Northern Hemisphere conifers (Ackerly & Reich 1999), it had lower Aarea, Amass and Nmass, and higher LMA than most or all of its broad-leaved counterparts, evergreen or deciduous. In the present study, species differences were strongly associated with leaf phenology and whether they were Myrtaceous or not, and are related to habitat types.
Variation in leaf attributes found between species within the three non-rainforest habitats was larger than the variation between these habitats. This is surprising given their different physical characteristics. The swamp is inundated for several months a year, and the soil has a high organic content with high moisture availability throughout the dry season [unpublished data, and as described by Kelley (2002) for a similar site]. The open forest has deep, well drained, relatively fertile soils, free of rock. By contrast, woodland soils are stony and infertile, and have poor subsurface drainage. As expected, based on the higher soil N and P at that site, species in the dry monsoon forest had higher mean Amass and Nmass, and lower LMA and leaf density than species in the other habitats. These characteristics, typical of fast-growing species in relatively favourable environments, were reflected in higher tree growth rates, basal area, stem density and canopy cover in this habitat (L.D.P., unpublished results).
Higher levels of soil N and P in Australian monsoon forest compared with adjacent savanna have been reported previously, and are attributed, at least in part, to less frequent fire in the monsoon forest (Bowman 1992). High nutrient content in leaves of dry monsoon forest relative to savanna species has also been recorded (Fensham & Bowman 1995; Schmidt et al. 1998). However, Fensham & Bowman (1995) found that leaves of one sclerophyllous monsoon forest species had similar nutrient concentrations to leaves of savanna species, suggesting that differences between the habitats were related to intrinsic leaf properties as well as soil fertility. This is consistent with our study, in which M. leucadendra had leaf N and P concentrations less than half those of the other species in the dry monsoon forest.
Differences between Myrtaceous and non-Myrtaceous species were generally larger than differences between habitats or leaf phenological guilds, and were clearly separated by principal components analysis (Fig. 2b; Table 5). Myrtaceous species were typically sclerophyllous, with larger LMA, leaf thickness and life span, and smaller Amass, Chlmass, Nmass and Pmass than non-Myrtaceous species. Only one non-Myrtaceous species, Buchanania obovata, was comparable to Myrtaceous species.
Myrtaceous species do not comprise the majority of species in north Australian savannas, but they often contribute the largest component of woody biomass in frequently burnt habitats (O’Grady et al. 2000). Myrtaceous leaves are characteristically sclerophyllous, and sclerophyllous leaves are usually associated with slow relative growth rates (Lambers & Poorter 1992; Wright & Westoby 2000). Therefore other factor(s) must confer a competitive advantage to Myrtaceous species in these tropical savanna environments. One probable factor is fire tolerance, as extensive, frequent fires are a feature of Australian savannas (Russell-Smith et al. 1997). Williams et al. (1999) found that deciduous non-eucalypt species comprised the group most susceptible to fire in Australian savanna. Based on their data, Myrtaceous and non-Myrtaceous species had similar plant survival rates after a single, high-intensity fire (86 vs 82%), but stem survival was higher in the Myrtaceous species (43 vs 15%). Our findings help explain the success of non-Myrtaceous species in areas relatively protected from fire, such as those where dry monsoon forests are found (Bowman 1992).
In terms of their leaf attributes, the four habitats dichotomized into the closed canopy (dry monsoon forest) and the open canopy habitats (woodland, open forest and swamp). These differences in leaf traits could be largely explained by differences between the mesophytic, often deciduous, species from non-Myrtaceous genera that prevailed in the dry monsoon forest, and the sclerophyllous, Myrtaceous species common in the other three habitats. Thus habitat differences were linked to the phylogeny and leaf phenology of the species found there. In a broad Australian context, there is an often sharp ecological and floristic dichotomy between quintessentially Australian vegetation (dominated by Eucalyptus and Acacia) and the rainforests that occur in the most humid climates and in fire-protected refugia (Bowman 2000). This study has shown that in northern Australia the dichotomy between rainforest and non-rainforest vegetation apparently extends to, and can be inferred from, leaf attributes.