Is tree diversity different in the Southern Hemisphere?

- Is tree diversity different down-under? - 307FORUMJournal of Vegetation Science 18: 307-312, 2007© IAVS; Opulus Press Uppsala.

FORUM

AbstractQuestions: Is tree diversity higher in the southern hemisphere? Are latitudinal asymmetries in diversity sensitive to sampling effects?Location: 198 forested locales worldwide.Methods: I re-analysed the Gentry database, which I augmented with an additional survey from New Zealand. Data were used to test whether latitudinal declines in tree diversity differ between the northern and southern hemispheres. Data were also used to test whether hemispheric asymmetries in diversity are sensitive to sampling effects, or geographic variation in tree densities. Results: Area-based measurements of species diversity are higher in the southern hemisphere. However, southern forests house denser plant populations. After controlling for geographic variation in tree densities, diversity patterns reverse, indicating tree diversity is higher in the northern hemisphere. Conclusions: Latitudinal changes in tree diversity differ between hemispheres. However, the nature of hemispherical asymmetries in species diversity hinges on how diversity is defined, illustrating how different definitions of diversity can yield strikingly different solutions to common ecological problems.

Keywords: Latitudinal diversity gradient; Sampling effect; Species diversity.

Nomenclature: Allan (1961) and Moore & Edgar (1970).

Is tree diversity different in the Southern Hemisphere?

Burns, K.C.

School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand; Fax +64 4 463 5331; E-mail kevin.burns@vuw.ac.nz; Web http://www.vuw.ac.nz/staff/kevin_burns/index.htm

Introduction

Latitudinal variation in species diversity has intrigued biologists for over two centuries (Hawkins 2001). How-ever, it has only recently been appreciated that declines in diversity towards the poles may differ substantially between hemispheres. In a recent review of latitudinal diversity asymmetries, Chown et al. (2004) argue that “…simple exercises – such as plotting richness values for different latitudes or latitudinal bands against each other for the hemispheres and examining the resulting relationship… – rarely appear in the literature. Thus, it is not yet clear how common or strong hemisphere-related asymmetry is.” (p. 460, Chown et al. 2004; cf. Hillebrand 2004). In a pioneering study, Gentry (1988) suggested that tree diversity might be higher ̒ down-under ̓in the south-ern hemisphere. He graphically illustrated that species diversity of woody plants follows a bell-shaped distribu-tion with latitude, rising from low diversity levels at the poles to a peak near the equator. But the peak in species diversity appeared to occur in the southern hemisphere. Diversity also seemed to decline more rapidly with latitude in the northern hemisphere. However, Gentry (1988) based this observation on a limited number of forest inventories and he did not statistically test for differences in diversity between hemispheres. Species diversity is deceptively difficult to character-ize. The most common measure of diversity is on an area-basis (i.e. species density, α-diversity, or the number of species present in a given area). However, area-based estimates of species diversity can be confounded by population density, if the number of individuals sampled varies among sampling points (Bunge & Fitzpatrick 1993; Gotelli 2001). Such ʻsampling effectsʼ can have impor-tant consequences to our understanding of how factors such as insularity and productivity influence taxonomic diversity (Hector et al. 2002; Forbes et al. 2001; Chiarucci et al. 2004; Lawes et al. 2005). However, “standardizing

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data sets by area… may produce very different results compared to standardizing by the number of individu-als collected, and it is not always clear which measure of diversity is appropriate” (p. 379, Gotelli & Colwell 2001). Here, I test whether tree diversity is higher in the southern hemisphere. Using the Gentry database, I evaluate whether hemispherical clines in area-based measurements of tree diversity (i.e. species richness per unit area) differ between hemispheres. I then as-sess latitudinal trends in tree population density and test whether latitudinal asymmetries in tree diversity remain unchanged after controlling for variation in plant density.

Methods

Analyses were conducted using the Alwyn H. Gentry Forest Transect Data Set (Phillips & Miller 2002). Gentry and his colleagues sampled a total of 226 forested locales across the globe with a sampling design comprised of 10 separate transects, each meas-uring 2 m × 50 m (Gentry 1982). The first transect typically began from a randomly chosen starting point in undisturbed forest and was oriented in a random direction. Each subsequent transect was then oriented in a random direction within a 180° arch from the end of the previous transect. All plants > 2.5 cm diameter at breast height (1.37 m) that were rooted within 1 m of the transect line was identified to species. Plants were classified as belonging to morpho-species when their taxonomic identity was uncertain. Each plant was also categorized according to growth habit, either as a tree, liana or hemi-epiphyte. As a result, each subsequent 0.1 ha plot provides an estimate of plant population density and species richness per unit area for each growth form. The full dataset is freely available on line (http://www.mobot.org/MOBOT/research/gentry/data.shtml) and is discussed in detail by Phillips & Miller (2002). Of the 226 plots included in the dataset, 29 differ from the protocol described above. Lianas and hemi-epiphytes were not recorded in 6 sites, and 23 sites were not sampled over a full 0.1 ha (i.e. < 10 transects were sampled). To promote unbiased comparisons, these plots were omitted from analyses, leading to a sample size of 197 standardized inventories. Forest inventories were also not distributed homogeneously across the globe. First, temperate forests in the northern hemisphere were sampled more intensely than south-temperate forests. The highest latitude sampled in the southern hemisphere was in south-central Chile (40°43' S, 72°18' W), while ten sites in North America and Europe were located above 42° latitude. Sampling intensity also differed between

continents (Africa = 18, Australasia = 38, Europe = 5, North America = 57, South America = 126), with over 80% of sampling points coming from North and South America. In an attempt to increase the representation of poorly sampled regions and latitudes, I used Gentry s̓ (1982) pro-tocol to sample an additional site in New Zealand. These data were collected in Otari-Wiltonʼs Bush (41º14' S, 174º45' E), which contains a large, undisturbed stand of conifer-broadleaf forest on the southern tip of the North Island, New Zealand (see Burns & Dawson 2005 for a detailed site description). Elevation ranges between 70 m and 280 m above sea-level, mean annual temperature is 12.8 ºC and total annual rainfall averages 1249 mm (Anon. 1996). I tested for hemispherical differences in area-based measures of species diversity (i.e. number of species per 0.1 ha) using the general linear model procedure in SPSS (Anon. 2002). The absolute value of latitude was used as a covariate and hemisphere (north or south) was considered a fixed factor. The full model, comprised of the independent effects of the covariate and the fixed-factor and their interaction was assessed. Following Engqvist (2005), the interaction term was used to test for differences in the slope of relationships for each hemisphere. Separate tests were conducted for trees, lianas (lianas and hemi-epiphytes combined) and total species diversity. Next, I re-assessed hemispherical differences in species diversity after controlling for latitudinal varia-tion in plant density. Least-squares regression was used to evaluate the relationship between plant density and latitude, and the relationship between plant density and species richness per unit area. Standardized residuals of the relationship between plant density and area-based measures of species diversity were then subject to the same general linear model procedure described above, using the same covariate (absolute value of latitude) and fixed-factor (hemisphere). Diversity and density estimates were log10 transformed to conform to normality assump-tions. Separate tests were again conducted for trees, lianas and total species diversity. Several additional analyses were conducted to control for geographic and latitudinal differences in sampling intensity. In addition to the analysis of the full dataset (N = 198), analyses were repeated after removing all sites located above 42° latitude to account for latitudinal differ-ences in sampling intensity (N = 188). Analyses were also repeated on North and South American sites exclusively, to account for differences in sampling intensity between continents. In the separate analysis of American sites, samples located on Caribbean islands were also omitted to control for insularity effects (N = 148). In all three sets of analyses, the dependent variable and covariate

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were variously transformed (i.e. squared, log10 or log10 + 1) to conform to assumptions when necessary. Lastly, I assessed climatic correlates of global variation in plant density. Temperature and precipitation data from were ob-tained from the International Panel for Climate Change, which were arranged as an array of half-degree longitude × latitude grid cells according to New et al. (1999). For each site in the full dataset (N = 198), monthly averages were obtained for the period 1961-1990 to calculate four climatic variables: (1) mean monthly temperature, (2) mean monthly precipitation, (3) the standard deviation of mean monthly temperature, and (4) the standard devia-tion of mean monthly precipitation, following Hartley et al. (2006). Standard deviations of monthly temperature and precipitation data were obtained to estimate annual fluctuations in climate. Relationships between total plant density and the four climatic variables were then assessed with multiple regression. Plant density, mean precipita-tion and standard deviation in temperature were log10 transformed, and mean temperature was squared, to conform to normality assumptions.

Results

A total of 346 woody plants were encountered in New Zealand (see App. 1). These included 323 trees, 22 lianas and one hemi-epiphyte. A total of 35 species were encountered, including 28 tree species, 6 liana species and one hemi-epiphyte species. Results from New Zealand were very similar to inventories of temperate forests in Chile (Phillips & Miller 2002). The total dataset consisted of 67 423 woody plants (trees = 55 913, lianas = 11 510) and 20 974 species occurrences (trees = 16 206, lianas = 4768). The total number of woody plant species occurring in each plot declined with latitude at a different rate in the northern and southern hemispheres (Table 1). The slope of the diversity-latitude relationship for all woody plants was steeper for the northern hemisphere (Fig. 1). Similar results were obtained in separate analyses of trees and lianas. Similar results were also obtained with the full data set, sites located below 42° latitude and non-insular, North and South American sites. Therefore, area-based diversity estimates indicate that

Table 1. F-statistics from general linear models of the effect of latitude and hemisphere on species diversity of lianas (including hemi-epiphytes), trees and both life forms combined. Results from area-based diversity estimates (species richness/0.1 ha) are shown alongside individual-based diversity estimates (residuals of relationships between plant density and species richness per unit area). Analyses were conducted on all fully-sampled Gentry plots (ʻfull global datasetʼ, N = 198), all plots located below 42° latitude to control for latitudinal differences in sampling intensity (ʻsites < 42° latitudeʼ, N = 188) and all non-insular plots located in North and South America below 42° latitude to control for continental differences in sampling intensity (N = 148). Subscripts refer to the more diverse hemisphere (S = southern hemisphere, N = northern hemisphere). Lianas Trees Trees & Lianas per-area per-individual per-area per-individual per-area per-individual

Full global dataset 4.6S* 24.2N*** 10.5S** 10.1N** 14.9S*** 14.8N***Sites < 42° latitude 5.5S* 11.6N** 4.5S* 16.1N*** 7.0S** 10.4N**North & South America (< 42°) 10.7S** 14.4N*** 4.3S* 29.1N*** 7.1S** 16.7N***

Fig. 1. A. Latitudinal variation in species richness per unit area (the total number of woody plant species per 0.1 ha); B. Latitudinal variation in species richness after controlling for plant density (standardized residuals of the relationship between species richness per unit area and plant density). Vertical dashed lines are drawn at the equator. Species richness per unit area declines more rapidly with latitude in the northern hemisphere, indicating tree diversity is higher in the southern hemisphere. However, the pattern reverses (i.e. diversity is higher in the northern hemisphere) after controlling for plant density.

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tree diversity is higher in the southern hemisphere. Plant population densities differed between hemi-spheres (Fig. 2, see also Enquist & Niklas 2001; Currie et al. 2004). Total plant density declined linearly with latitude (r2 = 0.364, P < 0.001), and species richness per unit area increased with plant density (r2 = 0.545, P < 0.001). General linear model analyses of the residuals of the relationship between species richness per unit area and plant density yielded different results from the previous analyses. After controlling for differences in plant density, diversity estimates again declined with latitude, but in this case declines were more rapid in the southern hemisphere (Fig. 1). Similar results were obtained in separate analyses of different growth forms and amalgamations of data (Table 1). Therefore, after controlling for plant density, tree diversity is higher in the northern hemisphere. Plant densities were correlated with several climatic variables. Total densities of woody plants were positively related with mean annual temperature (T = 2.28, P = 0.007) and negatively related to the standard deviation of average monthly temperatures (T = -5.12, P < 0.001). Plant densities were unrelated to mean annual precipita-tion (T = 0.01, P = 0.991) and the standard deviation of average monthly precipitation (T = -0.06, P = 0.953). Multicollinearly assumptions were met in all four in-dependent variables (variance inflation factor < 2.0 for all).

Discussion

Overall results showed that tree diversity is indeed different ʻdown-underʼ. However, the nature of hemi-spherical asymmetries in diversity is strongly depend-ent on how diversity is measured. When measured on a per-area basis, diversity appears to be higher in the southern hemisphere, which supports Gentryʼs (1988) speculation. However, plant density also varies asym-metrically between hemispheres, increasing linearly from north to south. After controlling for latitudinal differences in plant density, the direction of hemispherical diversity asymmetries reverses. On a per-individual basis, tree diversity is higher in the northern hemisphere. This result can be analogized to an imaginary land-scape that is randomly populated by plants belonging to a variety of species, but plant density is higher at one end of the landscape than the other. If two equal sized plots are placed on either side of the landscape, species richness per unit area will be higher on the side of the landscape containing more plants, because as more plants are sampled, more species will be encountered by chance (see Gotelli & Colwell 2001). Hemispherical asymmetries in tree species diversity appear to be influ-enced by a similar type of sampling effect. Except that the side of the landscape with more plants (the southern hemisphere) actually contains fewer species. Or more precisely, results suggest that one would encounter new species less rapidly while randomly inspecting plants in the more densely populated, southern hemisphere. Sampling effects have been hypothesized to generate the latitudinal diversity gradient. Higher productivity at the equator might lead to denser populations, which could then randomly ̒ sample ̓more species (see Evans et al. 2005). Although I did not intend to test the sampling effect hypothesis as an overarching explanation for the

Fig. 2. Relationships (A) between plant density (log10 transformed) and latitude, and (B) between species richness per unit area and plant density (both log10 transformed). Southern hemisphere latitudes have negative values.

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latitudinal gradient, my analyses argue against it. Even after removing the effect of plant density from area-based estimates of species diversity, diversity still peaks at low latitudes. Therefore, some factor associated with latitude (see Hawkins & Diniz-Filho 2005) is an important driver of geographic variation in individual-based estimates of species diversity. In a previous analysis of the Gentry dataset, Currie et al. (2004) found that plant density is correlated with evapotranspiration, albeit weakly (rs = 0.35). Analyses conducted here showed that plant density is more strongly associated with temperature variability (rs = – 0.42), indicating that areas with less variable monthly tempera-tures (i.e. more stable temperature regimes) house denser plant populations. This result suggests that temperature variability can partially explain latitudinal asymmetries in plant density. Annual fluctuations in temperature are much reduced in the southern hemisphere (Chown et al. 2004), due to smaller continental landmasses and the ameliorating effect of the ocean, which stores heat as latent energy. This effect appears to explain higher plant population densities in the southern hemisphere. However, the overall adjusted r2 value from this analy-sis is quite small, indicating that other factors, such as historical effects or soil conditions, are also important. Therefore, while the negative relationship between latitude and plant density appears to be associated with temperature variability, a comprehensive explanation for this pattern remains to be elucidated. Niklas et al. (2003) linked the relationship between plant density and species richness per unit area to plant size. Regardless of hemisphere, most species in Gen-tryʼs plots occur only as saplings. Therefore, sampling regimes that neglect to census smaller plants might seri-ously bias estimates of species diversity. The reversal of hemispherical asymmetries in diversity after controlling for sampling effects highlights a similar concern; dif-ferent ways of quantifying diversity can yield different geographic patterns in biodiversity. Overall results uncovered strong hemispherical asymmetries in tree diversity. However, the direction of hemispherical diversity asymmetries hinges on how species diversity is defined. On an area-basis, forests in the southern hemisphere house more species. However, patterns in species diversity are strongly influenced by geographic variation in plant density, and after correcting for sampling effects, diversity is higher in the northern hemisphere. Tree diversity therefore appears to be differ-ent down-under. However, identifying which hemisphere is more diverse hinges on oneʼs definition of diversity.

Acknowledgements. Alessandro Chiarucci, Gordon Jenkins, Michael Kessler, Michael Weiser and an anonymous reviewer provided helpful comments on earlier drafts of the manu-script.

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Received 28 September 2006;Accepted 23 December 2006;Co-ordinating Editor: S. Díaz.