ECOGRAPHY 27: 299 /310, 2004

Elevational gradients, area and tropical island diversity: an example from the palms of New Guinea
Steven Bachman, William J. Baker, Neil Brummitt, John Dransfield and Justin Moat

Bachman, S., Baker, W. J., Brummitt, N., Dransfield, J. and Moat, J. 2004. Elevational gradients, area and tropical island diversity: an example from the palms of New Guinea. / Ecography 27: 299 /310. The factors causing spatial variation in species richness remain poorly known. In this study, factors affecting species richness of palms (Palmae/Arecaceae) were studied along the elevational gradient of New Guinea. Interpolated elevational ranges were calculated from a database of all known collections for 145 species in 32 genera. The amount of land area at different elevations greatly affects the species richness gradient. If assessed in equal-elevation bands species richness appears to decline monotonically, but when assessed in equal-area bands species richness shows a pronounced midelevation peak, due to the large proportion of lowlands in New Guinea. By randomising species ranges within the total elevational gradient for palms and accounting for area, we found the mid-elevation peak to be consistent with a middomain effect caused by the upper and lower limits to palm distribution. Our study illustrates the importance of accounting for area in macroecological studies of richness gradients and introduces a novel yet simple method for doing this through the use of equal-area bands. Together, the effect of area and the mid-domain effect explain the majority of variation in species richness of New Guinea palms. We support calls for the multivariate assessment of the mid-domain effect on an equal footing with other potential explanations of species richness. S. Bachman, Dept of Geography and Earth Sciences, Brunel Univ., Uxbridge Middlesex, U.K. UB8 3PH. / W. J. Baker (correspondence: w.baker@rbgkew.org.uk), N. Brummitt, J. Dransfield and J. Moat, The Herbarium, Royal Botanical Gardens, Kew, Richmond, Surrey, U.K. TW9 3AB.

Along with the well-known latitudinal gradients in species richness, patterns of biotic diversity along elevational gradients have been studied for centuries (Willdenow 1805, Darwin 1859, Wallace 1876, Whittaker 1960, Brown 1971, Rahbek 1995, 1997). Many of these studies have attempted to correlate observed patterns of diversity with various environmental gradients such as precipitation, temperature, humidity and productivity. It has been generally recognised that species richness declines with elevation. However, monotonic declines in richness are less typical than are unimodal peaks or patterns where species richness plateaus before decreasing (Rahbek 1995). Monotonic declines in species richness are thought by some authors to mirror a

decrease in productivity (Rahbek 1997 and references therein, Kaspari et al. 2000), although productivity gradients have also been used to explain mid-elevation peaks in species richness (Rosenzweig 1992, 1995, Rosenzweig and Abramsky 1993). However, to date, no universal relationship between productivity and richness has been elucidated. In contrast, the relationship between area and number of species is well known (Arrhenius 1921, Williams 1943, Rosenzweig 1995). Traditionally, species richness is thought to increase with increasing area following a power-law model (Williamson 1988; but see also Connor and McCoy 1979). In regions with diverse landscapes that range from sea level to high mountains, the land

Accepted 16 December 2003 Copyright # ECOGRAPHY 2004 ISSN 0906-7590

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area in different elevational bands varies greatly. Commonly, land area decreases as elevation increases such that lowlands account for the highest proportion of the total land area of a given region (MacArthur 1972); mountainous islands such as New Guinea display this feature particularly well. It seems strange then that, when examining species richness along elevational gradients, some authors have not considered the influence of area (e.g. Patterson et al. 1998, Ohlemuller and Wilson 2000). Several studies show that when area has been controlled species richness peaks at mid-elevations (e.g. Lawton et al. 1987, Rahbek 1997), although unimodal peaks have been found without accounting for area (Koleff and Gaston 2001, Sanders 2002, Grytnes and Vetaas 2002). It has also been shown that area alone could explain a large proportion of the variance in the observed richness pattern (Rahbek 1997, Koleff and Gaston 2001, Sanders 2002). The mid-elevation peak is now recognised as a common pattern (Rahbek 1995, 1997, Heaney 2001, Kessler 2001, Nor 2001, Rickart 2001, Sanchez-Cordero 2001), but despite the recent resurgence of interest in studies of species richness along elevational gradients, a generally-accepted explanation for this mid-elevation peak has not yet been found. Recently, the potential influence of non-biological factors on species richness patterns has been highlighted (Colwell and Hurtt 1994, Colwell and Lees 2000). When species ranges are randomly placed within a geographically defined domain, a peak in richness inevitably arises towards the centre of this domain (Colwell and Lees 2000). In real terms, this domain may be an island or continent bounded by its shores, a mountain bounded by its summit and the lowlands at its base, or an ocean bounded by the surface and its floor. A gradient in elevation is a simple, one-dimensional domain. Within the domain, species with a range mid-point at midelevations will have a greater potential elevation range, or amplitude, as they can extend further both upwards and downwards than can those species whose range midpoint is found near the top or the bottom of the domain. Since species ranges are constrained geometrically in this way (they cannot extend either above the highest mountain top or below sea level), the number of overlapping elevational ranges will be greater at mid-elevations and, thus, so will species richness. This is due simply to species of moderate to large elevational range being more likely to cross the middle of the domain than to coincide at either boundary. The phenomenon, termed the mid-domain effect (MDE), is therefore dependent upon the underlying frequency distribution of relative species range-sizes. The mid-domain effect is attributed to these simple geometric constraints of the domain or, more accurately, to geometrically constrained stochastic processes affecting the underlying range-size frequency distribution (RSFD; Colwell et al. in press). 300

Despite growing evidence and support for the existence of the MDE (Colwell and Hurtt 1994, Lyons and Willig 1997, Pineda and Caswell 1998, Willig and Lyons 1998, Colwell and Lees 2000, Jetz and Rahbek 2001, Sanders 2002, Grytnes and Vetaas 2002), the concept has yet to gain widespread acceptance as a plausible factor contributing to richness patterns (Bokma and Mon kkonen 2000, Koleff and Gaston 2001, Diniz-Filho et al. 2002). Several studies (Lees et al. 1999, Jetz and Rahbek 2001, Koleff and Gaston 2001, Sanders 2002) have investigated the combined influence of area and MDE on species richness patterns and in each case richness was explained well by the two combined factors. To date, however, few MDE studies have focused on vascular plants (but see Grytnes and Vetaas 2002), and in addition, except for a pioneering study of butterflies in Madagascar (Lees et al. 1999), no MDE studies have focused on large tropical islands such as New Guinea. New Guinea offers a perfect template for MDE studies being rich in endemic species, relative to total species richness, mountainous, and clearly defined in terms of a domain. Furthermore, the deepening biodiversity crisis should surely direct such research to those areas, such as tropical islands, where the greatest threats to biodiversity exist. This study aims to investigate the influence of available area and MDE on species richness in palms (family Arecaceae or Palmae) along the elevational gradient of New Guinea and surrounding islands, one of the most biodiverse areas in the Asia-Pacific region. We use two methods, one published (Sanders 2002) and one novel, to ask the following questions: 1) Does available area affect palm richness at different elevations in New Guinea? 2) Do geometric constraints affect palm richness along this elevational gradient? 3) Do genera of palms also show the same patterns as species do? The methods and data used in this study will be critically examined and may help to highlight important issues for other studies aiming to investigate similar themes.

Methods
Study area and empirical data
New Guinea is the largest tropical island in the world with a surface area of 808 510 km2 and an elevational range extending from sea level to 5030 m, the highest peak being Puncak Jaya (also known as Mt. Carstenz). The study area (Fig. 1) comprises the Indonesian province of Papua (formerly Irian Jaya) and the independent country of Papua New Guinea, and is bounded in the east by the Louisiade Archipelago and in the west by the islands Misool and Waigeo. In addition to mainland New Guinea, other major islands included in the study area are Yapen, Biak, Manus and the Bismarck Archipelago. The island of Bougainville (a part of Papua
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Fig. 1. New Guinea and surrounding islands; the dark area represents the study region, the grey scale shading indicates elevational change. The island is divided into two political entities, the independent country Papua New Guinea to the east and the Indonesian province of Papua (formerly Irian Jaya) to the west. The islands to the north-east form the Bismarck Archipelago. Dots indicate the distribution of georeferenced collecting localities.

New Guinea) has been excluded because its biogeographic links are closer to the Solomon Islands than to New Guinea. The study area stretches over a relatively small latitudinal range (from 08 to 11840S), thus minimising any possible effect of a latitudinal gradient. The primary dataset for this study was extracted from a database of /3000 herbarium specimen records from the specified area. The data were gathered from herbaria at six institutions (Royal Botanic Gardens, Kew; the Papua New Guinea Forest Research Inst., Lae; Herbarium Bogoriense, Bogor, Indonesia; the National Herbarium of the Netherlands [Leiden branch]; the Univ. of Aarhus, Denmark and the Queensland Herbarium, Brisbane, Australia). The database has been compiled as part of a current taxonomic research project on the palm flora of New Guinea (Baker 2002). Each record in the database relates to a single herbarium collection, including all known duplicates of any given collection. As well as taxonomic data, each record includes all locality and elevation data from the data labels of each specimen; collecting localities are shown in Fig. 1. The variation in the number of collections along the elevational gradient, with amount of land area in successive equal-elevation bands, is depicted in Fig. 2. Elevation ranges were calculated from the database records using two separate methods. The first method used empirical elevation readings recorded in the field by the collector; this will be referred to as the field data method. This is regarded as a primary source of elevation data because it comes directly from the collectors field measurements. These data will most likely have been gathered using a barometric altimeter, but may also have been estimated using topographic maps. In the second method, elevation ranges were derived from a digital elevation model (DEM) produced by the United States Geological Service (Anon. 2001); this will be referred to as the DEM method. This is considered to be a secondary method because the elevation data are
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indirectly derived from the locality data of the specimens through a DEM and are highly dependent on the quality of that locality data and the DEM. The DEM method was only applied to records that were geo-referenced (i.e. spatially referenced to a point on the surface of the earth), either with a GPS unit, from a gazetteer or with a reliable map estimate. Using only those species and genera for which both georeferences and field recorded elevation data were available (145 species, 32 genera) it was possible to compare the influences of the two data types on the analysis of species richness patterns. It should be noted that the two data types (field and DEM) are not wholly statistically independent. However, we include both since field and DEM data may differ slightly for the same record, and more importantly, in some cases, individual specimen records may have either georeferences or field-recorded elevation data, but not both. This comparison of field and DEM records may therefore expose potential biases in our analysis due to these differing data collection techniques.

Fig. 2. The relationship between available area and number of collections in successive equal-elevation bands. Lowlands make up by far the largest area in New Guinea; the amount of available area decreases dramatically with increasing elevation. The number of collections is not uniform over the elevational gradient but it remains proportional to the amount of available area.

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When conducting a MDE analysis no taxon should have a range that extends beyond the domain being studied; in the narrowest sense, the species and genera should be endemic to the domain (Colwell and Lees 2000). In this study the lower limit of the domain is sea level and the upper limit is the maximum empirical elevation of palm records (Field data 0/2800 m, DEM 0/ 2803 m). Of the 145 species available for analysis, 21 were not endemic to the study region. However, the elevational ranges of these non-endemic species did not exceed the limits of the domain after the examination of additional non-New Guinea records. Therefore, all 145 species were used in the analyses. Of the 32 palm genera that occur in New Guinea, only 2 are endemic to the region as a whole. The elevational ranges of all genera within New Guinea were therefore compared with their ranges outside of the region and as a result 8 genera were excluded from the analyses because their ranges outside of the study region extended beyond the domain limits within the study region. Thus, 24 genera were used in the analyses.

Gaston 2001, Colwell et al. in press). The purely theoretical Models 1 /3 (Colwell 2000) were also not used because of the implicit biological assumptions they make regarding RSFDs (Colwell et al. in press). The model was iterated 100 times to produce the null distribution. The observed richness values and area values for each band were log-transformed to account for the relationship between species number and area. The MDE predictions were also log-transformed so that they could be compared with the log transformed observed richness values and area values. Using simple linear regression, the independent variables of area and MDE predictions were separately tested against our empirical dataset to examine the amount of variance in the observed richness that could be conditionally explained. The combined effects of both area and MDE predictions were also tested against observed richness. Tests of significance are complicated by the fact that richness figures for the elevational bands are spatially-autocorrelated and hence not statistically independent (Colwell pers. comm.). Consequently, no p-values are presented here. Method 2 Method 2 accounts for area by measuring richness along the elevational gradient in equal-area bands rather than equal-elevation bands. This method, despite its simplicity, appears not to have been used in species richness analyses so far. The elevational gradient was classified into equal-area bands using GIS software ArcView 3.2 (Anon. 1999). The original Digital Elevation Model (DEM) data (Anon. 2001) is given as integers (whole numbers), but because of the extremely large area of lowland in New Guinea this meant that the majority of pixels were classified as either 1 or 2 m elevation only. This did not allow sufficient equal-area bands to be produced, since it was impossible to split the largest band ( B/1 m elevation) any further. To overcome this problem the original elevation data was converted to decimal numbers and a random number between (/0.5 and'/0.5 added to the elevation of each pixel for all elevations (in ArcView Spatial Modeller the equation would be {[DEM] (/0.5'/Grid.MakeRandom}). This produced a grid that could be easily classified into equal-area bands. Unfortunately, however, in ArcView it is not possible to classify a floating number grid into equal areas. To determine the band boundaries, therefore, the new DEM data was exported to a database program (only land was exported / sea was treated as null, and removed) and pixels sorted by ascending value of elevation. The band boundaries were calculated from the number of pixels divided by the number of bands desired. The value for each band boundary was then simply read off from the row number within the database, for each of 5, 10 and 15 equal-area bands.
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Analytical methods
Two methods were used to investigate the influence of area and MDE on taxon richness along the elevational gradient. In order to explore the basic relationship between elevation and richness the gradient was divided into 100 m equal-elevation bands and total richness was calculated as the sum of all species or genera occurring within each band. Method 1 then specifically tests the separate and combined influences of area and MDE on observed richness patterns within these equal-elevation bands, using simple linear regression. Method 2 examines the amount of variance in observed richness that can be explained by MDE after area has been accounted for, by dividing the gradient into equal-area bands, also using simple linear regression. Method 1 Method 1 follows the procedure used by Sanders (2002). Observed richness was calculated by summing the number of species or genera in each 100 m elevation band. It was assumed that each taxon occurred in all bands between its minimum and maximum elevational limits. The amount of area in each band was calculated using the DEM. The MDE null distribution was calculated using RangeModel software (Colwell 2000). We used Model 4 (Colwell 2000) which selects (with replacement) ranges from the empirical range-size frequency distribution (RSFD) and randomly places them in the domain (the elevation gradient). Model 5 (Colwell 2000), which uses empirical midpoints and random range-sizes, was not used because the null model is too closely constrained by the empirical data (Koleff and 302

With area kept constant at each band, richness can be looked at anew. However, there is no set rule regarding the number of equal-area bands into which a gradient should be split. To explore the effect of the number of bands on richness estimates, we split the elevational gradient into 5, 10 and 15 equal-area bands. The elevational ranges for all these equal-area bands are given in Appendix 1. The equal-area richness patterns were then plotted against those predicted by the MDE null model under Model 4 of RangeModel (Colwell 2000). The model was iterated 100 times using the empirical RSFD. In using equal-area bands we have created bands with unequal elevation, since the amount of area in New Guinea declines with increasing elevation (see Fig. 2). In other words, the higher the equal-area band, the broader is its elevational range. Therefore multiple linear regression was used to compare the observed richness against expected richness derived from MDE null predictions with elevational range for each equal-area band as an additional explanatory variable. The procedure was carried out for species and genera using both types of elevation data (DEM and field data). Slope values for each relationship were also calculated, under the assumption that the closer the slope is to 1, the more closely the MDE null model predicts the number of observed taxa (see also Jetz and Rahbek 2001).

Results
Basic relationships between richness and elevation
Without accounting for area both species and genus richness of New Guinea palms decreases as elevation increases (Fig. 3A). Generic richness peaks in the lowest elevation band (0 /100 m) for both DEM and field data methods. Species richness also peaks in the lowest elevation band using the field data method, but peaks in the second band (201 /300 m) using DEM data. The DEM-derived richness estimates for both species and genera are consistently higher than the field data estimates along the gradient, with the exception of species for the first elevation band where the field data estimate is greater than the DEM estimate. However, the overall patterns along the gradient are broadly similar for both data types. Method 1 The relationships between New Guinea palm richness, area and MDE along the elevational gradient, presented as in Sanders (2002), are given in Fig. 4A /D. All r2 values are shown in Table 1. Area alone conditionally explained around half of the variance in observed richness pattern for both species and genera irrespective of data type used (min r2 0/0.45 [genera, DEM]; max r2 0/0.52 [species, Field and DEM]). MDE alone conECOGRAPHY 27:3 (2004)

Fig. 3. The relationship between richness and elevation within the study region. (A) species and generic richness within 100 m equal-elevation bands; (B) species and generic richness within equal-area bands. The thick, solid line represents species richness using eld data; the dot-dash line species richness with elevations calculated from a DEM; the thin, solid line generic richness using eld data and the dashed line generic richness with elevations calculated from a DEM.

ditionally explained very little of the variation in observed richness regardless of data type and taxonomic scale (min r2 0/0.04 [species, Field]; max r2 0/0.33 [species, DEM]). However, the combined effects of area and MDE conditionally explained a great deal of the variation (min r2 0/0.77 [genera, Field]; max r2 0/0.89 [species, DEM]) of the observed richness pattern, with the highest r2 value for species DEM data (Table 1). In general, the combined effects of area and MDE gave higher r2 values for DEM data (species, 0.89; genera, 0.84) than for field data (species, 0.84; genera, 0.77).

Method 2 The removal of the effect of area on richness through the use of equal-area bands yielded a mid-elevation peak in both species and genus richness patterns (Fig. 3B). This contrasts markedly with the basic relationship between richness and elevation, which is roughly monotonic (Fig. 3A). The relationships between richness, area and MDE are given in Fig. 5A /D for 15 equal-area bands. All r2 values are shown in Table 2. Although the MDE null predictions consistently underestimate observed richness, the variation in observed patterns at both taxo303

Fig. 4. Comparison of species and generic richness with amount of area and MDE null-model predictions along the elevational gradient. (A) species richness with elevations from eld data; (B) generic richness with elevations from eld data; (C) species richness with elevations from DEM data; (D) generic richness with elevations from DEM data. For each graph the solid line represents species or generic richness, the solid line with hollow circles shows area and the solid line with solid circles shows MDE null-model predictions.

nomic levels and with both data types are generally comparable with the null model predictions. Linear regression shows that the variance in species richness with field data in most cases is conditionally explained remarkably well by the MDE null predictions irrespective of the number of equal-area bands (min r2 0/ 0.90 [5 and 15 bands]; max r2 0/0.98 [10 bands]; see Table 2). However, for species richness from DEM data and generic richness with both field data and DEM data the number of equal-area bands does seem to have an influence; r2 values decrease in unison with number of

equal-area bands, and markedly so for generic richness with field data (r2 0/0.70, 15 bands; 0.66, 10 bands; 0.39, 5 bands). In general the variance in richness is best explained when 15 equal-area bands are used (species richness from DEM data, r2 0/0.98; generic richness from DEM data, r2 0/0.89; generic richness from field data, r2 0/0.70), although for species richness with field data the highest r2 value is with 10 equal-area bands. As with Method 1, DEM data consistently returns higher r2 values (species, 0.93 /0.98; genera, 0.82 /0.89) than does field data (species, 0.90 /0.98; genera, 0.39 /0.70). By

Table 1. Results from the simple linear regression analysis using Method 1. The separate and combined effects of area and MDE are shown. Note that in all cases the combined effects of area and MDE explain more of the variance in observed richness than either does alone. Data type Field Field Field Field Field Field DEM DEM DEM DEM DEM DEM Elevation range (m) 0 /2800 0 /2800 0 /2800 0 /2438 0 /2438 0 /2438 0 /2803 0 /2803 0 /2803 0 /2796 0 /2796 0 /2796 Taxonomic level Species Species Species Genera Genera Genera Species Species Species Genera Genera Genera Parameter observed observed observed observed observed observed observed observed observed observed observed observed vs vs vs vs vs vs vs vs vs vs vs vs area MDE MDE'/area area MDE MDE'/area area MDE MDE'/area area MDE MDE'/area r2 0.52 0.04 0.84 0.50 0.07 0.77 0.52 0.33 0.89 0.45 0.10 0.84

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Fig. 5. Comparison of observed richness patterns and MDE null-model predictions along the elevational gradient, split into 15 equal-area bands. (A) species richness with elevations from eld data; (B) generic richness with elevations from eld data; (C) species richness with elevations from DEM data; (D) generic richness with elevations from DEM data. For each graph the hollow circles show observed richness and solid circles show MDE null predictions.

adding elevational-width of equal area-bands as an additional explanatory variable in a multiple linear regression high r2 values increased marginally whereas low r2 values increased appreciably (see Table 2). Slope values for the relationship between generic richness and MDE null predictions for field and DEM data for 15 equal-area bands, and for field data for 10 equal-area bands were 5/1.09/0.1 (see Table 2). For all types of data, MDE predictions generally underestimated the observed numbers of taxa (see Fig. 5). Slope values for species-level data were all considerably further from 1 than for genus-level data (see Table 2), revealing a greater under-estimation of actual species richness

patterns by MDE null model predictions (see also Fig. 5).

Discussion
Data quality
With the field and DEM methods we have used two different techniques for obtaining elevation range data from specimen records. As one would expect, both methods have produced broadly similar patterns, although there are slight discrepancies with the max-

Table 2. Results from multiple linear regression analysis of richness against mid-domain effect predictions and equal-area elevational band-width using Method 2. MDE null predictions are correlated with observed richness patterns once area has already been accounted for. Data type Field Field Field Field Field Field DEM DEM DEM DEM DEM DEM Elevation range (m) 0 /2800 0 /2800 0 /2800 0 /2438 0 /2438 0 /2438 0 /2803 0 /2803 0 /2803 0 /2797 0 /2797 0 /2797 Taxonomic level Species Species Species Genera Genera Genera Species Species Species Genera Genera Genera No. equal area bands 5 10 15 5 10 15 5 10 15 5 10 15 Slope 1.39 1.61 1.63 0.48 0.92 0.90 2.04 1.97 1.99 0.38 0.88 1.06 r2 (MDE alone) 0.90 0.98 0.90 0.39 0.66 0.70 0.93 0.97 0.97 0.82 0.84 0.86 Multiple r2 0.92 0.98 0.95 0.99 0.93 0.91 0.94 0.98 0.97 0.95 0.85 0.87

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imum elevations. Assessing the accuracy of either method is problematic. The field data method may provide spurious results because pre-twentieth century herbarium records are less likely to have accurate elevation data due to imprecision of maps and inadequate measuring equipment; even modern altimeters can give misleading measurements. The DEM method may be inaccurate due to imprecise georeferencing or the inexactness of the DEM itself. A strength of this study is that it builds directly on current taxonomic expertise. Data for this analysis are derived directly from individual records for each species (i.e. herbarium specimens), which are primary observations. The database includes the vast majority of available specimen records for New Guinea palms and expert taxonomists have verified the identity of each record. Thus, we feel our data are impeccably sourced and any problem detected during the analysis can be readily investigated. Most other studies have had to rely on distribution data contained in published monographs and field guides, in the form of line maps or dot maps, or written descriptions of distributions. We have therefore avoided some of the additional assumptions associated with the use of such secondary data sources, such as poor coverage of specimens inadequately reflecting true geographic ranges, the incorrect identification of individual records, or outdated taxonomic concepts. As practising taxonomists, we encourage others to use a more explicit, specimen-based approach. Sampling procedure can have a significant influence on richness estimates (Wolda 1987, Rahbek 1995). When investigating Rapoports rule, for example, Colwell and Hurtt found that simply following a standard procedure, such as sampling with equal effort at points along a gradient, can produce a spurious Rapoport effect (Colwell and Hurtt 1994). The relationship between area and sampling effort in each elevational band in this study is illustrated in Fig. 2. Although the number of collections is not equal along the elevational gradient, the graph shows that collection intensity nevertheless varies in proportion with land area in each elevation band, as one would expect.

overestimated in the centre of the gradient, richness may also be underestimated at the periphery since it cannot be interpolated beyond the range limits (Grytnes and Vetaas 2002). However, interpolating species ranges is a pragmatic solution to an intractable analytical problem, as we have no evidence that species are not found where the ranges have been interpolated, which may not noticeably alter the underlying trends in richness (Lees et al. 1999). Furthermore, after plotting the residuals from the linear regression of log area and log species/ genus richness against elevation (Rahbek 1995) the midelevation peak was still evident with all four analyses (graphs not reproduced here).

The influence of area

The analysis of richness patterns of palm species and genera along the elevational gradient in New Guinea yields further evidence for the significant influence of area on these patterns. The species-area relationship has been universally acknowledged, although the exact structure of the relationship is still under discussion (Connor and McCoy 1979, Plotkin et al. 2000, Crawley and Harral 2001). Method 1 shows that area alone explains a good deal of the variation in observed richness (Table 1). Method 2 shows that by factoring out area the richness pattern changes from roughly monotonic to unimodal, irrespective of taxonomic scale or number of equal-area bands. This agrees with previous studies that have found a hump-shaped species richness pattern after accounting for area (Lawton et al. 1987, Rahbek 1997). However, if richness along the elevational gradient were entirely dependent on the effect of area, the richness pattern would vary little across the gradient when examined using equal-area bands. As can be seen in Fig. 3B this is not the case and richness peaks at mid-elevations when the effect of area is removed. The influence of area is completely removed using the equalarea band method and allows the area-controlled richness pattern to be directly compared with MDE null predictions. We suggest that all subsequent MDE analyses need to take into account the influence of area, and this can easily be achieved using the equal-area band methodology presented here. Using equal-area bands in regions where amount of available area declines steadily with elevation, such as New Guinea (see Fig. 2), means that equal-area bands increase in elevational breadth as elevation increases. This might mean that species richness for equal-area bands will increase with elevation simply because as the elevational breadth of each band increases so each band will include a greater number of species, assuming the RSFD remains roughly the same with elevation, and also because beta diversity (species turnover) tends to increase with elevation (Colwell pers. comm., see also
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Interpolation
It is an assumption inherent in this study that species occur in all elevational bands between the minimum and maximum observed values. Such interpolation is typical of analyses involving species richness estimates (Whittaker et al. 2001, Grytnes and Vetaas 2002). It has been suggested that species richness estimates based on interpolation may overestimate richness towards the centre of the gradient because species are only strictly observed in bands at the extreme ends of each species range (Grytnes and Vetaas 2002). In addition to being 306

Rahbek 1997). In New Guinea palms, elevational ranges increase with elevation for both species and genera (Spearmans rank correlation between mean elevational range and elevational breadth for equal-area bands: coefficient rs 0/0.72 and 0.79 for species field and DEM data, respectively, n0/145; 0.85 and 0.98 for generic field and DEM data, respectively, n0/24). This increase in mean elevational range accompanies a reduction in the number of taxa at higher elevations, so countering the possible artefacts from increases in the elevational breadth of equal-area bands. Furthermore, the addition of elevational width of equal-area bands to the regression model in most cases accounted for only a marginal increase in the amount of explained variation in the observed richness pattern (see Table 2).

The mid-domain effect in New Guinea palms

Despite growing evidence, there is still great scepticism surrounding the importance of the mid-domain effect. So far only a handful of studies have considered the influence of area and MDE on richness (Rahbek 1997, Lees et al. 1999, Jetz and Rahbek 2001, Koleff and Gaston 2001, Sanders 2002). In these studies, the combined effects of area and MDE were found to explain a large proportion of the variance in observed richness. Our study also supports these findings. MDE predictions conditionally explained up to 98% of the variance in observed richness in this study after the effect of area had been removed (species field data, 10 equalarea bands, r2 0/0.98). However, as the authors were themselves careful to point out, geometric constraints are an additional influence on patterns of species richness (hence the name mid-domain effect; Colwell and Lees 2000); it is not claimed to be the sole explanation. Vascular plants have rarely been considered in MDE analyses until now (but see Grytnes and Vetaas 2002), but our results and others point to the general influence of MDE across a wide range of taxa such as birds, mammals, insects, and vascular plants. This study furthermore shows that MDE is also important at different taxonomic scales. However, despite the high r2 values (Table 2), MDE null predictions consistently underestimate observed richness patterns (Fig. 5A /D). This may be a result of the way in which the RangeModel software (Colwell 2000) calculates richness along the domain (see Fig. 1 in Colwell and Lees 2000). Setting the bin range effectively determines the number of times the domain is intersected. For instance, if the domain limits are 0 and 1, and the number of bins is 5, the domain would be intersected at 0.1, 0.3, 0.5, 0.7 and 0.9. Every time a range crosses one of these points, the richness total for that bin increases by one. If a species range extended from 0.4 to 0.8, it would intersect the bins at 0.5 and 0.7, thus
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adding to their respective totals. Richness for each bin is calculated as the total number of ranges intersected at that point. Using this intersect method it is possible that very small ranges might lie between these points which will not be picked up in the richness totals for that bin. This is more likely to occur for RSFDs that contain a high proportion of small ranges. Taxa are also more likely to be missed when the number of bins is small, due to the increased size of the gap between the intersection points. This may explain why observed richness is explained least well (e.g. genus field data, 5 equal-area bands, r2 0/0.39) by the MDE when the gradient is split into fewer bins/equal area bands. Inspecting the slope values for all relationships, only those for generic field data for 10 and 15 equal-area bands and generic DEM data for 15 equal-area bands were within 0.1 of an ideal slope of 1.0. The slope when using only 5 equal-area bands for genera for both field data and DEM data was considerably smaller than for both 10 and 15 bands with the same data type, again suggesting that 5 equal-area bands is too few to accurately represent richness patterns over an elevational gradient of this size (see Table 2). Furthermore, the slope values are furthest from 1 for species data (especially species DEM data), showing that MDE predictions under-estimated observed numbers of taxa more when ranges were smaller, and lending weight to the supposition that small species ranges are being missed between the intersections of the domain. Analyses that have considered the combined effects of area and MDE (in one dimension), including this study, have shown that these factors can explain observed richness patterns well (Jetz and Rahbek 2001, Koleff and Gaston 2001, Sanders 2002). MDE null models have attracted criticism for only considering richness patterns across one dimension when, of course, species have ranges extending in two dimensions (Bokma and Monk konen 2000, Koleff and Gaston 2001). A two-dimen sional approach has also been developed (Jetz and Rahbek 2001) which indicates that MDE null predictions across two dimensions can still explain a significant amount of the variance in observed richness patterns. It must be noted, however, that these two-dimensional predictions did not explain as much as the one-dimensional models. In order to fully understand the importance of the MDE it needs to be considered alongside various other factors that may contribute to the pattern of species richness. Unfortunately, data were not available in this analysis for the investigation of other variables that may have contributed to the pattern (e.g. productivity, temperature). Two multivariate analyses have shown that the MDE can still be an important explanatory variable in studies of richness gradients (Lees et al. 1999, Jetz and Rahbek 2002); we support calls for the influence 307

of MDE to be further assessed on an equal footing with other determinants of species richness patterns.

The mid-domain effect and Rapoports elevational rule

Rapoports rule states that there is a simple positive correlation between species latitudinal range-size and latitude (Stevens 1989), following an original observation by Rapoport (1982). This idea has also been extended by Stevens (1992) to elevational gradients, where species elevational ranges would increase with elevation, and so decrease in extent towards the lowlands. Rapoports elevational rule runs counter to the expectation of the mid-domain effect, which predicts greatest species richness at middle elevations due to the geometric constraints exerted by the upper and lower boundaries of the elevational gradient. For New Guinea palms, elevational range does indeed increase with midpoint of elevation, and, as Fig. 3A shows, species richness does appear to be greater at low elevations without accounting for the differing amount of available area at different elevations. However, it should be evident from Fig. 3B that, after accounting for area, the results presented here provide support for the expectations of the mid-domain effect model, and against those of Rapoports elevational rule (see also Rahbek 1997). This suggests that it is simply the greater available area of lowland regions which gives rise to their apparent diversity, and that the Rapoport rescue effect, which remains largely untested in tropical lowland environments, may not be the cause of such species richness gradients.

islands. Given the urgent need to understand the factors dictating the distribution of tropical diversity, it is vital that new ecological models such as the mid-domain effect are explored over the broadest taxonomic spectrum and across a wide range of geographical scales and locations. Islands such as New Guinea present significant challenges to our understanding of biodiversity being extremely rich biologically and yet poorly explored. Detailed knowledge of tropical plant diversity is still limited by a shortage of good collections, especially for plant families such as palms, which are difficult to collect and often under-represented in herbaria. Although collection densities of palms in New Guinea remain low, a one-dimensional approach yields a wellsampled gradient that can be analysed effectively using null models. It seems likely that many similar datasets exist and we encourage others to undertake analyses such as ours. This study adds significantly to the growing body of evidence supporting the influence of the mid-domain effect. This effect is undoubtedly an important consideration for any analysis of richness gradients. Using a simple yet novel method, we have demonstrated that it is essential to account for the influence of area on species richness patterns when exploring concepts such as the mid-domain effect. In our study, the observed richness patterns can be explained to a strikingly large extent by the combined role of the mid-domain effect and area. In future, these factors need to be considered in a multivariate context to understand their ultimate importance relative to additional environmental variables. While findings such as ours may continue to be controversial in the short term, we believe that, in time, the role of the mid-domain effect will become increasingly accepted as one of several factors determining species richness patterns.
Acknowledgements / Many people contributed to the New Guinea palm database, in particular Roy Banka, Anders Barfod, Kate Davis, Anders Kjaer, Meesha Patel and Helen Sanderson. We thank the staff of the herbaria at Aarhus, Brisbane, Bogor, Kew, Lae and Leiden for kindly providing access to collections and data. We thank Robert Colwell, David Lees and John-Arvid Grytnes for valuable discussions and numerous comments on earlier versions of the manuscript. Carsten Rahbek made many suggestions that improved the paper. This work was supported by a student internship from the Royal Botanic Gardens, Kew to SPB, a studentship from the Bernard Sunley Charitable Trust to NAB and by funding from the BAT Biodiversity Partnership to the Palms of New Guinea project.

Taxonomic scale
This study is one of the first yet completed to assess the mid-domain effect at both species and genus level. Although the use of indicator taxa remains contentious for biodiversity studies, genera are now well established as reliable higher-taxonomic surrogates for species-level diversity patterns (Williams and Gaston 1994, La Ferla et al. 2002). It is clear from Fig. 5 that patterns in taxon richness across the elevational gradient, including the results of mid-domain effect null model simulations, are similar and highly correlated between both species and genera, further demonstrating the generality of the middomain effect.

References
Conclusions
Few studies of this kind have focused on vascular plants and even fewer have been based on taxa from tropical 308
Anon. 1999. ArcView GIS. / ESRI, Redlands, California. Anon. 2001. GTOPO30 / Global topographic data. / USGS, B/http://edcdaac.usgs.gov/gtopo30/gtopo30.html /, last accessed: 30 Sept 2002. Arrhenius, O. 1921. Species and area. / J. Ecol. 9: 95 /99.
ECOGRAPHY 27:3 (2004)

Baker, W. J. 2002. The palms of New Guinea project. / Fl. Males. Bull. 13: 35 /37. Bokma, F. and Monkkonen, M. 2000. The mid-domain effect and the longitudinal dimension of continents. / Trends Ecol. Evol. 15: 288 /289. Brown, J. H. 1971. Mammals on mountaintops: nonequilibrium insular biogeography. / Am. Nat. 105: 467 /478. Colwell, R. K. 2000. RangeModel: a Monte Carlo simulation tool for assessing geometric constraints on species richness. Ver. 3. / Users guide and application, B/http://viceroy.eeb. uconn.edu/asn/. Colwell, R. K. and Hurtt, G. C. 1994. Nonbiological gradients in species richness and a spurious Rapoport effect. / Am. Nat. 144: 570 /595. Colwell, R. K. and Lees, D. C. 2000. The mid-domain effect: geometric constraints on the geography of species richness. / Trends Ecol. Evol. 15: 70 /76. Colwell, R. K., Rahbek, C. and Gotelli, N. J. in press. The middomain effect and species richness patterns: what have we learned so far. / Am. Nat. Connor, E. F. and McCoy, E. D. 1979. The statistics and biology of the species-area relationship. / Am. Nat. 113: 791 /833. Crawley, M. J. and Harral, J. E. 2001. Scale dependence in plant biodiversity. / Science 291: 864 /868. Darwin, C. 1859. On the origin of species by means of natural selection or the preservation of favoured races in the struggle for life. / John Murray, London. Diniz-Filho, J. A. F. et al. 2002. Null models and spatial patterns of species richness in South American birds of prey. / Ecol. Lett. 5: 47 /55. Grytnes, J. A. and Vetaas, O. R. 2002. Species richness and altitude: a comparison between null models and interpolated plant species richness along the Himalayan altitudinal gradient, Nepal. / Am. Nat. 519: 294 /304. Heaney, L. R. 2001. Small mammal diversity along elevational gradients in the Philippines: an assessment of patterns and hypotheses. / Glob. Ecol. Biogeogr. 10: 15 /39. Jetz, W. and Rahbek, C. 2001. Geometric constraints explain much of the species richness pattern in African birds. / Proc. Natl. Acad. Sci. USA 98: 5661 /5666. Jetz, W. and Rahbek, C. 2002. Geographic range size and determinants of avian species richness. / Science 297: 1548 / 1551. Kaspari, M., ODonnell, S. and Kercher, J. R. 2000. Energy, density, and constraints to species richness: studies of ant assemblages along a productivity gradient. / Am. Nat. 155: 280 /293. Kessler, M. 2001. Pteridophyte species richness in Andean forests in Bolivia. / Biodiv. Conserv. 10: 1473 /1495. Koleff, P. and Gaston, K. J. 2001. Latitudinal gradients in diversity: real patterns and random models. / Ecography 24: 341 /351. La Ferla, B. et al. 2002. Continental scale patterns of biodiversity: can higher taxa accurately predict African plant distributions? / Bot. J. Linn. Soc. 138: 225 /235. Lawton, J. H., MacGarvin, M. and Heads, P. A. 1987. Effects of altitude on the abundance and species richness of insect herbivores on bracken. / J. Anim. Ecol. 56: 147 /160. Lees, D. C., Kremen, C. and Andriamampianina, L. 1999. A null model for species richness gradients: bounded range overlap of butteries and other rainforest endemics in Madagascar. / Biol. J. Linn. Soc. 67: 529 /584. Lyons, S. K. and Willig, M. R. 1997. Latitudinal patterns of range size: methodological concerns and empirical evaluations for New World bats and marsupials. / Oikos 79: 568 / 580. MacArthur, R. H. 1972. Geographical ecology: patterns in the distribution of species. / Harper and Rowe. Nor, S. M. 2001. Elevational diversity patterns of small mammals on Mt. Kinabalu, Sabah, Malaysia. / Glob. Ecol. Biogeogr. 10: 41 /62.

Ohlemuller, R. and Wilson, J. B. 2000. Vascular plant species richness along latitudinal and altitudinal gradients: a contribution from New Zealand temperate rainforests. / Ecol. Lett. 3: 262 /266. Patterson, B. D. et al. 1998. Contrasting patterns of elevational zonation for birds and mammals in the Andes of southeastern Peru. / J. Biogeogr. 25: 593 /607. Plotkin, J. B. et al. 2000. Predicting species diversity in tropical forests. / Proc. Natl. Acad. Sci. USA 97: 10850 / 10854. Pineda, J. and Caswell, H. 1998. Bathymetric species-diversity patterns and boundary constraints on vertical range distributions. / Stud. Oceanogr. 45: 83 /101. Rahbek, C. 1995. The elevational gradient of species richness: a uniform pattern? / Ecography 18: 200 /205. Rahbek, C. 1997. The relationship among area, elevation, and regional species richness in Neotropical birds. / Am. Nat. 149: 875 /902. Rapoport, E. H. 1982. Areography: geographical strategies of species. The Fundacion Bariloche Series Vol. 1. / Pergamon Press. Rickart, E. A. 2001. Elevational diversity gradients, biogeography and the structure of montane mammal communities in the intermountain region of North America. / Glob. Ecol. Biogeogr. 10: 77 /100. Rosenzweig, M. L. 1992. Species diversity gradients: we know more and less than we thought. / J. Mammal. 73: 715 /730. Rosenzweig, M. L. 1995. Species diversity in space and time. / Cambridge Univ. Press. Rosenzweig, M. L. and Abramsky, Z. 1993. How are diversity and productivity related? / In: Ricklefs, R. E. and Schluter, D. (eds), Species diversity in ecological communities: historical and geographical perspectives. Univ. of Chicago Press, pp. 52 /65. Sanchez-Cordero, V. 2001. Small mammal diversity along elevational gradients in Oaxaca, Mexico. / Glob. Ecol. Biogeogr. 10: 63 /76. Sanders, N. 2002. Elevational gradients in ant species richness: area, geometry, and Rapoports rule. / Ecography 25: 25 / 32. Stevens, G. C. 1989. The latitudinal gradient in geographic range: how so many species coexist in the tropics. / Am. Nat. 133: 240 /256. Stevens, G. C. 1992. The elevational gradient in altitudinal range: an extension of Rapoports latitudinal rule to altitude. / Am. Nat. 140: 893 /911. Wallace, A. R. 1876. The geographical distribution of animals. / Macmillan. Whittaker, R. H. 1960. Vegetation of the Siskiyou Mountains, Oregon and California. / Ecol. Monogr. 30: 279 /338. Whittaker, R. J., Willis, K. J. and Field, R. 2001. Scale and species richness: toward a general hierarchical theory of species diversity. / J. Biogeogr. 28: 453 /470. Willdenow, K. L. 1805. The principles of botany, and vegetable physiology. / Blackwood, Cadell and Davies, London. Williams, C. B. 1943. Area and number of species. / Nature 152: 264 /267. Williams, P. H. and Gaston, K. J. 1994. Measuring more of biodiversity: can higher-taxon richness predict wholesale species richness. / Biol. Conserv. 67: 211 /217. Williamson, M. 1988. Relationship of species number to area, distance and other variables. / In: Myers, A. A. and Giller, P. S. (eds), Analytical biogeography. Chapman and Hall, pp. 94 /115. Willig, M. R. and Lyons, S. K. 1998. An analytical model of latitudinal gradients of species richness with an empirical test for marsupials and bats in the New World. / Oikos 81: 93 /98. Wolda, H. 1987. Altitude, habitat and tropical insect diversity. / Biol. J. Linn. Soc. 30: 313 /323.

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Appendix 1. Ranges of equal-area bands for each of 5, 10 and 15 bands used. Minimum and maximum elevations in metres for each equal-area band along the elevation gradient are given (as used in Method 2). Ranges are shown separately for each data type (Field and DEM).
Band Field data, Species Min (m) 5 Bands 1 2 3 4 5 0.5 14.5 122.8 304.6 923.2 Max (m) 14.5 122.8 304.6 923.2 2800.0 1.2 14.5 56.7 122.8 219.8 304.6 550.3 923.2 1631.8 2800.0 1.0 1.5 14.5 40.8 74.1 122.8 185.4 252.7 304.6 435.7 630.8 923.2 1467.3 2017.2 2800.0 Field data, Genera Min (m) 0.5 12.7 113.3 296.6 855.4 0.5 1.2 12.7 52.7 113.3 206.2 296.6 487.0 855.4 1510.8 0.5 1.0 1.5 12.7 37.4 69.4 113.3 172.4 238.5 296.6 376.7 587.8 855.4 1262.5 1722.5 Max (m) 12.7 113.3 296.6 855.4 2438.0 1.2 12.7 52.7 113.3 206.2 296.6 487.0 855.4 1510.8 2438.0 1.0 1.5 12.7 37.4 69.4 113.3 172.4 238.5 296.6 376.7 587.8 855.4 1262.4 1722.5 2438.0 DEM data, Species Min (m) 0.5 14.5 122.8 304.6 923.7 0.5 1.2 14.5 56.7 122.8 219.9 304.6 550.8 923.7 1633.5 0.5 1.0 1.5 14.5 40.8 74.1 122.8 185.5 252.9 304.6 436.1 631.3 923.7 1468.7 2019.7 Max (m) 14.5 122.8 304.6 923.7 2803.0 1.2 14.5 56.7 122.8 219.9 304.6 550.8 923.7 1633.5 2803.0 1.0 1.5 14.5 40.8 74.1 122.8 185.5 252.9 304.6 436.1 631.3 923.7 1468.7 2019.7 2803.0 DEM data, Genera Min (m) 0.5 14.5 122.7 304.6 922.6 0.5 1.2 14.5 56.6 122.7 219.7 304.6 550.0 922.6 1629.9 0.5 1.0 1.5 14.5 40.8 74.0 122.7 185.3 252.6 304.6 435.4 630.3 922.6 1465.9 2015.0 Max (m) 14.5 122.7 304.6 922.6 2797.0 1.2 14.5 56.6 122.7 219.7 304.6 550.0 922.6 1629.9 2797.0 1.0 1.5 14.5 40.8 74.0 122.7 185.3 252.6 304.6 435.4 630.3 922.6 1465.9 2015.0 2797.0

10 Bands 1 0.5 2 1.2 3 14.5 4 56.7 5 122.8 6 219.8 7 304.6 8 550.3 9 923.2 10 1631.8 15 Bands 1 0.5 2 1.0 3 1.5 4 14.5 5 40.8 6 74.1 7 122.8 8 185.4 9 252.7 10 304.6 11 435.7 12 630.8 13 923.2 14 1467.3 15 2017.2

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