Biological Conservation, Vol. 84, No. 3, pp.

251-262, 1998
PII: ELSEVIER

S0006-3207(97)00115-8

1998 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0006-3207/98 $19.00 + 0.00

P A T T E R N S OF A F R I C A N P R I M A T E D I V E R S I T Y A N D T H E I R E V A L U A T I O N F O R THE SELECTION OF C O N S E R V A T I O N AREAS

Jocelyn E. Hacker, a G u y C o w l i s h a w b* & Paul H. Williams c

aEcology and Conservation Unit, Department of Biology, University College London, Gower Street, London WCI E 6BT, UK ~Department of Anthropology, University College London, Gower Street, London WCIE 6BT, UK CBiogeography and Conservation Laboratory, Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

(Received 25 January 1997; revised version received 1 July 1997; accepted 10 July 1997)

Abstract This study evaluates spatial patterns o f primate diversity and their implications f o r conservation area-selection in continental Africa and Madagascar. Each cell in a 1 latitude-longitude grid is scored for taxon richness, character richness, rarity-weighted richness (endemism), and threatened taxon richness. The spatial patterns o f these measures are plotted and compared. Hotspots o f taxon richness and threatened taxon richness are clustered and show a high degree o f congruence, but endemic hotspots are scattered and show little coincidence with either. The efficiency o f area-selection through complementarity is demonstrated and the influence o f the conservation status o f the target taxa on that efficiency is investigated. Complementary areas selected on the basis o f threatened taxa tend to capture a greater proportion o f total taxon richness than areas selected on a more indiscriminate basis. At a finer spatial scale, local sites o f high primate taxon richness are similarly shown to contain a greater proportion o f threatened taxa and possess threatened taxa o f higher conservation status. These results suggest that the protection o f areas containing threatened taxa will also lead to the protection o f areas o f high taxon richness among African primates. 1998 Elsevier Science Ltd. All rights reserved Keywords: primates, diversity, conservation, area-selection, Africa.

INTRODUCTION

Biodiversity is a multifaceted phenomenon which can be valued in a variety of ways. One important consequence of this is that the identity of conservation priorities can be highly dependent on the method of evaluation *To whom correspondence should be addressed. Fax: 0171380 7728; e-mail: g.cowlishaw@ucl.ac.uk 251

employed. Understanding how different values can lead to different priorities is of fundamental importance in the development of biodiversity conservation strategies. One criterion which is particularly relevant in the evaluation of conservation areas is the richness of the fauna or flora present. Another is the conservation status of those taxa. For the goal of effective biodiversity conservation, which of these values should receive greatest priority is a moot point. The attribution of greatest value to areas of high species richness can potentially lead to a rapid deterioration of diversity, through a lack of consideration of the needs of threatened taxa (Kershaw et al., 1995). Alternatively, a focus on sites which contain threatened taxa might lead to the neglect of highly diverse areas. Indeed, even in the same area, management for threatened species may reduce diversity (e.g. Alper, 1992). This dilemma between richness and threat has led many practitioners to adopt an approach which incorporates both criteria into their conservation strategy. The IUCN/SSC Primate Specialist Group "has set itself the goal of maintaining the current diversity of the order Primates, with a dual emphasis on: (1) ensuring the survival of endangered and vulnerable species wherever they occur; and (2) providing effective protection for large numbers of primates in areas of high primate diversity and/or abundance" (Oates, 1986; see also Oates, 1996). With this two-pronged strategy in mind, Oates evaluated a set of sites in Africa using rank scores for species richness, endemism and conservation status. These parameters were combined into a single rank index which was used to identify the priority sites among the range of options identified. The purpose of this paper is to develop this approach in order to explore in more detail the patterns of richness, rarity and endangerment and their implications for conservation area-selection in African primate taxa. Our development of the approach is threefold. First, we use four diversity parameters at a broader scale across the entire continent. Second, our evaluation procedure recognizes

252

J. E. Hacker, G. Cowlishaw, P. H. Williams

This report is used since it is the only source in which (I) taxa are coded for conservation status to the subspecific level (using the most recent taxonomic information available) and (2) taxa in both continental Africa and Madagascar are coded using the same system. The distribution data for the 205 taxa were taken from the most recent sources available (Appendix 1). The ranges in these sources were copied on to a 1o latitude-longitude grid map of sub-Saharan Africa and Madagascar. A taxon was considered to be present in a cell when its range covered more than one half of the area of that grid cell. Macaca sylvanus was incorporated throughout the analysis but does not appear on the maps provided (Figs 1 and 2) because its range is north of the Sahara. Papio hamadryas extends its geographic range into Arabia but these populations were excluded from the analysis owing to their location and genetic isolation. The assessment of conservation status of each taxon is taken from the CAMP analysis, which follows Mace and Lande (1991). Their classification consists of a series of codes based on an increasing risk of extinction over a diminishing period of time; safe, vulnerable, endangered and critical. According to these criteria, 90 of the 205 African taxa are threatened (Table 1). The phylogenetic tree for these taxa was based on the composite estimate of phylogeny by Purvis (1995). A limited number of alterations were necessary to match the list of taxa on this phylogeny to that in the C A M P analysis. These were (1) the addition of all sub-species (treated as multiple branches arising from a single point at the end of the relevant species branch); (2) the removal of Cercopithecus dryas (not recognized by Oates, 1986; now synonymous with C. salongo: Oates, 1996); and (3) the inclusion of Cercopithecus denti as a subspecies of C. wolff (Lernould, 1988). In addition, it was necessary to add the following taxa (whose positions on the tree were determined from the same papers); seven Lepilemur species (Harcourt and Thornback, 1990), Galago thomasi and G. gallarum (Nash et al., 1989), Cercopithecus pygerythrus, C. sabaeus, C. albogularis, C. sclateri and C. atys (Lernould, 1988), Colobus vellerosus and Procolobus gordenorum, P. pennanti and P. rufomitratus (Oates, 1986).
Table 1. African primate taxa and conservation status

all taxa up to the level of subspecies. Finally, we conduct these analyses with the primates of both continental Africa and Madagascar. We have three main aims in this exercise. First, to describe spatial patterns of primate diversity for each evaluation criterion. Second, to identify the respective hotspots of diversity and their characteristics in accordance with these values. Finally, to investigate the efficiency of area-selection by complementarity and how it might be influenced by the conservation status of target taxa. We also describe a previously undetected but important relationship between taxon richness and conservation status. Since a detailed network of complementary reserves has already been proposed for continental African primates (Oates, 1986, 1996) and broadly reviewed for Malagasy primates (Mittermeier et al., 1992), the purpose of this study is not to define a range of alternative sites. Rather, our focus lies in the systematic examination of how alternative evaluation measures for primate diversity might influence area conservation strategies. Area-selection is a particularly relevant aspect of conservation planning for primates, since habitat loss and site protection are widely seen as the key issue in their conservation (Oates, 1986) and their wide appeal may make them ideal flagships for tropical ecosystems (Mittermeier, 1988).

METHODS

Primate diversity is evaluated across Africa at a 1 latitude-longitude grid cell scale. These cells are not proposed as the unit of conservation, but rather that key sites might, in principle, be identified within such an area. However, to substantiate the conclusions obtained at this scale, we also carry out an analysis at the local site level. Madagascar, because of its size and distinctiveness of taxa, is often considered a separate region from continental Africa for the purposes of conservation planning. However, rather than make any a priori assumptions, all these analyses were conducted for continental Africa both including and excluding Madagascar. Comparison between the two reveals that the inclusion of the latter has little effect on the emergent patterns in the former. Consequently, and for the sake of brevity, only the results of the inclusive analysis are described.
The database

Taxon

Total taxa

Conservation status C E V CEV 25 4 22 32 7 65 25 Safe 24 l0 7 74 0 91 24

For each of the 205 primate species and subspecies of continental Africa and Madagascar, the database compiled for this paper describes (l) the geographic range, (2) the conservation status, and (3) the phylogenetic relationships of each of the taxa. The list of taxa follows the Primate Conservation Assessment and Management Plan (or C A M P report: Stevenson et al., 1992), prepared for the IUCN/SSC Primate Specialist Group and Captive Breeding Specialist Group (see Mace, 1994).

Lemuriformes Lorisiformes Colobines Cercopithecines Pongids Africa Madagascar

49 14 29 106 7 156 49

7 10 8 0 0 4 2 5 15 4 7 21 1 0 6 7 12 46 7 10 8

Data from Stevenson et al. (1992); C (critical), E (endangered), V (vulnerable), CEV (all threatened taxa) and safe (all nonthreatened taxa).

P r i m a t e diversity and conservation

253

Evaluation criteria Biological diversity can be evaluated on the basis of single or multiple criterion indices. In this analysis of area evaluation, four indices, two of each type, are employed. The first single-criterion index is 'taxon richness', i.e. the total number of lowest-rank taxi, either species or subspecies, present. The second is 'character richness', a measure of the evolutionary distinctiveness of the t a x i present. Here this is calculated on a phylogenetic basis, as the number of nodes (branching points) between the primate taxi at that site (Faith, 1994; Humphries and Williams, 1994). There are two alternative approaches used in multiple-criterion evaluation (e.g. Williams, 1997). The first is to devise a single index which combines two or more criteria. This method is used for the first such index, where taxon richness is weighted by the geographic range size of the species present to determine the 'rarity-weighted richness' of an area. Range size is a common measure of rarity (Gaston, 1994), and is used in the evaluation of the conservation status of primates in the IUCN/SSC Action Plans (Mittermeier et al., 1992; Oates, 1996) but not the C A M P report (Stevenson et al., 1992). Rarity-weighted richness is calculated as the sum of rarity scores for all taxi present in a grid cell, where the rarity score for each taxon is the reciprocal of the number of cells in which it occurs (e.g. Williams et al., 1996); the cells which score most highly are therefore those which have a large number of restricted-range taxi. The second approach to multiple-criterion indices is that of sequential filtering. This is used in the final index, in which taxon richness is combined with endangerment by discarding all taxi which are not classified as threatened (following Stevenson et al., 1992; Table 1) and then evaluating taxon richness for the remaining database of threatened taxi. This measure is called 'threatened taxon richness'. Area selection algorithm The principle of complementarity is widely seen as the most efficient way to achieve the goal of all-taxon representation in a set of protected areas. This efficiency has been formally demonstrated in a variety of taxi (e.g. Afrotropical antelope: Kershaw et al., 1995; South African estuarine avifauna: Turpie, 1995; British birds: Williams et al., 1996). Complementarity has also been informally applied in the identification of a network of reserves for the conservation of continental African primates (Oates, 1986). In the following analyses, the efficiency of this method is formally demonstrated for the primates of Africa including Madagascar, and the effects of the conservation status of the target taxi on this efficiency is investigated. The procedure used here to implement complementarity is a heuristic approximation to truly optimal sets and hence produces a 'nearminimum' set, i.e. that set of grid cells which approaches the fewest cells required to represent each taxon at least once (although higher thresholds of representation

can be set; e.g. Margules et al., 1988). The algorithm has three steps (Williams, 1994): (1) select those grid cells which have taxa limited solely to that cell (or, where more than one representation per taxa is required, those cells which contain taxa which occur in fewer cells than the representation goal), (2) order all the remaining grid cells according to their rarity-weighted richness score (where there is a tie between cells, that cell with the greatest number of taxa is selected), (3) pass backward through this sequence and eliminate redundant grid cells by removing those which lack unique taxa within the selected set. The resulting collection of grid cells is a near-minimum set. Other than the proportion of cells that are essential to this set (either because they contain a unique taxon or combination of taxa), flexibility of choice with grid cells outside the set is possible.

Diversity at local sites In order to substantiate the conclusions drawn from the macro-scale analysis, further tests are carried out using data for named sites in Africa. The majority of these sites are protected areas. The continental African sites are drawn from several sources to represent a range of countries, geographical areas and primate communities. In total, 17 sites are used across 12 countries with between 1 to 16 taxi (Appendix 2). Sites are only included where it is certain that nocturnal as well as diurnal taxi were recorded. These taxi are mostly identified to species and are hence coded for conservation status following Oates (1996) (Stevenson et al., 1992 only provide codes at the subspecific level). These codes are numeric and range from one to four (the safest to the most endangered species; Oates, 1996). Sites in Madagascar are taken from Mittermeier et al. (1992). These comprise a total of 35 sites with between 1 to 11 taxi, which are coded for conservation status in the same source using a similar numerical system to Oates. A further 11 sites in Madagascar are excluded since they do not specify either the species or the subspecies of a taxon present.

RESULTS

Spatial patterns of diversity Patterns of primate diversity according to the four evaluation criteria employed are plotted across sub-Saharan Africa and Madagascar (Fig. 1). The first notable feature is a consistent attribution of high value to equatorial regions by each of the four measures. Several coastal stretches also possess relatively high scores. Second, Madagascar scores moderately well in terms of taxon richness but performs poorly in character richness. This is because the continental cells contain taxi which are more widely dispersed across the phylogeny than the Malagasy cells (which contain only lemurs); since character richness counts the number of intervening nodes between taxi, continental Africa

254
(a)

J. E. Hacker, G. Cowlishaw, P. H. Williams

(b)

(c)

(d)

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............ iiii~iii:..... ,J

,. lli
|

j
Africa, with the exception of the barbary macaque of Morocco and Algeria (not shown) and the gelada b a b o o n of the Ethiopian Highlands. Finally, the patterns of rarity-weighted richness are generally more patchy than either of those obtained using the preceding all-taxon measures, with coastal areas in particular growing in importance. Madagascar scores very highly in this measure of rarity, since the geographic ranges of all Malagasy taxa are limited to the size of the island. The total number of primate taxa, occupied grid cells (total number of cells which contain primate taxa) and records per taxa (the number of grid cells per taxa) for these patterns are summarized in Table 2.

Fig. 1. Comparison of patterns of primate diversity in Africa using three different evaluation measures on a 1 latitude-longitude
grid: (a) taxon richness, (b) character richness, (c) threatened taxon richness and (d) rarity-weighted richness. In each of the four maps the grid cell with the maximum value is shown in black, whereas the other non-zeros scores are grouped into five classes (corresponding to the grey scale shown to the left of map (d)), each of which contains approximately equal numbers of grid cells. The maps have been smoothed by taking each cell's score as the mean score of the surrounding squares. The five cells containing the barbary macaque in north Africa are not shown. scores more highly. A measure of phylogenetic diversity that also incorporated branch lengths on the phylogenetic tree would generate higher scores for the Malagasy fauna, since m a n y Lemuriform taxa are of more ancient lineage than other African primates. With the exception of Madagascar, taxon richness and character richness show a high degree of similarity, supporting the findings of previous studies that taxon richness can generally be a good surrogate for character richness (e.g. Williams and Humphries, 1996). Third, threatened taxon richness also peaks in equatorial regions, particularly in west and central Africa. M a d a g a s c a r scores moderately highly, but threatened taxa are entirely absent from southern and northern

Primate diversity and conservation

Hotspots

255

(a)

(c)

Fig. 2. Comparison of hotspots of primate diversity in Africa (the top 5% of all grid cells) selected using different evaluation measures: (a) taxon richness, (b) rarity-weighted richness, and (c) threatened taxon richness. Grid cells with maximum values are shown in black, whereas the other non-zero scores are grouped into four classes (corresponding to the grey scale shown to the left of the maps), each of which contains approximately equal numbers of grid cells. The hotspot positions do not always exactly match the patterns shown in Fig. 1, since the hotspots are identified from the unsmoothed data.

Hotspots were identified as the top-scoring 5% of grid cells (Prendergast et al., 1993) for taxon richness, rarityweighted richness and threatened taxon richness (Fig. 2, Table 3). These hotspots can be related to the communities identified in the Action Plan for African primate conservation (Oates, 1986, 1996). The hotspots of taxon richness are clustered in two areas in West and Central Africa (Fig. 2(a)). These appear to correspond with the C a m e r o o n - W e s t e r n Equatorial and the Eastern Z a i r e Western Rift communities identified by Oates, respectively. A handful of outliers is observed between these clusters and in eastern Madagascar. Although each cell contains a large number of species, this set of hotspots represents less than half of all African primate taxa due to the high incidence of duplication a m o n g these areas. This is illustrated by the high number of records per taxon (Table 3 and Fig. 3). The highly dispersed rarity-weighted richness hotspots (Fig. 2(b)) incorporate further grid cells in the U p p e r Guinea, Ethiopian Highlands and Coastal East Africa communities, in addition to further continental grid cells in areas outside the Oates' communities. The largest cluster of rarity-weighted hotspots occurs in Madagascar. Overall, this set of hotspots represents 80% of all taxa (Table 3). Such coverage is achieved because this criterion weights areas in favour of those which contain taxa less likely to be found elsewhere; however, as a consequence, it performs relatively poorly in terms of the number of records of each taxon represented (Fig. 3) (comparison between taxon richness and rarity-weighted richness hotspots: Wilcoxon matchedpairs test, z = - 3 . 9 1 , p <0.001). The coverage of threatened taxa and all taxa in both sets of hotspots shows a high degree of similarity; 51 or 80% of threatened taxa in comparison to 45 and 80% of all taxa, using taxon richness or rarity-weighted richness criteria, respectively. Since the hotspots using these two criteria show widely different patterns of distribution, it is unsurprising that there is very little coincidence in their geographic localities for any subset of these areas (Table 4). The hotspots of threatened taxon richness show a similar distribution pattern to that found for all-taxon richness, except for an additional cluster of coastal grid cells which appear to fall in the Upper Guinea community
Table 2. Baseline diversity and distribution data for primate taxa in Africa

All taxa

Threatened taxa a CEV CE 36 125 174 C 14 39 48

Number of taxa Number of occupied grid cells Number of records (grid cells per taxon) b

205 1825 8205

90 784 1806

aSame key for column headings as Table 1. bSummed across all taxa.

256

J. E. Hacker, G. Cowlishaw, P. H. Williams

set for (l) all threatened taxa (i.e. all critical, endangered and vulnerable taxa), (2) all critical and endangered taxa, and (3) all critical taxa alone. The efficiency of coverage of all taxa (threatened and non-threatened) was then examined for each of the four cases, both in terms of (1) the total ratio of taxa to cells for the network as a whole, and (2) the mean number of taxa per grid cell in the network (Fig. 5). The results show that a focus on threatened taxa (rather than all taxa) provides more efficient coverage in terms of the mean taxa per cell. Furthermore, the total ratio of taxa per cell increases the higher the level of threat used as the

(Fig. 2(c)). The hotspots for threatened taxa attain similar taxon coverage as those for taxon richness, but in half the number of grid cells (Table 3). This is true for both threatened taxa and all taxa in each cell. This level of representation is below that of rarity-weighted hotspots, but its efficiency is marginally higher; i.e. the ratio of taxa per grid cell is 1-8 for rarity-weighted richness hotspots and 2.2 for threatened taxon richness hotspots. In terms of records per taxon (Fig. 3), the pattern obtained using this method resembles that of rarityweighted richness (z = - 0 . 6 6 , p = 0 . 5 1 ) not taxon richness (z = -6-32, p < 0.001). Importantly, there is a high degree of coincidence in the geographic distributions of the hotspots for all taxa and threatened taxa (Table 4). This might suggest that the proportion of threatened taxa in a community is similar across cells (see below). In contrast, there is little overlap between the hotspots for threatened taxon richness and rarity-weighted richness.
Area-selection

100 ig

Taxon richness hotspots

~ ig

10'

0 o .0

On the basis of complementarity, only 3.8% of grid cells (69 areas) are required to ensure that each primate taxon in Africa is represented at least once (Table 5). O f these, the majority have a high degree of flexibility with other cells (only 16 of these 69 cells are irreplaceable in achieving the goal of at least one record for every taxon). A comparison of the characteristics of the chosen cells with those comprising hotspots, a possible alternative set of areas which might be targeted for conservation, confirms the highly efficient performance of the complementarity approach in conservation areaselection (compare Tables 3 and 4). However, this method generates relatively fewer records per taxon (cf. Figs 3 and 4; compared with hotspots of taxon richness: z = -6.14, p < 0.001; rarity-weighted richness: z = -7.81, p<0.001; threatened taxon richness: z=-4.00, p < 0.001). In order to investigate how the degree of extinction risk of target taxa can influence area-selection efficiency, we reiterated the complementarity algorithm following the preselection removal of progressively more endangered taxa. Thus, after identifying the near-minimum set of areas for all taxa, we identified the near-minimum
Table 3. Descriptive statistics for hotspots identified using different evaluation criteria

il l li!ll,, ,al,J,,,, , , ,n,,,

15 30 45 60

I
75

90

Number of grid cells

100 m

Rarity-weighted hotspots

Ililrlll,,u,n
t

15

30

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60

75

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Threatened taxon richness hotspots

Evaluation criterion Taxon richness Rarity-weighted richness Threatened taxon richness

Primates of cells All taxa All taxa Threatened taxa All taxa

Number Number Records of cells of taxa per taxa a 92 (5) 92 (5) 40 (5) 40 (2) 92 (45) 163 (80) 46 (51) 89 (43) 13-4 5-1 5-9 6.1

I Ilil, ,i,u
i

II

15

30

45

60

75

90

Number of grid cells

Fig. 3. Comparison of the distribution of the number of grid

The figures in parentheses are the absolute values expressed as a percentage of the total number of cells and taxa present (Table 2). aTotal number of records across represented taxa, divided by the number of represented taxa.

cells per taxon across taxa in the network of hotspots selected on the basis of different evaluation measures: (a) taxon richness (records per taxa among those represented: median = 6), (b) rarity-weighted richness (median = 3), and (c) threatened taxon richness (median =4). The maximum number of grid cells in each case is 92, 92 and 40, respectively (Table 3).

P r i m a t e diversity a n d conservation

257

c r i t e r i o n for selection. These effects a r e m a r k e d , a l t h o u g h it is n o t p o s s i b l e to a t t a c h a p - v a l u e to their statistical significance since the subsets which are being c o m p a r e d are nested w i t h i n o n e a n o t h e r . A l t h o u g h the s e c o n d o f these results necessitates t h a t the entire netw o r k identified will be p r o t e c t e d , the f o r m e r suggests that, even o n a cell-by-cell basis within a m i n i m u m set, a r e a - s e l e c t i o n o n the basis o f t h r e a t e n e d t a x a will be m o r e effective in m a x i m i z i n g t a x o n richness t h a n areaselection o n a less d i s c r i m i n a t i n g basis. Table 4. Coincidence of hotspots using different diversity evaluation criteria Comparison between criteria Taxon vs rarity-weighted richness Taxon vs threatened taxon richness Rarity-weighted vs threatened taxon richness Subset of first x grid cells, where x is 5 20 All 0 (0) 4 (80) 0 (0) 2 (10) 9 (45) 3 (15) 22 (24) 25 (63) 12 (30)

T a x o n richness and conservation status This last finding suggests t h a t regions with severely e n d a n g e r e d p r i m a t e t a x a m i g h t score m o r e highly in t e r m s o f t a x o n richness. T o investigate this p a t t e r n at a higher resolution, d a t a were collected f r o m a range o f local sites (see M e t h o d s ) a n d g r o u p e d into a series o f f o u r nested categories, defined b y the c o n s e r v a t i o n status o f the m o s t t h r e a t e n e d t a x o n at t h a t site. A c o m p a r i s o n o f the m e a n n u m b e r o f t a x a p e r site in each o f these nested categories (Fig. 6) shows t h a t sites which c o n t a i n the m o s t seriously t h r e a t e n e d t a x a have the highest t a x o n richness, b u t as the severity o f t h r e a t for the m o s t t h r e a t e n e d t a x o n at t h a t site declines so t o o does the t a x o n richness o f t h a t site. This higher resolution d a t a b a s e differs f r o m t h a t used at the grid cell scale in b o t h the c o d i n g system for c o n s e r v a t i o n status and, in the case o f the c o n t i n e n t a l A f r i c a n d a t a s e t , the t a x o n o m i c level o f interest (see M e t h o d s ) . C o n s e q u e n t l y , the result t h a t m o r e highly t h r e a t e n e d t a x a tend to o c c u r in c o m m u n i t i e s o f g r e a t e r t a x o n richness a p p e a r s to be

The actual number of cells, expressed as the percentage of cells in that subset, is given in parentheses. Owing to problems of non-correspondence and non-independence, we follow Prendergast et al. (1993), Curnutt et al. (1994) and Kershaw et al. 0995) and do not use statistical tests in these comparisons. Table 5. Performance of complementarity selection method using different grid cell evaluation criteria Evaluation criterion Primates in cell Number Number Records of cells of taxa per taxa a 69 (4) 205 (100) 41 (5) 90 (100) 41 (2) 155 (76) 2-4 1.7 2-4

0 o "1o =-6

1.00

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Proportion

o "1o o 0.75 o ~3

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CE

CEV
a 0.02 i 0.03

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Taxon richness All taxa Threatened Threatened taxa taxon richness All taxa

Proportion of all grid cells (n=1825) (a}

The figures in parentheses are the absolute values expressed as a percentage of the total number of cells and taxa present (Table 2). aTotal number of records across represented taxa, divided by the number of represented taxa.

o o 1o 1-

14 12

CE

CEV

CEVS

10 D. 100 x m x 8 6

Complementary area method all taxa selection

~ lO m

0.01

0.02

0.03

0.04

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Proportion of all grid cells (n=1825}

Z 1 i 0 15 30 45 60 75 90

(b)

Number of grid cells

Fig. 4. The distribution of grid cells per taxon across taxa in the network of cells selected on the basis of complementarity (records per taxa among those represented: median = 1). The total number of cells in this near-minimum set is 69 (Table 5).

Fig. 5. Patterns of efficiency in the near-minimum set when the grid cells are selected on the basis of taxa of specific conservation status; critical (C), critical and endangered (CE), all threatened taxa (CEV) and all taxa (CEVS). Efficiency is shown in terms of (a) the total ratio of taxa per cell for the entire network and (b) the mean number of taxa per cell (standard error bars are shown). In both cases, the coverage of taxa includes both threatened and non-threatened taxa.

258
10

J. E. Hacker, G. Cowlishaw, P. H. Williams a series of both biological and methodological insights. These insights have potentially important consequences for area-selection in primate conservation. Some of these can be seen in the analysis of complementary areaselection efficiency. In terms of the principal values of taxon richness and rarity-weighted richness, there is surprisingly little correspondence between the two. However, this pattern is not unique; Prendergast et al. (1993) found that rare species are often outside hotspots of high species richness for plant and animal taxa in the UK, Fjelds~ (in press) found no correlation between the number of endemics and species richness in the avifauna of Andean montane forests, and Williams et al. (1996) report a low correlation between taxon richness and rarity-weighted richness for British birds (but see Thomas and Mallorie, 1985, for a contrary trend in patterns of butterfly richness and rarity in Morocco). Nevertheless, these previous studies were all restricted to relatively small land areas. Prendergast et al. (1993) suggest that their findings are

0 4-, @)

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,"~- 14

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Fig. 6. Patterns of taxon richness in a selection of sites across (a) Madagascar and (b) continental Africa. Sites are grouped on the basis of possession of a taxon of specific conservation status, ranked from 1 to 4 in increasing level of threat (see Methods; cf. Fig. 5). The mean number of all taxa per site and standard error are shown, with number of sites in each category listed in parentheses.

Taxon richness

(a)

- 0.6
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a~ 0.5
0.4

robust. These data were then used to investigate whether the proportion of threatened taxa at a site showed any general relationship to the number of taxa present. Plotting these data for Madagascar and continental Africa (Fig. 7) reveals a strong positive correlation in both cases (Spearman rank correlations: Madagascar rs = 0.40, p = 0-02; continental Africa rs = 0.83, p < 0.001).

-,

0.3

0.2
O '~ 0.1

o
D-

0.0
i
5

i
10

15

20

T a x o n richness

DISCUSSION These analyses illustrate how different facets of African primate diversity can show dissimilar patterns of spatial distribution. The comparisons of these patterns provide

(b) Fig. 7. Relationship between taxon richness and the proportion of taxa which are threatened at sites in (a) Madagascar and (b) continental Africa. Threatened taxa possess a threat code of > 1 (see Methods).

Primate diversity and conservation

259

scale-dependent and may be specific to fragmented landscapes, such that greater coincidence would be seen at larger scales. This argument is supported by largescale analyses of richness and rarity in both the terrestrial bird species of Australia (Curnutt et al., 1994; using a 1 grid cell scale) and the seed plant families of the world (Williams et aL, 1994; using a 10 grid cell scale). Yet the findings of this study, conducted at an identical scale to that of Curnutt et al. (1994), suggest that areas of high taxon richness are not always associated with a high rarity-weighted richness even at this scale. A full understanding of those processes which do and do not lead to a coincidence between these two facets of diversity clearly requires further research. Hotspots for threatened taxon richness similarly show little correspondence to those for rarity-weighted richness, despite the fact that rarity can be interpreted as an alternative measure of a taxon's extinction threat (review in Gaston, 1994; see also Bibby et al., 1992). There are several possible reasons why the two measures showed such little similarity in the present study; (1) only one measure of rarity is used (range size) while other measures may be more relevant (e.g. population size: see Gaston, 1994); (2) a more strongly non-linear system might be more accurate at reflecting the concept of rarity (e.g. the reciprocal of the square of range size); (3) many threatened taxa are not rare but are still at risk of extinction because they are rapidly declining in numbers (e.g. Mace, 1994); and (4) this measure of rarity is weighted by species richness and is therefore a rather complicated guide to where the rarest species are congregated. In the latter case, this emphasizes the problems of combinatorial scoring, which includes subjectivity in combination weighting and a lack of transparency (e.g. Margules, 1989; Turpie, 1995). Alternative measures, such as the number of species in a site which fall below a certain threshold in range size (i.e. following the pre-selection filtering of taxa with large distributions), would be more explicit. Nevertheless, the current method has the advantage that it makes no assumptions about the requisite threshold values, since all taxa contribute on a sliding scale. Whichever method is preferred, these points emphasize the caution which should be employed when equating rarity with conservation status. Perhaps the most important finding of this study is that hotspots for threatened taxa are largely coincident with those for taxon richness (Fig. 2, Table 4). The most parsimonious explanation of this pattern might be that it simply reflects the way in which we classify the viability of taxa; that in any given primate community a similar proportion of taxa (typically those which fall into the bottom end of the range in traits such as population density and geographic distribution) tend to be considered threatened. However, this does not appear to be the case, since the proportion of threatened taxa is greater in sites of higher taxon richness (Fig. 7) and there is a clear association between taxon richness and

the severity of threat to the endangered taxa present (Fig. 6). At the coarser grid cell scale, this latter relationship also emerges in the described patterns of efficiency of taxon representation in complementary areaselection (Fig. 5). One alternative explanation of these associations is that primates with smaller ranges might be more common in areas of higher taxon richness (rarity and taxon richness do share high scores in equatorial areas; Fig. 1) and also more likely to be classified as threatened (see Methods). Yet although range size and richness do show some similarity at the continental scale, this explanation is weakened by the fact that rarity-weighted richness hotspots show little coincidence with hotspots for either taxon richness or threatened taxon richness (Table 4). Two further explanations can be entertained. One possibility is that areas of high diversity might also be areas of particularly high habitat quality, and threatened primates which find it difficult to sustain viable populations elsewhere can do so in such areas. A more worrying interpretation is that areas of high primate diversity (primarily equatorial forest) tend to suffer the greatest menace from human activities and so also contain more threatened taxa, whereas areas of low diversity are at less risk and therefore contain fewer threatened taxa. It is notable, in this respect, that Balmford and Long (1994) have reported that tropical forest areas of high avian endemism are being lost at a higher rate than those of lower endemism. Further research is urgently required into these associations to examine the processes which might be responsible for such patterns, and to examine why a similar trend has recently been described for Neotropical birds (the proportion of threatened species increases with species richness at a coarse 611,000km 2 grid cell level: Gaston and Blackburn, 1996) but not for Afrotropical antelopes (sites of high taxon richness do not show a strong coincidence with sites containing a large number of threatened taxa: Kershaw et al., 1995). Each of these latter two explanations has quite different implications for current practice in African primate conservation. On the one hand, if taxon richness and the proportion of threatened taxa in an area are correlated solely as a result of particular qualities of the local habitat, then the integrity of that habitat must be successfully maintained. If these qualities are related to specific ecological processes in which there are no anthropogenic influences, then human activities in those areas (including community-based conservation projects) should be limited. Alternatively, if local human communities contribute constructively to these ecological processes by a particular form of resource utilisation, then this activity should be continued at an appropriate beneficial level as a management tool to maintain diversity. Scrutiny of the four sites with the highest primate diversity in our sample for continental Africa (Fig. 7) suggests that both of these approaches are required, since both Pleistocene forest refuges and

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J. E. Hacker, G. Cowlishaw, P. H. Williams

habitat heterogeneity through historical cultivation m a y contribute to high taxon richness depending on the site in question (e.g. Korup: Ministry of Plan and Regional Development, 1990; Tiwai: Oates et al., 1990, respectively). On the other hand, if taxon richness is spatially correlated with the proportion of threatened taxa because taxon-rich areas tend to occur where deforestation or hunting are most severe, then the primary goal of local conservation action should always be the control of these adverse anthropogenic forces. This might involve improved protection measures together with the active involvement of local communities. In conclusion, this paper examines the divergent consequences of using, and the inter- relationships between, different criteria in the evaluation and selection of sites for primate conservation. The findings presented include a newly-described association between taxon richness and endangerment. This pattern exists at both fine and coarse spatial scales and suggests that a focus of site protection on areas of high primate richness is also likely to benefit a disproportionately large number of threatened taxa, placing primate conservationists in a relatively fortuitous position. It is hoped that the information presented here might serve a useful role in future site evaluation and conservation planning for primates (see Oates, 1986, 1996; Mittermeier et al., 1992). Although the choice of sites will also be influenced by additional factors not incorporated into this analysis, such as land costs and population viability, the baseline patterns of taxon richness, rarity and conservation status described should remain a component of key importance in the conservation process.

ACKNOWLEDGEMENTS We are very grateful to John Oates for providing us with a preview copy of the new Action Plan for African Primates and for making valuable comments on an earlier draft of this paper. Thanks also to T o m Butynski, Brian Davis, and three anonymous referees for their helpful comments; to Andy Purvis for his help and advice in the early stages of the project; and to the trustees of the Natural History Museum and the staff of the Biogeography and Conservation Department for the use of facilities, including computer access made available by the Darwin Initiative for the Survival of Species. J.H. was supported by an N E R C grant; G.C. was funded by an E S R C Research Fellowship.

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Purvis, A. (1995) A composite estimate of primate phylogeny. Philosophical Transactions of the Royal Society of London B 348, 405-421. Stevenson, M., Baker, A. and Foose, T. J. (1992) Conservation Assessment and Management Plan for Primates. IUCN/SSC Captive Breeding Specialist Group and IUCN/SSC Primate Specialist Group. Struhsaker, T. T. (1967) Ecology of vervet monkeys (Cercopithecus aethiops) in the Masai-Amboseli Game Reserve, Kenya. Ecology 48, 891-904. Tattersall, I. (1982) The Primates of Madagascar. Columbia University Press, Columbia. Thomas, C. D. and Mallorie, H. C. (1985) Rarity, species richness and conservation: butterflies of the Atlas mountains in Morocco. Biological Conservation 33, 95-117. Turpie, J. K. (1995) Prioritizing South African estuaries for conservation: a practical example using waterbirds. Biological Conservation 74, 175-185. Waser, P. M. (1987) Interactions among primate species. In Primate Societies, eds B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W., Wrangham and T. T. Struhsaker, pp. 210-226. Chicago University Press, Chicago. Williams, P. H. (1994) WORLDMAP: priority areas for biodiversity. Version 3.08/3.18. Privately distributed, London. Williams, P. H. (in press) Key sites for conservation: areaselection methods for biodiversity. In Conservation in a Changing World." Integrating Processes into Priorities for Action, eds. G. M. Mace, A. Balmford, and J. Ginsberg. Zoological Society of London, London. Williams, P. H. and Humphries, C. J. (1994) Biodiversity, taxonomic relatedness and endemism in conservation. In Systematics and Conservation Evaluation, eds. P. L. Forey, C. J. Humphries and R. I. Vane-Wright, pp. 269-287. Clarendon Press, Oxford. Williams, P. H. and Humphries, C. J. (1996) Comparing character diversity among biotas. In Biodiversity: A Biology of Numbers and Difference, ed. K. J. Gaston, pp. 54-76. Blackwell, Oxford. Williams, P. H., Humphries, C. J. and Gaston, K. J. (1994) Centres of seed-plant diversity: the family way. Proceedings of the Royal Society of London B 256, 67-70. Williams, P., Gibbons, D., Margules, C., Rebelo, A., Humphries, C. and Pressey, R. (1996) A comparison of richness hotspots, rarity hotspots and complementary areas for conserving diversity of British birds. Conservation Biology 10, 155-174. Wolfheim, J. (1983) Primates of the World." Distribution, Abundance and Conservation. University of Washington Press, Seattle, WA.
APPENDIX 1 Source references for the geographic distributions of African species and sub species

Taxon Lemuriformes Lorisiformes Colobinae Cercopithecines Pongidae

Reference 1, 2, 3, 4 5 6, 7, 8, 9, 10, 11, 12 7, 13, 14, 15, 16 10, 15, 17

1. Harcourt and Thornback, 1990; 2. Mittermeier et al., 1992; 3. Mittermeier et al., 1994; 4. Tattersall, 1982; 5. Nash et al., 1989; 6. Colyn, 1987; 7. Dandelot, 1971; 8. Oates et al., 1994; 9. Kingdon, 1971; 10. Lee et al. 1988; 11. Napier and Napier, 1970; 12. Oates, 1986; 13. Groves, 1978; 14. Homewood and Rodgers, 1981; 15. Wolfheim, 1983; 16. Lernould, 1988; 17. Harcourt and Fossey, 1981.

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APPENDIX 2

Sites in continental Africa Site Cameroon Ethiopia Gabon Kenya Country Korup Bole Makoukou Amboseli Diana Laikipia Tana R. Tsaobis Yankari Assirik Tiwai Gombe Mahale Ugalla Kibale Lomako Kasanka Source of data Ministry of plan and regional development (1990) Dunbar and Dunbar (1974) Gautier-Hion (1978) Struhsaker (1967) Moreno-Black and Maples (1977) Barton (1989) Decker (1994) G. Cowlishaw (unpublished) J. Rudge (pers. comm.) Byrne (1982) Oates et aL (1990) Goodall (1986) Nishida (1990) Itani (1979) Waser (1987) Badrian and Malenky (1984) Farmer (1992)

Namibia Nigeria Senegal Sierra Leone Tanzania Uganda Zaire Zambia