Biological Conservation 93 (2000) 163±175
www.elsevier.com/locate/biocon
Coincidence and mismatch of biodiversity hotspots:
a global survey for the order, primates
A.H. Harcourt
Department of Anthropology, University of California, One Shields Ave., Davis, CA 95616, USA
Received 16 June 1999; accepted 14 September 1999
Abstract
A global survey of a well-studied order of tropical mammals, primates, is used to explore the use of diversity hotspots in conservation. The results at this shallow taxonomic level match those for most cross-phylum analyses. Overlap of hotspots for species,
genera, trait-complexes, families, and threatened species varies with the continent, and the comparison. Overlap is best in Africa
and Madagascar, and poorest in Asia, but reasons for the di€erences need exploring. A complete mismatch of taxonomic and
threatened species hotspots in South America, resulting from the mismatch of the hotspots of diversity and human destruction,
suggests that conservation biologist's hotspot approach could bene®t from adding hotspots of human threat to the analysis of
diversity hotspots. Conservationists' use of hotspot analysis seems to have been largely empirical. If analysis of single orders can
contribute to conservation, application of biogeographic theory to our knowledge of the distribution of the order, primates, is the
next step. # 2000 Elsevier Science Ltd. All rights reserved.
Keywords: Biodiversity; Biogeography; Hotspot; Primates; Threatened species
1. Introduction
`Hotspots', regional concentrations of species, have
been of interest to biogeographers since the early 1800s
(Browne, 1983). They are also of interest to conservationists, because of their potential to provide easy identi®cation of sites for preservation of biodiversity
(Terborgh and Winter, 1983; Myers, 1988; Prendergast
et al., 1993; Pressey et al., 1993; Scott et al., 1993;
Dobson et al., 1997; Mittermeier et al., 1998; Reid,
1998). However, while some areas of high diversity
overlap, often they do not. Thus in the USA, the southeast is an overall hotspot, but endangered plants are
largely in the west (Dobson et al., 1997; Ricketts et al.,
1999). In Transvaal, South Africa, little overlap exists of
hotspots or coldspots among plant and animal phyla, or
even among rare representatives of those phyla (van
Jaarsveld et al., 1998). In Britain, the maximum overlap
between any two taxa is only 34% (butter¯ies and dragon¯ies), and two charismatic taxa, birds and butter¯y,
overlap by only 12% (Prendergast et al., 1993). Even
E-mail address: [email protected] (A.H. Harcourt).
among the relatively similar Ugandan forests, only three
of 10 comparisons across ®ve phyla were signi®cantly
congruent once area of forest was accounted for
(Howard et al., 1998). Thus from identifying sites that
might contain hotspots for several taxa, the hotspot
approach has moved more strongly to identifying complementary sites, namely the range of sites that represent as much as possible of the range of taxa (Pressey et
al., 1993; Williams et al., 1997). However, a potential
complication for generalisation across continents is the
®nding that the extent of overlap (or lack of it) that
exists between particular taxa varies with continent
(Pearson and Carroll, 1998).
As the examples given above indicate, coincidence
and mismatch of hotspots tends to be sought among
classes or phyla. The greater the number of phyla with
overlapping hotspots, the less area needs conserving to
protect biodiversity, and thus the more likely biodiversity is to be protected. In addition, the practical hope
was that hotspots for easily seen and identi®ed charismatic taxa would match those for less obvious taxa. Far
less frequently are the regional comparisons done at
shallower taxonomic levels, except at the local scale; the
reason is that we do not expect concordance at shallow
0006-3207/00/$ - see front matter # 2000 Elsevier Science Ltd. All rights reserved.
PII: S0006-3207(99)00145-7
164
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
taxonomic levels (Reid, 1998). Hacker et al. (1998)
recently provided one of the few applications of the
hotspot approach within an order, the primates. They
showed that hotspots for threatened primate subspecies
in Africa and Madagascar together were hotspots for all
primate subspecies, but that little overlap existed
between hotspots of endemics (rare subspecies) and
either threatened subspecies or all subspecies, because
endemic hotspots were scattered.
By comparison to many other taxa, the order primates consists of mostly large, easily observable species,
even the nocturnal ones. They are thus well-studied
(Rowe, 1996). Consequently, we probably have as good
information on the global distribution of primate taxa
as we do for any other tropical order. Such information
is particularly important, because tropical countries
have generally been less well surveyed and currently
have less funding for surveys than do temperate countries (Myers, 1984; Harcourt, 1995; Howard et al.,
1998). Primates could thus be good indicator species for
countries with less opportunity for biological surveys
than others. Understanding of the distribution of their
diversity could therefore be especially useful. In order to
further explore the generality of the hotspot approach, I
here provide the ®rst, detailed global assessment of
coincidence and mismatch of hotspots for the order,
primates, at several taxonomic levels of analysis, treating each continent separately.
Hotspots for di€erent taxonomic levels are compared,
as are hotspots for di€erent trait-complexes, including
threatened species. The main questions concern how
well the generic hotspots represent the speci®c ones;
how well either of these represent the various trait
complexes; and ®nally, how well the threatened species'
hotspots overlap the various taxonomic hotspots. In
other words, can we use deeper taxa as indicators? Does
the taxon's hotspots of overall diversity represent the
variety within the taxon?; and will conservation of
threatened taxa conserve the full variety of the taxon?
2. Methods
2.1. Sources of data
The basis of this analysis are the distribution maps
[`coverages' in geographic information systems (GIS)
terminology] of individual species [N=about 60 species
per continent, except Madagascar with 30 (see Figs.
1±4)]. These were digitised from maps in Wolfheim
(1983), with subsequent correction and addition from,
in particular, Niemitz (1984), Hershkovitz (1987a;
1987b; 1990), Lernould (1988), Nash, Bearder and
Olson (1989), Harcourt and Thornhill (1990), Corbet
and Hill (1992), Groves (1993), Rylands, Coimbra-Filho
and Mittermeier (1993), Ford (1994), Mittermeier et al.
(1994), Oates, Davies and Delson (1994), and Kinzey
(1997). The `Regions' feature class of ARC/INFO
(ESRI Inc., 1998a) was then used to draw `polygons';
that delineated regions with di€ering numbers of species. The result is areas of concentration of those di€ering numbers of species.
Taxonomic nomenclature and listing is mostly from
Corbet and Hill (1991) and Groves (1993). Where the
sources di€ered, the one with the fewer species was
chosen, although Papio remains as ®ve species. Callicebus is treated as three species (as in Wolfheim 1983),
because the two main authorities di€er (Hershkovitz,
1990; Groves, 1993).
Threatened taxa are those listed in the 1996 IUCN
Red List of Threatened Animals (IUCN, 1996) as Vulnerable, Endangered, and Critically Endangered. While
the categorisation of status in the Red List is challenged
for some taxa (Mrosovsky, 1997), and con¯icts with
published, substantiated analyses for others (Harcourt,
1996), nevertheless, it is the most complete source
available, and heavily used in national conservation
policy. Not all taxa in the IUCN List were included in
the analysis here. Missing species are those that do not
appear in one or other of the taxonomic sources. The
missing species are largely recent splits re¯ecting minor
morphological variations at single geographic sites,
some of which are taxonomically contested. The exclusion of the IUCN species in no instance a€ects the
IUCN classi®cation of their sister species, because the
geographic ranges of the excluded species are very small
by comparison to their sister species' ranges. Brachyteles
is the one exception: the split species each have about
the same size of geographic range. However, the original single species is as threatened as either of IUCN's
two species. The IUCN species not included in this
analysis are, in IUCN order of listing, Aotus brumbacki,
A. lemurinus, Brachyteles hypoxanthus, Callicebus
dubius, Cebus kaapori, C. xanthosternos, Cercopithecus
preussi, C. sclateri, C. solatus, Hapalemur aureus,
Macaca brunnescens, M. pagensis, Microcebus myoxinus, Saimiri oerstedii (possibly a human introduction),
S. vanzolinii, Trachypithecus delacouri, and T. poliocephalus.
The maps are displayed in ArcView's (3.1) Geographical projection (ESRI Inc., 1998b).
2.2. De®nitions of hotspots
No one de®nition or mode of measurement of a hotspot seems to be preferred. Here, I use overlap of the
distribution maps of individual taxa (not the common
counts of taxa in quadrats). Where the sample size is
large enough, four levels of concentration of taxa are
shown. The four levels are as near as possible in quartiles of the number of taxa with overlapping distributions, starting from the lowest quartile, but the exact
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
proportion of taxa in the top quartile varies depending
on the number of taxa in the sample. A `hotspot' is
de®ned here as the top quartile (or the top half for
threatened species).
165
2.3. Analysis
Where hotspot overlap is concerned, two main measures are given. The proportion of a hotspot that is
Fig. 1. Map of concentrations of primate taxa separated into quartiles of numbers of species. Africa (omitting northern Africa and the Barbary
macaque, Macaca sylvanus).
166
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
overlapped by another hotspot (e.g., the proportion of
the species' hotspot that is overlapped by the generic
hotspot), and the proportion of taxa that are overlapped by a hotspot (e.g., the proportion of species
overlapped by the generic hotspot). The former measure
is, in e€ect, the probability of a point site in a hotspot
hitting the other hotspot. By de®nition, 25% of the taxa
of the overlapped taxonomic category will be at that
Fig. 2. Map of concentrations of primate taxa separated into quartiles of numbers of species. Asia (omitting Japan and the Japanese macaque,
Macaca fuscata). The omissions of the two Macaca are merely for reasons of space on the page. The species were included in analysis, and neither
omission in presentation a€ects the resulting hotspots.
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
point site. In contrast, often more than 25% of the species of the overlapped category will be overlain, because
the identity of the species di€er from point to point
within a hotspot, even though there will be the same
proportion of the total across the hotspot. The usual use
of hotspots is as guidance for conservation e€ort.
167
Almost all the hotspots are orders of magnitude larger
than the average current protected area. For instance,
Africa's mean current reserve size is 2000 km2 (Miller et
al., 1995), whereas its species' and threatened species'
hotspots are each over half a million square kilometres
in total. Thus, a point site is going to be closer in size to
Fig. 3. Map of concentrations of primate taxa separated into quartiles of numbers of species. Madagascar.
168
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
the average reserve than is the size of a whole hotspot.
The number of species within a reserve is thus going to
be somewhere between the number at a point site, and
the number overlapped by a whole hotspot, and probably far closer to the former.
3. Results
Throughout, I treat the continents in alphabetical
order. Hotspots for primate taxa in the four continents
are obvious, whatever the level of analysis (Figs. 1±5).
Fig. 4. Map of concentrations of primate taxa separated into quartiles of numbers of species. South America.
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
As many others have shown, primate hotspots cluster at
the equator, except in Madagascar. They also cluster in
forests, the habitat of most primate species (Wallace,
1876, Ch. 17; Terborgh and Schaik, 1987), and in areas
of high rainfall, except in Asia (Reed and Fleagle, 1995).
169
Africa's hotspots contain the highest number of species,
despite Asia and South America having very similar
numbers of species in total. Nevertheless, conserving
just Africa's hotspots will not conserve a representative
sample of all primates. As Wallace (1876, Vol.2, p.179)
Fig. 5. Maps of concentrations of threatened primate taxa, in two categories of numbers of species. (a) Africa; (b) Asia (omitting Japan and the
Japanese macaque, Macaca fuscata); (c) Madagascar; (d) South America.
170
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
that more variety is probably contained in a generic
hotspot than in a speci®c one, given that two genera are
on average more di€erent than are any two species
within those genera. However, the relative diversity
within di€erent taxonomic levels varies according to the
identity of the taxa compared (Crozier, 1997).
The relative size and number of the generic and speci®c hotspots varies across continents, but overlap of
the speci®c hotspots by the generic hotspots is 75% or
more for all continents, except Asia (Figs. 1±4; Table 2).
Overlap of the speci®c by the generic hotspots is highest
in Africa, where the generic and speci®c hotspots' overlap with the subspeci®c hotspots is also high [compare
Fig. 1a,b with Hacker et al.'s (1998) Fig 2a]. In Asia, a
concentration of e€ort on generic hotspots would lead
to conservation in only Borneo, so missing the mainland
speci®c hotspots (Fig. 2 a,b). Generic hotspots cover
about 50% of the number of species for all continents,
except again Asia, whereas the speci®c hotspots cover
75% or more of genera on all continents (Table 3).
The generic hotspot covers over 50% of the area of
the threatened hotspots in Africa and Madagascar,
compared to none of them in Asia or South America
(Table 2). However, for none of the continents does the
generic hotspot cover substantially more threatened
species than does the speci®c hotspot, and indeed in
Asia it covers a third of the number of threatened species (Table 3). For primates, therefore, genera are not
useful indicator taxa in a hotspot application for conservation.
wrote, `The most striking fact presented by this order . . .
is the strict limitation of well-marked families to de®nite
areas'. Baboons, for example, occur in only Africa, gibbons in only Asia, lemurs in only Madagascar, and
marmosets in only South America. Because the taxa
di€er across the continents, so too do the traits that they
represent (Terborgh and Schaik, 1987; Maurer et al.,
1992; Kappeler and Heymann, 1996; Williams and
Humphries, 1996).
In all the continents, a relatively small proportion of
the total area covered by primates (<10%) contains a
relatively large proportion of the total number of taxa
in that continent (Table 1). Thus the speci®c hotspots
contain 40±62% of species (Table 1), and the generic
hotspots, 67±93% of genera.
However, the Lemuridae in Madagascar illustrate the
di€erence that de®nitions can make to the size of a
hotspots, and therefore in inferences from hotspots'
analysis. The Lemuridae's top quartile hotspot could
reasonably be de®ned as either the 5-species zone (as
here), or as the 4±5 species zone. The 5-species hotspot
covers 275 km2; the 4±5 species zone covers 28 350 km2,
a 100-fold di€erence (Fig. 3g).
3.1. Deeper taxa as indicator taxa
Can deeper taxa (genera rather than species, families
rather than genera) be used as indicator taxa? In this
paper I ask whether generic hotspots include most species. Deeper taxa have sometimes been found to be
adequate indicators (Williams and Gaston, 1994), and
sometimes not so found (van Jaarsveld et al., 1998).
However, the studies di€ered not only in the region
studied, but also in their de®nition of what a hotspot
was (as is often the case in the hotspot literature).
Another reason to concentrate on generic hotspots is
3.2. Hotspots for trait-complexes
A number of authors have raised the issue of the
importance of diversity of form, as well as of number of
taxa (Janzen, 1988; Jablonski, 1995; Dingle et al., 1997;
Table 1
Percent total geographic area and percent species of primates per continent covered by ROW hotspots
Africa
Asia
Madagascar
South America
% Area
% Species
% Area
% Species
% Area
% Species
% Area
% Species
Species
Genera
Nocturnal
Diurnal
For. Cerc.a
Colobinae
Apes
Cheirogaleidae
Indriidae
Lemuridae
Callitrichidae
Cebinae
Aotinae, etcb
1.6
3.2
0.4
3.4
1.2
2.5
±
±
±
±
±
±
±
62
66
55
71
67
55
±
±
±
±
±
±
±
1.7
1.2
8.2
0.5
±
±
0.3
±
±
±
±
±
±
40
22
50
31
±
±
17
±
±
±
±
±
±
7.5
5.6
0.0
4.3
±
±
±
5.2
5.9
0.1
±
±
±
53
50
33
47
±
±
±
53
43
37
±
±
±
4.9
10.1
±
±
±
±
±
±
±
±
0.1
1.6
6.6
41
47
±
±
±
±
±
±
±
±
35
24
47
Threatened
2.0
60
5.3
36
9.6
70
1.7
18
a
b
For. Cerc., Forest Cercopithecine.
Aotinae etc., Aotinae, Pithecinae, Atelinae.
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
Hacker et al., 1998; Jernvall and Wright, 1998; see also
Shepherd, 1998). Thus Williams and Humphries (1996)
showed for Bombus bees, that while the hotspot for
number of species was in South America, the hotspot
for number of individual traits was in central and eastern Eurasia, and the hotspot for number of combinations of characters was in eastern Eurasia. For African
primates, Hacker et al. (1998) showed a good match of
taxonomic and character richness across Africa. Madagascar, however, has only one major taxon, the Lemuroidea, and their character richness index was derived
from taxonomic variety, so causing a mismatch between
subspecies richness and character richness (Hacker et
al., 1998). The trait-complex examined in this paper, for
purposes of illustration, is activity period. This traitcomplex correlates strongly with body mass and sociality: nocturnal taxa are usually smaller and more solitary than are diurnal species (Clutton-Brock and
Harvey, 1977). The trait-complex is also a taxonomic
grouping in Africa and Asia, because the the nocturnal
taxa tend to be prosimians. In Madagascar, all the primates are prosimians, and there the two activity periods
(and their associated traits) are not distributed randomly among the taxa. South America has only one
nocturnal taxon, Aotus, and is thus excluded.
The overlap of speci®c and generic hotspots with
trait-complex hotspots, and the overlap among trait-
171
complex hotspots varies with continent (Figs. 1±3;
Tables 2 and 3). The match was most consistent in
Africa, and relatively high, as was the match between
subspeci®c and character richness in Hacker et al.'s
(1998) analysis. However, the western hotspots of nocturnal and diurnal primates miss one another (Fig. 1).
In Asia, large contrasts in the size of the hotspots, and
the con®nement of the generic hotspots to Borneo, produce imbalance in overlap of both area and number of
taxa. In Madagascar, both speci®c and generic hotspots
overlap well the diurnal hotspots, but there is complete
mismatch of the nocturnal and diurnal hotspots themselves. However, the species and generic hotspots in
Madagascar overlay a large (>50%) proportion of
both the nocturnal and diurnal species (Table 3).
3.3. Hotspots for families
The more restricted the taxonomic grouping, the
less likely is it that hotspots will coincide, for both
historical and environmental biogeographic reasons
(Williams and Humphries, 1996; Reid, 1998). Nevertheless, within one mammalian order that is largely
con®ned to one habitat, tropical forest, considerable
overlap of family hotspots by speci®c or generic hotspots
might be expected. Families can also be considered as
trait-complexes.
Table 2
Summary of overlap of area of hotspotsa
Africa
Hotspots
Hotspots
Species
Genera
Threatened
Species
±
93
51
Asia
Hotspots
Hotspots
For. Cerc.b
23.5
19.5
2
Colobine
5
3
14
Genera
45.5
±
45.5
Nocturnal
57
73
28
Diurnal
45
46
23
Species
Genera
±
31
61
45
±
0
Diurnal±Mon- Apes
keys
99
0
20
0
76
0
Threatened
Species
Genera
Threatened
Nocturnal±
Prosim
19.5
11.5
43
Madagascar
Hotspots
Hotspots
Species
Genera
Threatened
Species
±
75
100
Genera
100
±
100
Nocturnal
0
15
100
Diurnal
99
87.5
100
Cheirogaleidae
0
0
2
Indriidae
94
95
99
South America
Hotspots
Hotspots
Species
Genera
Threatened
Species
±
100
0
Genera
48
±
0
Callitrichidae
100
100
0
Cebinae
0
11
0
Aotinae, etc.c
52
80
0
Threatened
0
0
±
a
Threatened
40
73
±
20
0
±
Lemuridae
100
0
100
Threatened
77
58
±
Entries, percent of COLUMN hotspot overlapped by ROW hotspot, or percent chance of point protected area in row hotspot overlapping
column hotspot.
b
For. Cerc., Forest Cercopithecine.
c
Aotinae etc., Aotinae, Pithecinae, Atelinae.
172
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
Overlap of the speci®c and generic hotspots with the
familial hotspots is variable within as well as between
continents. While no one continent stands out as
obviously more or less consistent than any other, especially with regard to area of of overlap, a consistently
large proportion of Madagascar's species from separate
families are overlapped by both the speci®c and generic
hotspots (Figs. 1±4; Tables 2 and 3). In addition, the
familial hotspots themselves rarely show substantial
overlap (Figs. 1±4). In Africa, the far, western colobine
hotspot [foregut fermentation with lysozyme as the
trait-complex (Messier and Stewart, 1997)] is an obvious
outlier, but nevertheless the speci®c and generic hotspots overlap the ranges of over 50% of colobine species
(Fig. 1; Tables 2 and 3). In Asia, the scattered speci®c
hotspots overlap a greater number of familial hotspots
regions than do the more con®ned generic hotspots
(Fig. 2; Table 2). Although the ape hotspot is an
obvious outlier, the speci®c hotspot overlaps the ranges
of 50% of the ape species (Table 3). Perhaps the most
noticeable phenomenon in Madagascar is the lack of
any overlap by the speci®c or generic hotspots of the
cheirogaleid hotspot (Fig. 3; Table 2), yet the 100%
overlap with number of cheirogaleid species (Table 3).
In South America, the familial hotspots are o€set
enough, and the sizes of the speci®c ranges di€erent
enough, to produce confusing di€erences between hotspot overlap, and proportion of species overlapped by
the hotspots (Table 2 vs 3).
3.4. Threatened species hotspots
Threatened taxa, and ecosystems are a non-random
selection of all taxa and ecosystems (Jernvall and
Wright, 1998). Overlap of either speci®c or generic hotspots with the hotspots for threatened species is therefore not necessarily expected, and in some cases not
found (Prendergast et al., 1993). At the same time, a
concentration of species with small geographic ranges
could form a speci®c hotspot, which is then necessarily a
threatened species hotspot because species with small
geographic ranges are threatened (Brown, 1995, p. 215).
Also, primates are concentrated in tropical forest, and
tropical forest is under threat (Hannah et al., 1994;
Table 3
Summary of taxonomic overlap of hotspotsa,b
Africa
Taxa
Hotspots
Species
Genera
Threatened
Species
n=58
62
65.5
59
Asia
Taxa
Hotspots
Species
Genera
Threatened
Species
n=58
40
22
36
Madagascar
Taxa
Hotspots
Species
Genera
Threatened
Species
n=30
53
50
70
South America
Taxa
Hotspots
Species
n=66
41
47
18
Species
Genera
Threatened
a
Genera
21
81
86
86
Nocturnal
15
80
80
60
Diurnal
42
62
64
62
For. Cerc.c
17
71
76.5
65
Colobine
7
57
57
71
Genera
12
75
67
58
Nocturnal±Prosim
7
43
29
29
Diurnal±Monkey
39
36
20
33
Apes
12
50
25
50
Threatened
31
29
10
±
Genera
14
93
93
93
Nocturnal
17
76
76
88
Diurnal
13
61
54
77
Cheirogaleidae
7
100
100
100
Indriidae
14
64
64
79
Genera
16
75
81
37
Callitrichidae
29
31
34
28
Cebinae
5
60
80
20
Aotinae, etc.d
32
47
53
9
Threatened
20
20
20
±
Threatened
10
50
50
±
Lemuridae
9
56
44
78
Threatened
17
69
53
±
Entries, percent of COLUMN taxa overlapped by ROW hotspot.
Note for all continents except Madagascar, if overlap was less than 1000 km2 for any species, the species was omitted, because most species'
ranges were far larger, and thus preserving that 1000 km2 would make little di€erence to persistence. In Madagascar, many species had extremely
small ranges.
c
For. Cerc., Forest Cercopithecine.
d
Aotinae etc., Aotinae, Pithecinae, Atelinae.
b
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
Olson and Dinerstein, 1998). Thus, for African and
Malagasay primates combined, Hacker et al.'s (1998)
results indicate good overlap between threatened subspeci®c hotspots and total subspeci®c hotspots. Given
the importance that we need to attach to threatened
taxa, overlap of hotspots of overall diversity with
threatened hotspots needs to be good if it is to be useful.
In this global analysis, the overlap in either direction
between speci®c or generic hotspots and threatened
species hotspots is better in Africa, and especially
Madagascar, than it is in Asia or South America (Figs.
1±4 vs 5; Tables 1±3). In Africa, about 50% overlap of
hotspot areas occurred (Figs. 1 and 5a; Table 2), with a
slightly higher percentage for proportion of species and
genera overlain by the threatened hotspots (Table 3).
Hacker et al. (1998) found substantial overlap in Africa
between the threatened and total subspeci®c hotspots,
although their analysis of subspecies produced an east
African threatened hotspot, whereas this analysis has
only central and west African threatened species hotspots (Fig. 5a). In Asia, the speci®c, and especially generic hotspots miss the northern hotspot of threatened
mainland species (Figs. 2 and 5b), but despite the relatively high overlap of speci®c by threatened hotspots
(Figs. 2 and 5b; Table 2), only the proportion of genera
overlapped by the threatened hotspot exceeds 50%
(Table 3). In Madagascar, as said, overlap in both
directions of both area and number of taxa is high (Fig.
3; Tables 2 and 3). In South America, by contrast, a
complete mismatch of hotspots occurs: the taxonomic
hotspots (speci®c to familial) are in the west, but the
threatened hotspots are in the south-eastern forests
(Figs. 4 and 5d; Table 2). Correspondingly, the proportion of threatened species overlain by species or generic
hotspots, or the proportion of species or genera overlain
by the threatened hotspots is very low (Table 3).
With respect to overlap of subtaxonomic hotspots
and species by the threatened hotspots, the overlap of
area of subtaxonomic hotspots, and especially of the
overlap with number of species of those subtaxa, is also
consistently better in Africa and Madagascar than in
Asia or South America (Tables 2 and 3).
4. Discussion
The nature of overlap of hotspots varies considerably
among the continents. My speci®c to familial level analysis closely matches Hacker et al.'s (1998) subspeci®c
analysis in indicating substantial overlap of the various
hotspots in Africa and Madagascar. However, these
continents are not models for the global distribution of
primates. Asia especially, but also South America, have
disjunct distributions of primates. Thus a hotspot
approach to conservation of primates will in general
work better in Africa and Madagascar than in Asia or
173
South America. That is, use of hotspots to position
protected areas will overlap more trait-complexes, more
taxa, and more threatened species in Africa and Madagascar than in Asia or South America.
The most obvious geographic contrast between Asia
and the other three continents is that Asia is a heavily
divided landmass, which might correlate with its heavily
divided distribution of primates (e.g., Brandon-Jones,
1996). South America shows the severest mismatch of
taxonomic hotspots with hotspots for threatened species, and vice versa. Manne et al. (1999) found for South
America the same mismatch between diversity hotspot
and threatened species hotspot for passerine birds, and
for the same reason: human disturbance is intense in the
south-eastern, Brazilian, Atlantic coast forest, but not
yet in the west (Hannah et al., 1994; Olson and Dinerstein, 1998).
Conservation needs shortcuts because time and
money are so lacking (Mittermeier et al., 1998). But
precisely because of the constraints, shortcuts must be
backed by strongly substantiated analysis (Leader-Williams and Albon, 1988). The hotspot analysis reported
here for one order of mammals, primates, epitomises
most, maybe all, hotspot analyses. De®nitions of hotspots massively a€ect their size and site, and hence
degree of overlap. While some considerable overlap of
hotspots across di€erent taxonomic (or other) categories exists, there is appreciable mismatch. And much
of the mismatch is unexplained, including obvious differences between continents in degree and nature of
overlap and mismatch. However, the alternative to
regional analyses, a site by site approach, depends on
immense amounts of data (Caughley, 1994; Oates,
1994). While we have the distributional data for primates, which is precisely the reason for their use here to
examine the hotspot approach, we do not for many
other taxa, especially tropical taxa (Harcourt, 1995;
Howard et al., 1998). Although none of the mismatches
identi®ed by this study mean that the hotspot approach
is useless, the analysis con®rms how careful its application needs to be, especially if it is to be applied globally
(Pressey et al., 1993; Pearson and Carroll, 1998; Reid,
1998; Ricketts et al., 1999).
Hotspot analysis, like much biological conservation,
concentrates on threatened wildlife more than the
threats that make the analysis necessary in the ®rst
place. The South American mismatch between hotspots
of diversity and hotspots of threatened species emphasises the necessity of bringing together our knowledge of
biodiversity with our knowledge and understanding of
the intensity and nature of threats to that biodiversity.
The conservation biologist's hotspot approach could
surely bene®t from more analyses that add hotspots of
human threat to the analysis of diversity hotspots in
order to, for example, more exactly distinguish safe,
diverse sites (where conservation will be cheap) from
174
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
highly threatened, diverse sites (where conservation is
expensive but vital). For instance, Dobson et al.'s (1997)
hotspot analysis indicates that in the USA, the latter
situation obtains, because hotspots of overall density of
endangered species overlap signi®cantly with hotspots
of agricultural output.
Caughley (1994) has suggested that much conservation biology su€ers because ecology, unlike population
biology, has so few general theories on which conservation management can be based. Consequently, he suggests, conservation often proceeds on an inecient case
by case basis. These results from a detailed analysis of
one taxon that shows such unexplained variability
across continents and taxa in overlap of hotspots are a
good illustration of Caughley's point. We could not a
priori predict what hotspots would have overlapped on
what continents by how much. Thus we proceed only
empirically. Biogeography is the obvious theoretical
discipline to bring to hotspot analysis if we want general
predictability. While the original Pleistocene refugium
hypothesis (Ha€er, 1969) promised a general theory
behind the hotspot approach, forest refugia are proving
dicult to demonstrate (e.g. Beven et al., 1984; Oates,
1988; Colyn et al., 1991; Colinvaux et al., 1996; Jolly et
al., 1997). However, various other areas of biogeography seem directly applicable, such as refugium theory in general, vicariance biogeography, and the
biogeography of abundance (e.g. Vermeij, 1978; Brundin, 1988; Lynch, 1988; Hengeveld, 1990; Gaston, 1994;
Brown, 1995; Rosenzweig, 1995). If analysis of single
orders has anything to contribute to conservation, the
next step is to intensify application of these areas of
biogeography to explaining the distributions of the
members of the order, primates.
Acknowledgements
The author wishes to thank Mark Byars and especially Sean Parks for producing the hotspot maps, and
Guy Cowlishaw, John Oates, Sean Parks, Walter Reid,
Kelly Stewart and the journal's referees for comments
that considerably improved the paper.
References
Beven, S., Conner, E.F., Beven, K., 1984. Avian biogeography in the
Amazon basin and the biological model of diversi®cation. J. Biogeog 11, 383±399.
Brandon-Jones, D., 1996. The Asian Colobinae (Mammalia: Cercopithecidae) as indicators of Quaternary climatic change. Biol. J.
Linn. Soc 59, 327±350.
Brown, J.H., 1995. Macroecology. University of Chicago Press, Chicago.
Browne, J., 1983. The Secular Ark. Studies in the History of Biogeography. Yale University Press, New Haven, Connecticut.
Brundin, L.Z., 1988. Phylogenetic biogeography. In: Myers, A.A.,
Giller, P.S. (Eds.), Analytical Biogeography. Chapman and Hall,
London, pp. 343±369.
Caughley, G., 1994. Directions in conservation biology. J. Anim. Ecol
63, 215±244.
Clutton-Brock, T.H., Harvey, P.H., 1977. Primate ecology and social
organization. J. Zool., Lond 183, 1±39.
Colinvaux, P.A., 1996. de Oliveira, P. E., Moreno, J.E., Miller, M.C.
and Bush, M.B. A long pollen record from lowland Amazonia: forest and cooling in glacial times. Science 274, 85±88.
Colyn, M., Gautier-Hion, A., Verheyen, W., 1991. A re-appraisal of
palaeoenvironmental history in Central Africa: evidence for a major
¯uvial refuge in the Zaire Basin. J. Biogeog 18, 403±407.
Corbet, G.B., Hill, J.E., 1991. A World List of Mammalian Species.
Oxford University Press, Oxford.
Corbet, G.B., Hill, J.E., 1992. The Mammals of the Indomalayan
Region: A Systematic Review. Oxford University Press, Oxford.
Crozier, R.H., 1997. Preserving the information content of species:
genetic diversity, phylogeny, and conservation worth. Ann. Rev.
Ecol. Syst 28, 243±268.
Dingle, H., Carroll, S.P., Loye, J.E., 1997. Conservation, behavior,
and 99% of the world's biodiversity: is our ignorance really bliss?
In: Clemmons, J.R., Buchholz, R. (Eds.), Behavioral Approaches to
Conservation in the Wild. Cambridge University Press, New York,
pp. 72±92.
Dobson, A.P., Rodriguez, J.P., Roberts, W.M., Wilcove, D.S., 1997.
Geographic distribution of endangered species in the United States.
Science 275, 550±553.
ESRI Inc., 1998a. ARC/INFO, 7.1.2. Environmental Systems
Research Institute, Inc., Redlands, California.
ESRI Inc., 1998b. ArcView GIS, 3.1. Environmental Systems
Research Institute, Inc., Redlands, California.
Ford, S.M., 1994. Taxonomy and distribution of the owl monkey. In:
Baer, J.F., Weller, R.E., Kakoma, I. (Eds.), Aotus: The Owl Monkey. Academic Press, San Diego, pp. 1±57.
Gaston, K.J., 1994. Rarity. Chapman and Hall, London.
Groves, C.P., 1993. Order Primates. In: Wilson, D.E., Reeder, D.M.
(Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference. Smithsonian Institution Press, Washington, D.C,
pp. 243±277.
Hacker, J.E., Cowlishaw, G., Williams, P.H., 1998. Patterns of African primate diversity and their evaluation for the selection of conservation areas. Biol. Conserv. 84, 251±262.
Ha€er, J., 1969. Speciation in Amazonian forest birds. Science 165,
131±137.
Hannah, L., Lohse, D., Hutchinson, C., Carr, J.L., Lankerani, A.,
1994. A preliminary inventory of human disturbance of world ecosystems. Ambio 23, 246±250.
Harcourt, A.H., 1995. Population viability estimates: theory and
practice for a wild gorilla population. Conserv. Biol 9, 134±142.
Harcourt, A.H., 1996. Is the gorilla a threatened species? How should
we judge? Biol. Conserv 75, 165±176.
Harcourt, C.S., Thornback, J., 1990. Lemurs of Madagascar and the
Comoros. IUCN Ð The World Conservation Union, Gland.
Hengeveld, R., 1990. Dynamic Biogeography. Cambridge, University
Press, Cambridge.
Hershkovitz, P., 1987a. The taxonomy of South American sakis, genus
Pithecia (Cebidae, Platyrrhini): a preliminary report and critical
review with the description of a new species and a new subspecies.
Am. J. Primatol 12, 387±468.
Hershkovitz, P., 1987b. Uacaries, New World monkeys of the genus
Cacajao (Cebidae, Platyrrhini): a preliminary taxonomic review with
the description of a new subspecies. Am. J. Primatol 12, 1±53.
Hershkovitz, P., 1990. Titis, New World Monkeys of the genus Callicebus (Cebidae, Plattyrrhini): a preliminary taxonomic review.
Fieldiana Zoology 55, 1±109.
Howard, P.C., Viskanic, P., Davenport, T.R.B., Kigenyi, F.W., Baltzer, M., Dickinson, C.J., Lwanga, J.S., Matthews, R.A., Balmford,
A., 1998. Complementarity and the use of indicator groups for
reserve selection in Uganda. Nature 394, 472±475.
A.H. Harcourt / Biological Conservation 93 (2000) 163±175
IUCN, 1996. 1996 IUCN Red List of Threatened Animals. IUCN,
Gland, Switzerland.
Jablonski, D., 1995. Extinctions in the fossil record. In: Lawton, J.H.,
May, R.M. (Eds.), Extinction Rates. Oxford University Press,
Oxford, pp. 45±54.
Janzen, D.H., 1988. Tropical dry forests. The most endangered major
tropical ecosystem. In: Wilson, E.O., Peter, F.M. (Eds.), Biodiversity. National Academy Press, Washington, D.C, pp. 130±137.
Jernvall, J., Wright, P.C., 1998. Diversity components of impending
primate extinctions. Proc. Nat. Acad. Sci., USA 95, 11279±11283.
Jolly, D., Taylor, D., Marchant, R., Hamilton, A., Bonne®lle, R.,
Buchet, G., Riollet, G., 1997. Vegetation dynamics in central Africa
since 18,000 yr BP: pollen records from the interlacustrine highlands
of Burundi, Rwanda and western Uganda. J. Biogeog 24, 495±512.
Kappeler, P.M., Heymann, E.W., 1996. Nonconvergence in the evolution of primate life history and socio-ecology. Biol. J. Linn. Soc
59, 297±326.
Kinzey, W.G. (Ed.), 1997. New World Primates. Ecology, Evolution
and Behavior. Aldine de Gruiter, New York.
Leader-Williams, N., Albon, S.D., 1988. Allocation of resources for
conservation. Nature 336, 533±535.
Lernould, J.-M., 1988. Classi®cation and geographical distribution of
guenons: a review. In: Gautier-Hion, A., BourlieÁre, F., Gautier, J.P.,
Kingdon, J. (Eds.), A Primate Radiation: Evolutionary Biology of
the African Guenons. Cambridge University Press, Cambridge, pp.
54±78.
Lynch, L.Z., 1988. Refugia. In: Myers, A.A., Giller, P.S. (Eds.), Analytical Biogeography. Chapman and Hall, London, pp. 311±342.
Manne, L.L., Brooks, T.M., Pimm, S.L., 1999. Relative risk of
extinction of passerine birds on continents and islands. Nature 399,
258±261.
Maurer, B.A., Brown, J.H., Rusler, R.D., 1992. The micro and macro
in body size evolution. Evolution 46, 939±953.
Messier, W., Stewart, C.-B., 1997. Episodic adaptive evolution of primate lysozymes. Nature 385, 151±154.
Miller, K., Allegretti, M.H., Johnson, N., Jonsson, B., 1995. Measures
for conservation of biodiversity and sustainable use of its components. In: Heywood, V.H., Watson, R.T. (Eds.), Global Biodiversity
Assessment. Cambridge University Press, Cambridge, pp. 915±1061.
Mittermeier, R.A., Myers, N., Thomsen, J.R., 1998. da Fonseca, G.
A.B. and Olivieri, S. Biodiverity hotspots and major tropical wilderness areas: approaches to setting conservation priorities. Conserv.
Biol 12, 516±520.
Mittermeier, R.A., Tattersall, I., Konstant, W.R., Meyers, D.M.,
Mast, R.B., Nash, S.D., 1994. Lemurs of Madagascar. Conservation International, Washington, D.C.
Mrosovsky, N., 1997. IUCN's credibility critically endangered. Nature
389, 436.
Myers, N., 1984. The Primary Source. Tropical Forests and Our
Future. W.W. Norton and Co, New York.
Myers, N., 1988. Threatened biotas: hotspots in tropical forests. The
Environmentalist 8, 178±208.
Nash, L.T., Bearder, S.K., Olsen, T.R., 1989. Synopsis of Galago
species characteristics. Int. J. Primatol 10, 57±80.
Niemitz, C., 1984. Taxonomy and distribution of the genus Tarsius
Storr, 1780. In: Niemitz, C. (Ed.), Biology of Tarsiers. Gustav
Fischer, Stuttgart, pp. 1±16.
Oates, J.F., 1988. The distribution of Cercopithecus monkeys in West
African forests. In: Gautier-Hion, A., BourlieÁre, F., Gautier, J.-P.
(Eds.), A Primate Radiation: Evolutionary Biology of the African
Guenons. Cambridge University Press, Cambridge, pp. 79±103.
Oates, J.F., 1994. Africa's primates in 1992: conservation issues and
options. Am. J. Primatol 34, 61±71.
175
Oates, J.F., Davies, A.G., Delson, E., 1994. The diversity of living
colobines. In: Davies, A.G., Oates, J.F. (Eds.), Colobine Monkeys.
Their Ecology, Behaviour and Evolution. Cambridge University
Press, Cambridge, pp. 45±73.
Olson, D.M., Dinerstein, E., 1998. The Global 2000: a representation
approach to conserving the earth's most biologically valuable ecoregions. Conserv. Biol 12, 502±515.
Pearson, D.L., Carroll, S.S., 1998. Global patterns of species richness:
spatial models for conservation planning using bioindicator and
precipitation data. Conserv. Biol 12, 809±821.
Prendergast, J.R., Quinn, R.M., Lawton, J.H., Eversham, B.C., Gibbons, D.W., 1993. Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365, 335±337.
Pressey, R.L., Humphries, C.J., Margules, C.R., Vane-Wright, R.I.,
Williams, P.H., 1993. Beyond opportunism: key principles for systematic Reserve selection. Trends Ecol. Evol 8, 124±128.
Reed, K.E., Fleagle, J.G., 1995. Geographic and climatic control of
primate diversity. Proc. Nat. Acad. Sci., USA 92, 7874±7876.
Reid, W.V., 1998. Biodiversity hotspots. Trends Ecol. Evol 13, 275±280.
Ricketts, T.H., Dinerstein, E., Olson, D.M., Loucks, C., 1999. Who's
were in North America? BioScience 49, 369±381.
Rosenzweig, M.L., 1995. Species Diversity in Space and Time. Cambridge University Press, Cambridge.
Rowe, N., 1996. The Pictorial Guide to the Living Primates. Pogonias
Press, East Hampton, NY.
Rylands, A.B., Coimbra-Filho, A.F., Mitermeier, R.A., 1993. Systematics, geographic distribution, and some notes on the conservation status of the Callitrichidae. In: Rylands, A.B. (Ed.), Marmosets
and Tamarins. Systematics, Behaviour, and Ecology. Oxford University Press, Oxford, pp. 11±77.
Scott, J.M., Anderson, H., Davis, F., Caicoo, S., Csuti, B., Edwards,
T.C.J., Noss, R., Ulliman, J., Groves, C., Wright, R.G., 1993. Gap
analysis a geographic approach to protection of biological diversity.
Wildl. Monogr 123, 1±41.
Shepherd, U.L., 1998. A comparison of species diversity and morphological diversity across the North American latitudinal gradient.
J. Biogeog 25, 19±29.
Terborgh, J., Schaik, C.P.v., 1987. Convergence vs nonconvergence in
primate communities. In: Gee, J.H.R., Giller, P.S. (Eds.), Organization of Communities Past and Present. Blackwell Scienti®c Publications, Oxford, pp. 185±203.
Terborgh, J., Winter, B., 1983. A method for siting parks and reserves
with special reference to Columbia and Ecuador. Biol. Conserv 27,
45±58.
van Jaarsveld, A.S., Freitag, S., Chown, S.L., Muller, C., Koch, S.,
Hull, H., Bellamy, C., KruÈger, M., EndroÈody-Younga, S., Mansell,
M.M., Scholtz, C.H, 1998. Biodiversity assessment and conservation strategies. Science 279, 2106±2108.
Vermeij, G.J., 1978. Biogeography and Adaptation. Harvard University Press, Cambridge, MA.
Wallace, A.R., 1876. The Geographical Distribution of Animals.
Macmillan, London.
Williams, P.H., Gaston, K.J., 1994. Measuring more of biodiversity:
can higher-taxon richness predict wholesale species richness Biol?
Conserv 67, 211±217.
Williams, P.H., Gaston, K.J., Humphries, C.J., 1997. Mapping biodiversity value worldwide: combining higher-taxon richness from different groups. Proc. Roy. Soc. Lond. B 264, 141±148.
Williams, P.H., Humphries, C.J., 1997. Comparing character diversity
among biotas. In: Gaston, K.J. (Ed.), Biodiversity. A Biology of
Numbers and Di€erences. Blackwell Science, Oxford, pp. 54±76.
Wolfheim, J.H., 1983. Primates of the World: Distribution, Abundance and Conservation. University of Washington Press, Seattle.