Threatened primates experience high human densities: Adding an index of threat to the IUCN Red List criteria

Abstract

IUCN Red List conservation status is apparently judged mainly by assessment of species' susceptibility to threat. However, risk must often depend also on the threat itself. Therefore, we investigate the value of adding to IUCN's current criteria a separate index of threat, human density. Human density in the geographic range of Threatened primate species is significantly higher than in the range of Lower Risk species. Thus, Threatened species are both susceptible, and experience more threat. However, the match is far from perfect. Given abundant other evidence of adverse effects of high human density, the mismatch emphasizes the potential benefit of adding an index of threat to the current criteria. A main advantage might be improved assessment, given the amount of up-to-date data on threats compared with the paucity on reactions to threat. The simplest means of incorporation might be to increase the status of species that experience higher than a certain threshold human density.

Full text

Threatened primates experience high human densities: adding an
index of threat to the IUCN Red List criteria
A.H. Harcourt*, S.A. Parks
Department of Anthropology, University of California, One Shields Avenue, Davis, CA 95616, USA
Received 26 March 2001; received in revised form 15 December 2001; accepted 17 April 2002
Abstract
IUCN Red List conservation status is apparently judged mainly by assessment of species’ susceptibility to threat. However, risk
must often depend also on the threat itself. Therefore, we investigate the value of adding to IUCN’s current criteria a separate index
of threat, human density. Human density in the geographic range of Threatened primate species is significantly higher than in the
range of Lower Risk species. Thus, Threatened species are both susceptible, and experience more threat. However, the match is far
from perfect. Given abundant other evidence of adverse effects of high human density, the mismatch emphasizes the potential
benefit of adding an index of threat to the current criteria. A main advantage might be improved assessment, given the amount of
up-to-date data on threats compared with the paucity on reactions to threat. The simplest means of incorporation might be to
increase the status of species that experience higher than a certain threshold human density. #2002 Elsevier Science Ltd. All rights
reserved.
Keywords: Conservation; Human density; IUCN; Primates; Red List
1. Introduction
IUCN currently uses for its influential Red List of
threatened species three main indices to determine the
conservation status of a species (IUCN, 1996, 2000).
These indices are, broadly, the species’ population size,
rate of population decline, and its geographic range. The
fourth index, a population viability analysis, is hardly
used at all. If any one of the indices indicates that a spe-
cies crosses a threshold (below a certain population size
or geographic range, above a certain rate of decline), the
species is given the relevant higher conservation status
(from Lower Risk to Vulnerable to Endangered to Cri-
tically Endangered; IUCN, 1996, 2000).
These indices assess, in effect, the species’ predisposi-
tion to threat, and their reaction to it. That is entirely
appropriate, because species react differently to the
same threat (Brown, 1971; Terborgh, 1974; Diamond,
1984; Jablonski, 1991; Laurance, 1991; Leach and
Givnish, 1996; Harcourt, 1998; Jernvall and Wright,
1998; Cowlishaw and Dunbar, 2000; Harcourt, 2001).
However, estimates of relative probability of extinction,
which is essentially what the Red List classifications are,
depend not just on the species’ susceptibility to threat,
but also on the nature and intensity of the threat itself.
The crucial distinction between susceptibility to threat
and intensity of threat is one that is hidden not only by
the current Red List criteria, but perhaps also by the use
of the word ‘threatened’ which can mean both ‘suscep-
tible’ and ‘under threat’. An open house is susceptible to
burglary, but it is not threatened by it unless a burglar is
in the vicinity. Thus, a species becomes more threatened
as soon as a large, polluting city is built next to its
range, even if population size, rate of decline, and geo-
graphic range all remain the same. That is why analyses
showing that hotspots of biodiversity are also hotspots
of human activity are so alarming (Dobson et al., 1997;
Cincotta et al., 2000; Balmford et al., 2001).
The performance of the IUCN Red List criteria are
continuously evaluated both within IUCN (Hilton-
Taylor, 2000) and outside (Akc¸ akaya et al., 2000). Here
we add to those evaluations by proposing that several
advantages would accrue if an index of threat were
explicitly incorporated as an additional major criterion
to categorize the conservation status of species.
0006-3207/02/$ - see front matter #2002 Elsevier Science Ltd. All rights reserved.
PII: S0006-3207(02)00146-5
Biological Conservation 109 (2003) 137–149
www.elsevier.com/locate/biocon
* Corresponding author.
E-mail address: ahharcourt@ucdavis.edu (A.H. Harcourt).

First, an additional separate, explicit criterion, espe-
cially one for which abundant evidence indicates its
relevance, should improve assessment of risk, because it
could provide an extra indicator of risk that is not
necessarily always used in the current criteria.
Second, increased transparency is a goal of the Red
List changes (Hilton-Taylor, 2000). Adding threat as a
separate criterion should make explicit what might be
a fairly cryptic index already sometimes used. Measures
of threat in the form of ‘levels of exploitation’, and ‘the
effects of introduced taxa, hybridization, pathogens,
pollutants, competitors, or parasites’ are currently listed
as potential measures to predict future population
decline (IUCN, 1996, 2000). However, intensity of any
threat itself is not a separate criterion in the Red List’s
assessment of conservation status (IUCN, 1996, 2000).
Thus its incorporation into assessment of status is both
presumably irregular, and also hidden to the user.
Third, if a species’ conservation status was explicitly
indicated as due to threat, as opposed to reaction to
threat, management might be better refined. The Red
Lists are produced to focus attention on especially
threatened species and to help prioritization of action
(Mace, 1995; IUCN, 2000). Management decisions
could be very different depending on whether the threat
itself, or the species’ response to the threat, is judged to
be the prime danger. If threat is the main problem, the
threat needs mitigation (e.g. prevent settlement around
the forest); if susceptibility is the main problem, we
mitigate that (e.g. translocate individuals to increase
genetic heterogeneity).
Fourth, conservation status is best assessed with
good, abundant, up-to-date, easily obtainable data
(Gaston, 1994, p. 144). Data on human activity are such
(e.g. World Resources Institute, 2000). By contrast, data
on population size and rate of population decline are
usually little more than informed guesswork, especially
in tropical countries (Harcourt, 1995).
A specific index of threat needs to be chosen. Abun-
dant evidence indicates that across continents, rates of
disappearance of habitat and of species correlate with
human density, or other measures of human activity
(Parker and Graham, 1989; Barnes, 1990; Hannah et
al., 1994; Kerr and Currie, 1995; McNeely et al., 1995;
Harcourt, 1996; Bawa and Dayanandan, 1997; Hoare
and Du Toit, 1999; Muchaal and Ngandjui, 1999;
Robinson et al., 1999; Cowlishaw and Dunbar, 2000,
Chapter 8; Woodroffe, 2000; McKinney, 2001). Also
up-to-date, precise data on human density are easily
available (e.g. World Resources Institute, 2000). We
therefore suggest that human density as an index of
threat might be a good candidate criterion to use as an
additional measure for assessing a species’ conservation
status.
We here test the value of adding threat in the form of
human density as a criterion by calculating mean
human density in the geographic range of all primate
species, one of the better known orders of mammal, and
comparing it with the species’ 1996 Red List conserva-
tion status. The predictions are that (1) Threatened
species experience a higher human density in their geo-
graphic range than do the Lower Risk species (Wright
and Jernvall, 1999); and that (2) the most threatened
species will experience the highest human density.
Additionally, we assess conservation status on the basis
of only the two measures for which most data are
available, geographic range of species, and human den-
sity within the range. The null hypothesis is that threat
is well incorporated into the current listing, and thus
that the new listing will match the current Red List. If
the new list shows a change in conservation status of
many species, the value of the Red List probably needs
reassessment.
2. Methods
We used the IUCN Red List (IUCN, 1996) to sepa-
rate taxa according to their conservation status. [We did
not use the latest listing (IUCN, 2000), because its tax-
onomy is too new for adequate assessment.] The status
of each species was then related to human density. As in
all such analyses, circularity is a potential problem if the
correlate tested was explicitly used in the assessment of
conservation status in the first place. We cannot know
whether it was for Red List categorizations, because so
few of the IUCN Red List assessments are published,
and the unpublished ones are so difficult to obtain.
Previous detailed IUCN Red List assessments for pri-
mates have been produced, but they were published
before the current quantitative criteria were finalized
(Lee et al., 1988; Harcourt and Thornback, 1990).
Geographic range as used by IUCN probably includes
an element of human influence, but how much, we do
not know. With so little indication of whether or how
human density was used in assessing status in the cur-
rent Red List, we consider that it is valid to test human
density as a potentially useful additional index of con-
servation status.
Analyses were performed for the globe, and then for
the continents separately, because continents differ so
greatly in their proportions of threatened species
and their human density, as well as in many other
aspects of their natural and human geography (World
Resources Institute, 2000).
2.1. Conservation status
IUCN now has five main categories of conservation
status (IUCN, 2000), three threatened categories—
Critically Endangered, Endangered, Vulnerable—and
two Lower Risk categories, Near Threatened and Least
138 A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149

Concern. We combine these two safer categories into
one, Lower Risk.
2.2. Taxonomy
Taxonomic nomenclature and listing is mostly from
Groves (1993), Corbet and Hill (1991), and the Red List
(IUCN, 1996). Where the sources differed, the one with
the fewer species was chosen, although Papio remains as
five species. Callicebus is treated as three species (as in
Wolfheim 1983), because the two main authorities differ
(Hershkovitz, 1990; Groves, 1993). Not all taxa in the
Red List (IUCN, 1996) were included in the analysis
here. Missing species are those that do not appear in
one or other of the two main taxonomic sources. The
missing species are largely recent splits reflecting minor
morphological variations at single geographic sites,
some of which are taxonomically contested. The exclu-
sion of the 1996 IUCN Red List species in no instance
affects the Red List classification of their sister species,
because the geographic ranges of the excluded species
are very small by comparison with 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 the Red List’s two species. The 1996 Red
List species not included in this analysis are, in order of
listing, Aotus brumbacki, A. lemurinus, Brachyteles
hypoxanthus, Callicebus dubius, Cebus kaapori, Cebus
xanthosternos, Cercopithecus preussi, Cercopithecus
sclateri, Cercopithecus solatus, Hapalemur aureus,
Macaca brunnescens, Macaca pagensis, Microcebus
myoxinus, Saimiri oerstedii (possibly a human introduc-
tion), Saimiri vanzolinii, Trachypithecus delacouri, and
Trachypithecus poliocephalus.
2.3. Geographic range
We took species’ geographic range from, in effect,
convex polygon coverages digitized from maps in
Wolfheim (1983), with subsequent correction and addi-
tion from, in particular, Corbet and Hill (1992), Groves
(1993), Niemitz (1984), Hershkovitz (1987a, b; 1990),
Lernould (1988), Nash et al., (1989), Harcourt and
Thornback (1990), Rylands et al. (1993), Ford (1994),
Mittermeier et al. (1994), Oates et al. (1994), and Kinzey
(1997). The coverages produce maximum ranges, and
thus minimize recent retreats of range due to humans.
2.4. Human density
Human density data were taken from the CIESIN
web site (Tobler et al., 1995). These density data are far
more precise than in most other such global analyses,
which often use countrywide means as the data (e.g.
Kerr and Currie, 1995; McKinney, 2001). The data are
presented in the site as a grid with a cell size of
0.0830.083 degrees (or 5050, or approximately 9
km9 km at the equator). We used the ‘smoothed’ ver-
sion of the data in the site, because it removes abrupt
transitions in density at political boundaries, and thus
provides a more realistic distribution of densities.
From the data, we calculated the mean density in each
species’ geographic range by use of Arc/Info (ESRI Inc.,
1998a) and ArcView GIS (ESRI Inc., 1998b). Each
species’ geographic range was converted to a grid/raster
format using ArcView GIS. The ‘con’ functions in Arc/
Info ‘clipped’ the human density that overlapped the
particular geographic range of a species. The mean
value of such overlapping human density values was
used in this paper.
Means are affected by extremes, of course. However,
we suggest that a species’ range that is mostly empty of
humans, but has a city at one edge, is better represented
by a density value that incorporates that city than one
that does not, such as the mode or median.
2.5. Statistics and independence of data
Statistical tests require independence of data. Given
that certain sorts of organism are inherently more prone
to extinction than are others (earlier), species might not
be independent data points: if one species in a genus or
family is Threatened, the others might be more likely to
be also. Furthermore, neither species, nor human den-
sities are equally distributed across the globe. Therefore,
phylogeny is confounded with human density. Asia, for
instance, has an overall human density about five times
that of the other continents ((World Resources Insti-
tute, 1998). Thus, all five of the purely Asian snub-
nosed langur species [Pygathrix (Rhinopithecus)] are not
only Threatened but also in regions of relatively high
human density (147 people/km
2
), whereas all five
baboon species of Africa (Papio) are both Low Risk and
in relatively low density (median of 26 people/km
2
).
Therefore, in addition to analysis with species as data
points, we also take account of phylogeny by use of
Comparative Analysis by Independent Contrasts
(CAIC) (Purvis and Rambaut, 1995), and we examine
the continents separately. For this analysis, the phylo-
geny used is that of Purvis and Webster (1999), which is
an update from the phylogeny of Purvis (1995), perhaps
the most broadly substantiated single phylogeny for all
primates so far published.
These means of accounting for dependence still do not
get over the problem that several species can overlay a
region with a single human density. However, (1) unless
overlap of geographic range is complete, two species
have the chance to experience different mean densities in
their range; (2) as species can react differently to the
same threat, even if the overlap is complete, the two
species could have a different conservation status.
A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149 139

Statistical tests are performed with JMP (SAS Insti-
tute Inc, 1995), and with Statview SE+ (Abacus Con-
cepts, 1990–1991) for the Wilcoxon matched pairs,
signed rank tests. All probabilities are two-tailed.
3. Results
3.1. Human density in relation to Red List conservation
status
The current IUCN criteria apply to all taxa and all
continents. Globally, human density is higher in the
geographic ranges of Threatened species than it is in
the ranges of Lower Risk species, differing significantly
across the four IUCN classes of conservation status
(F=9.15; df=3; P<0.0001) (Table 1; Fig. 1). While
human density does not differ across the three classes of
Threatened status (F=0.92, df=2), the human density
of each threatened status class independently differs
significantly from that of Low Risk species (N=45, 22,
9 vs. 127; df=1; F>7.0; P<0.01). Combining the three
Threatened classes, human density in the geographic
ranges of Threatened species (56 people/km
2
) is sig-
nificantly greater (F=25.65; df=1; P<0.0001) than
that in the geographic ranges of Lower Risk species (21
people/km
2
) (Table 2, Fig. 2). Thus the first prediction
that threatened species will experience higher human
density than unthreatened is upheld. However, the sec-
ond, that degree of threat would be proportional to
human density, is not.
A very strong continental effect exists in this global
comparison of densities, indeed a stronger effect than of
conservation status, whether four, three, or two levels
of conservation status are analyzed (F>50.0,
P<0.0001). That is not surprising given the differences
between the continents in overall densities, and propor-
tions of Threatened species (Fig. 1). We nevertheless
lump the continents in the global comparisons, because
that is how IUCN currently produces its Red Lists.
Accounting for phylogeny by use of CAIC (Methods),
the difference is upheld. With 200 species available for
comparison, 50 contrasts between phylogenetically
independent taxa with different conservation status
indicate that the more threatened taxa are significantly
likely to experience higher human density than are taxa
of lower conservation status (across the four categories,
32 of the 50 contrasts showed the more threatened
taxon with higher human density than the less threa-
tened taxon; N=32/18; T=356; z=2.72; P<0.01).
Comparing all Threatened with Low Risk (two cate-
gories, N=44 contrasts), the difference was even more
obvious (N=32/12; T=184; z=3.63; P<0.001). As in
the phylogenetically uncorrected analysis, no significant
differences existed within the Threatened classes
(N=16/9; T=118, z=1.2; P>0.1).
Taking the continents separately [significant hetero-
geneity exists among them (earlier)], human density
correlates significantly with conservation status in Asia
and in South and Central America, but not in Africa or
Madagascar (Table 2, Fig. 1). However in no continent
alone are the differences significant when phylogeny is
accounted for (P>0.1).
IUCN (1996) lists nine primate species as Data Defi-
cient, all in Asia. [By 2000, over twice as many were so
listed, over two thirds of them in Asia (IUCN, 2000).
Many of these were not included in this analysis, for the
reasons stated in Section 2.] Data Deficient species are
not assigned a threat status. If the median human den-
sity of 56 people/km
2
for Threatened species is taken as
a threshold, and taxa above that threshold classified as
Threatened, five of the nine Data Deficient species
should be classified as Threatened. In other words, use
of human density as a criterion allows the Red List to
provide a warning that otherwise would be missing.
3.2. The distribution of status in relation to human
density
So far we have analyzed human density in relation to
Red List status, asking whether taxa with higher Red
List status experience higher human densities. They do.
Alternatively, we can ask about the distribution of taxa
of different Red List status in regions of differing
human density. To answer this question, we divided the
range of human densities per continent and globally
into five equal divisions, and examined the distribution
of species of different status across the divisions.
The results provide rather a different picture from the
previous analysis, although the same trend. A sub-
stantial majority of species on all continents except
Madagascar exist in the lowest quantile of human den-
sity (74% in Africa, 67% in Asia, 92% in the Americas,
33% in Madagascar, and 91% globally). In other
words, and not surprisingly, most taxa, including some
Critically Endangered taxa, occur in regions of low
human density—most primates are in forest, in which
humans tend not to be at high density.
A methodological consequence of the fact that most
taxa are in this one category of lowest quantile of
human density is that there are not enough entries in the
other four quantiles to compare the distribution of all
four conservation categories across all five human den-
sity categories. We thus performed a 22w
2
on number
of Threatened compared with Lower Risk species in the
lowest density quantile compared with the rest. The
result is, as expected, a significantly greater proportion
of Threatened species in regions of higher human den-
sity than in regions of the lowest human density across
the globe and in the Americas, but not in the other
continents (Globe, w
2
=13.3, P<0.001; Americas,
w
2
=9.1, P<0.01; Africa, Asia, Madagascar, P>0.1).
140 A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149

Table 1
Per continent for each primate species for which data are available, their IUCN Red List conservation status (IUCN), mean human density in their
geographic range in people/km
2
(HD), the size of their geographic range in km
2
10
4
(GR) (or ‘extent of occurrence’; IUCN, 1996), and their new
conservation status with human density and geographic range alone used to classify status (New CS) (see Section 2 for details)
IUCN HD GR New CS
Africa
Allenopithecus nigroviridis 4 8.33 38.92 L
Arctocebus aureus 4 7.50 75.66 L
Arctocebus calabarensis 4* 142.23 23.54 H
Cercocebus agilis 4 9.52 101.31 L
Cercocebus galeritus 4 4.53 0.39 I
Cercocebus torquatus 4* 97.56 51.30 I
Cercopithecus ascanius 4 29.76 281.39 I
Cercopithecus campbelli 4* 61.06 52.03 I
Cercopithecus cephus 4 17.42 75.01 L
Cercopithecus diana 3* 58.36 32.04 H
Cercopithecus erythrogaster 3* 281.40 2.80 H*
Cercopithecus erythrotis 3* 134.41 8.55 H
Cercopithecus hamlyni 4* 43.92 26.04 H
Cercopithecus lhoesti 4* 66.09 38.75 I
Cercopithecus mitis 4* 32.39 418.12 I
Cercopithecus mona 4* 135.78 46.01 I
Cercopithecus neglectus 4 17.67 284.12 L
Cercopithecus nictitans 4* 44.99 161.99 I
Cercopithecus petaurista 4* 62.33 58.37 I
Cercopithecus pogonias 4 16.54 94.08 L
Cercopithecus wolfi 4 18.38 143.43 L
Chlorocebus aethiops 4 31.24 1439.37 I
Colobus angolensis 4 21.00 204.60 L
Colobus guereza 4* 38.30 236.60 I
Colobus polykomos 4* 33.51 47.80 I
Colobus satanas 3 9.01 28.77 I
Colobus vellerosus 3* 79.55 31.74 H
Erythrocebus patas 4 27.11 592.43 L
Euoticus elegantulus 4 8.25 72.96 L
Euoticus pallidus 4* 139.05 21.16 H
Galago alleni 4* 38.35 61.15 I
Galago gallarum 4 12.22 78.20 L
Galago matschiei 4* 104.30 19.18 H
Galago moholi 4 18.31 442.24 L
Galago senegalensis 4* 34.11 785.46 I
Galagoides demidoff 4* 35.36 435.48 I
Galagoides thomasi 4* 45.84 68.80 I
Galagoides zanzibaricus 4 30.43 117.17 I
Gorilla gorilla 2 15.81 80.86 L
Lophocebus albigena 4 16.25 170.33 L
Lophocebus aterrimus 4 13.77 96.53 L
Macaca sylvanus 3* 176.91 7.74 H
Mandrillus leucophaeus 2* 88.82 12.43 H
Mandrillus sphinx 4 11.30 42.84 L
Miopithecus talapoin 4 17.32 117.11 L
Otolemur crassicaudatus 4 27.07 418.06 L
Otolemur garnetti 4* 33.44 66.99 I
Pan paniscus 2 7.84 46.80 L
Pan troglodytes 2 29.11 249.80 I
Papio anubis 4* 34.18 806.91 I
Papio cynocephalus 4 20.97 379.97 L
Papio hamadryas 4 31.17 114.02 I
Papio papio 4 25.59 39.49 L
Papio ursinus 4 22.09 317.82 L
Perodicticus potto 4* 38.72 339.72 I
Procolobus badius 4* 38.03 226.14 I
Procolobus verus 4* 65.72 47.04 I
Theropithecus gelada 4* 104.74 12.49 H
(Table continued on next page)
A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149 141

Table 1 (continued)
IUCN HD GR New CS
Southeast Asia
Hylobates agilis 4 50.92 50.45 I
Hylobates concolor 2* 223.61 10.99 H
Hylobates gabriellae 4 94.48 27.66 H
Hylobates hoolock 4* 154.32 79.45 I
Hylobates klossii 3 56.80 0.91 H
Hylobates lar 4* 105.31 76.19 I
Hylobates leucogenys 4 46.54 17.22 H
Hylobates moloch 1* 990.71 5.39 H*
Hylobates muelleri 4 20.57 56.47 L
Hylobates pileatus 3 74.71 22.16 H
Hylobates syndactylus 4 77.56 20.37 H
Loris tardigradus 3* 311.32 81.32 I
Macaca arctoides 3* 156.48 172.65 I
Macaca assamensis 3* 144.73 156.69 I
Macaca cyclopis 3* 400.33 3.14 H*
Macaca fascicularis 4* 130.26 253.58 I
Macaca fuscata 2* 322.45 16.83 H
Macaca maura 2* 193.45 1.49 H*
Macaca mulatta 4* 236.81 577.84 I
Macaca nemestrina 3 81.31 312.69 I
Macaca nigra 2 52.30 1.69 H
Macaca ochreata 4 32.94 3.69 H
Macaca radiata 4* 287.97 70.82 I
Macaca silenus 2* 260.13 3.51 H*
Macaca sinica 4* 270.33 6.49 H
Macaca thibetana 4* 332.88 138.70 I
Macaca tonkeana 4 40.34 11.10 H
Nasalis larvatus 3 31.85 28.40 H
Nycticebus coucang 4* 113.73 375.82 I
Nycticebus pygmaeus 3* 122.25 45.92 I
Pongo pygmaeus 3 11.41 31.83 I
Presbytis comata 2* 928.97 4.79 H*
Presbytis frontata 4 22.37 25.77 I
Presbytis hosei 4 12.42 22.22 I
Presbytis melalophos 4 81.24 65.74 I
Presbytis potenziani 3 56.80 0.92 H
Presbytis rubicunda 4 15.86 65.42 L
Presbytis thomasi 4 59.17 5.07 H
Pygathrix avunculus 1* 147.44 1.13 H*
Pygathrix bieti 2 48.02 3.64 H
Pygathrix brelichi 2* 253.74 0.44 H*
Pygathrix nemaeus 2 82.92 41.57 I
Pygathrix roxellana 3* 163.63 2.48 H*
Semnopithecus entellus 4* 333.82 281.52 I
Simias concolor 2 56.80 0.92 H
Tarsius bancanus 4 104.27 34.54 H
Tarsius dianae 4 14.00 0.02 I
Tarsius spectrum 4 56.24 7.99 H
Tarsius syrichta 4* 148.42 6.47 H
Trachypithecus auratus 3* 848.30 13.03 H
Trachypithecus cristatus 4 84.88 123.43 I
Trachypithecus francoisi 3* 197.52 17.36 H
Trachypithecus geei 4 88.27 1.38 H*
Trachypithecus johnii 3* 327.42 2.43 H
Trachypithecus obscurus 4 88.37 23.51 H
Trachypithecus phayrei 4 103.62 123.93 I
Trachypithecus pileatus 3* 191.80 44.53 I
Trachypithecus vetulus 3* 309.73 4.73 H*
Madagascar
Allocebus trichotis 1 15.89 0.07 I
Avahi laniger 4* 27.20 9.30 I
142 A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149

Table 1 (continued)
IUCN HD GR New CS
Avahi occidentalis 3* 19.28 1.00 I
Cheirogaleus major 4* 25.61 12.04 I
Cheirogaleus medius 4 11.64 14.64 I
Daubentonia madagascariensis 2* 26.01 12.87 I
Eulemur coronatus 3 16.00 0.75 I
Eulemur fulvus 4 17.58 24.76 I
Eulemur macaco 3 14.47 1.00 I
Eulemur mongoz 3* 21.19 2.46 I
Eulemur rubriventer 3* 29.36 6.39 H
Hapalemur griseus 4* 28.77 13.29 I
Hapalemur simus 1* 41.10 0.07 H
Indri indri 2* 25.52 5.21 I
Lemur catta 3 11.88 12.30 I
Lepilemur dorsalis 3 16.68 0.65 I
Lepilemur edwardsi 4 9.56 5.42 I
Lepilemur leucopus 4 15.59 3.46 I
Lepilemur microdon 4* 23.96 4.08 I
Lepilemur mustelinus 4* 31.07 6.62 H
Lepilemur ruficaudatus 4 9.90 5.83 I
Lepilemur septentrionalis 3* 17.92 0.21 I
Microcebus murinus 4 11.07 17.21 I
Microcebus rufus 4* 28.63 13.65 I
Mirza coquereli 3 8.94 3.86 I
Phaner furcifer 4 8.71 4.35 I
Propithecus diadema 2* 27.98 7.28 I
Propithecus tattersalli 1 11.00 0.05 I
Propithecus verreauxi 3 10.78 20.34 I
Varecia variegata 2* 26.79 6.34 I
Americas
Alouatta belzebul 4* 5.43 174.00 L*
Alouatta caraya 4* 14.29 236.73 L
Alouatta fusca 3* 64.62 83.90 I
Alouatta palliata 4* 60.65 56.54 I
Alouatta pigra 4* 43.34 28.91 H
Alouatta seniculus 4* 11.05 579.75 L
Aotus azarae 4 3.72 56.58 L
Aotus infulatus 4 4.77 336.15 L*
Aotus miconax 3* 6.75 19.90 I
Aotus nancymae 4 0.62 27.09 I
Aotus nigriceps 4 2.01 121.64 L*
Aotus trivirgatus 4 2.09 83.73 L
Aotus vociferans 4* 20.71 199.31 L
Ateles belzebuth 3* 15.07 227.38 L
Ateles chamek 4 4.09 188.86 L*
Ateles fusciceps 3* 43.22 13.15 H
Ateles geoffroyi 4* 55.26 84.89 I
Ateles marginatus 2 4 36.91 L
Ateles paniscus 4 3.8 96.01 L
Brachyteles arachnoides 2* 86.99 43.09 I
Cacajao calvus 3 1.59 17.02 I
Cacajao melanocephalus 4 0.54 67.66 L
Callicebus moloch 4 2.81 405.50 L*
Callicebus personatus 3* 68.88 72.74 I
Callicebus torquatus 4 1.14 189.48 L*
Callimico goeldii 3 2.55 113.17 L
Callithrix argentata 4 3.81 111.42 L
Callithrix aurita 2* 142.62 17.35 H
Callithrix emiliae 4 1.41 21.41 I
Callithrix flaviceps 2* 52.08 4.32 H
Callithrix geoffroyi 3* 28.12 12.33 I
(Table continued on next page)
A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149 143

3.3. Conservation status judged using only human
density and geographic range
In the new listing of conservation status tested here,
we use only two indices of risk, human density and
geographic range, the two indices with the most data.
While Threatened species experience higher human
densities than Lower Risk species, and on average have
smaller geographic ranges, meaning that geographic
range correlates with density (N=203; F=7.46;
P<0.01), the relationship between the two indices of
threat is not nearly tight enough for either to be used as
a surrogate of the other (r
2
adj.=0.03).
We divide conservation status into three categories,
High, Intermediate, and Low Priority. High Priority taxa
experience high human density (more than the median)
in a small geographic range (less than the median);
Intermediate Priority taxa experience either high human
density in a large geographic range, or low human den-
sity in a small geographic range; and Low Priority taxa
experience low human density in a large geographic
range. We further divide the High and Low priority
categories. Thus Very High Priority species are those
with human density in their geographic range higher
than the upper quartile value for the globe, along with a
geographic range size lower than the lower quartile
value. Similarly Very Low Priority species would be
those with human density lower than the lower quartile,
and geographic range size above the upper quartile.
The new list (Table 1) is quite different from the cur-
rent one. Instead of just nine Critically Endangered pri-
mate species in the 1996 Red List, there are 54 High
Table 1 (continued)
IUCN HD GR New CS
Callithrix humeralifer 4 1.75 20.34 I
Callithrix hybrids 4* 46.22 19.40 H
Callithrix jacchus 4* 32.94 65.94 I
Callithrix kuhlii 4* 47.27 2.76 H
Callithrix nigriceps 3 1.01 1.41 I
Callithrix penicillata 4* 21.27 131.13 L
Cebuella pygmaea 4 1.27 135.94 L*
Cebus albifrons 4* 8.01 388.54 L*
Cebus apella 4* 14.05 1209.53 L
Cebus capucinus 4* 37.85 42.39 I
Cebus olivaceus 4* 7.92 198.47 L*
Chiropotes albinasus 4 2.52 66.58 L
Chiropotes satanas 4 4.66 205.74 L*
Lagothrix flavicauda 1* 8.52 0.57 I
Lagothrix lagotricha 4 4.64 352.46 L*
Leontopithecus caissara 1* 70.37 0.36 H
Leontopithecus chrysomelas 2* 22.73 3.57 I
Leontopithecus chrysopygus 1* 129.37 4.56 H*
Leontopithecus rosalia 1* 375.71 2.66 H*
Pithecia irrorata 4 1.77 137.95 L*
Pithecia monachus 4 2.35 111.76 L
Pithecia pithecia 4 2.62 178.15 L*
Saguinus bicolor 4* 18.57 5.78 I
Saguinus fuscicollis 4 3.16 169.66 L*
Saguinus geoffroyi 4* 28.21 6.06 I
Saguinus imperator 4 1.52 22.38 I
Saguinus inustus 4 0.46 36.06 I
Saguinus labiatus 4 0.93 29.49 I
Saguinus leucopus 3* 73.82 5.88 H
Saguinus midas 4 3.62 158.91 L*
Saguinus mystax 4 0.72 59.71 L
Saguinus nigricollis 4 4.66 26.84 I
Saguinus oedipus 2* 91.51 4.98 H*
Saguinus tripartitus 4 4.95 3.09 I
Saimiri sciureus 4 4.29 586.06 L*
IUCN status: 1=Critically Endangered; 2=Endangered; 3=Vulnerable; 4=Lower Risk. New CS: H=High Priority (above median human density/
below median geographic range); L=Low Priority (the opposite); I=Intermediate Priority. * in IUCN column indicate species with human densities
in their geographic range of more than the median for the continent, in other words species that might be especially at risk within each IUCN Red
List status. * in New CS column indicate species that are either Very High or Very Low Priority (above and below upper and lower quartiles for
density and range, accordingly).
144 A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149

Priority species (‘H’ in the Table’s New CS column).
Furthermore, 17 of these are currently listed in the Red
List as Low Risk (‘4’ in the IUCN column). The new
classification produces 15 Very High Priority species
(‘H*’), none of which is Low Risk. Instead of 128 Low
Risk species, there are 60 Low Priority species (L under
New CS), none of which is Critically Endangered in the
IUCN Red List, although two of them Endangered (‘2’
under IUCN). And 16 Very Low Priority species exist
(‘L*’), all of them previously Low Risk in the Red List.
All are in South America. Four Data Deficient species
become High Priority, and one is Low Priority.
4. Discussion
4.1. Threat as an additional Red List criterion
This study indicates that, in general, primate species
that are currently reacting poorly to threats (as judged
by current IUCN Red List status) are also especially
threatened, because they experience relatively high
human densities in their geographic range (Figs. 1 and
2). If the relationship between current status and human
density were tight, adding human density as another
criterion by which to judge status would not improve
Fig. 1. Human density within primate species’ geographic ranges by IUCN Red List conservation status of the species. Results are median species’
density at each status for each region. Low Risk=Lower Risk; Vuln=Vulnerable; End’d=Endangered; Crit. End=Critically Endangered.
Madag.=Madagascar; S/C Amer.=South and Central America. Details of statistical tests are given in Table 2.
Table 2
ANOVAR statistics for comparisons of human density across all four categories of conservation status (All), and between Threatened and Low Risk
categories (T vs LR); and for comparisons between Threatened and Low Risk categories when phylogeny is controlled for by comparative analysis
by independent contrasts (T vs LRCAIC), where the statistic is the zvalue from Wilcoxon matched pairs, signed rank tests of the results of the
comparative analysis by independent contrasts (N=50 contrasts)
Conservation Status Globe Africa Asia Madagascar S/C America
F/z P<F/z P<F/z P<F/z P<F/z P<
All (df=2–3) 9.15 0.0001 2.06 ns 3.08 0.04 1.50 ns 8.11 0.0001
T vs LR (df=1) 25.65 0.0001 2.81 0.1 7.10 0.02 0.15 ns 18.27 0.0001
TvsLRCAIC 3.63 0.001 1.52 ns 0.97 ns 0.0 ns 1.95 0.1
N=217 species (61 in Africa, 51 in Asia, 32 in Madagascar, and 73 in the Americas). Probability given as ‘ns’ when P>0.1.
A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149 145

the categorization of conservation status. However, the
relationship between current Red List status and human
density is very loose, so loose that within the three
Threatened Red List categories, no relationship at all
exists (Fig. 1).
Furthermore, the new classification of conservation
status tested here, which was based on geographic range
and human density alone (the two indices for which
most data are available), produced many differences
from the current Red List, which is based largely on
geographic range and population parameters (Table 1).
Unless one, or the other, or both lists are completely
invalid, the loose fit between human density and current
status, and the lack of match between two lists, each
based on sensible criteria, indicate that adding human
density as an explicit criterion might improve the use-
fulness of the current Red List, especially if the cate-
gorizations are altered to reflect the inevitable
uncertainty of the data (Akc¸ akaya et al., 2000).
At the very least, the addition of a separate criterion
of threat (measured as human density) would provide a
means to provisionally classify the current Data Defi-
cient species, so taking them out of the current vacuum
of effectively uncategorized status. More generally, the
addition, by providing an explicit measure of an
obvious component of risk, should make the assessment
of status more accurate. It should also make it more
usable, given that managers need to know why a species
is in danger before they can implement the best means
of preventing further or future decline.
While the more criteria used to assess a species’ con-
servation status, the more likely the classification is to
be accurate, there are drawbacks. More criteria means
more complexity and time in production of the list.
How might the addition of a criterion of threat most
simply and usefully be made?
The most seriously threatened species are the ones
that require the most immediate concern. These are
arguably the six species of the nine that IUCN (1996)
classified as Critically Endangered that we show to have
unusually high human densities within their geographic
range, namely Hylobates moloch (Asia), Pygathrix
avunculus (Asia), Hapalemur simus (Madagascar), and
Leontopithecus caissara,chrysopygus, and rosalia (South
America). The simplest change would simply be to
increase their status.
More generally, within each current category of Red
List status, the species facing the most threat are those
that occur in regions of higher than average human
density. The current listing could be simply refined
overall by raising the status of those species within
the current categories that experience greater than the
average human density. Callithrix kuhlii, Low Risk
according to the 1996 Red List (IUCN, 1996), dropped
from the 2000 List (IUCN, 2000), but a species with the
fifth smallest geographic range in the Americas and with
a human density in its range in the American upper
quartile (Table 1), is an example of a species whose Red
List status might need re-examination.
Human density is the measure of threat used here.
Human density is of course going to change, as will the
population size, geographic range and so on of the spe-
cies, and indeed their taxonomic status. Hence the con-
tinuous reassessment of conservation status that IUCN
conducts (IUCN, 2000). While the current threshold
criteria are absolute (e.g. more or less than a stated
threshold population size), our suggestion that species
at higher than median human density are given higher
status means the use of a relative measure. The measure
is relative in both time and space. We see no problem
with that, and indeed an advantage. The world will not
conserve all species; decisions of priority have to be
made; adding a criterion of above or below median
human density for the region (whether it be the globe or
the continent) is an explicit means of prioritization.
4.2. Problems with threat as a criterion
One problem with the use of high human density to
indicate potential risk is that Low Risk commensals,
such as the rhesus macaque, Macaca mulatta, and the
hanuman langur, Semnopithecus entellus, could achieve
high conservation status. In effect, ‘weed’ species would
be counted as threatened because of their association
with humans. However, a characteristic of most weed
species is that they have both large populations and
large geographic ranges. Thus, they should not be cate-
gorized as especially threatened. Such is the case with
the rhesus and hanuman langur.
Fig. 2. Summary comparison of log
10
human density within primate
species’ geographic ranges against the species’ IUCN Red List con-
servation status. ‘Threatened’ includes Vulnerable, Endangered, and
Critically Endangered species. Shown are medians, mean (square
symbol), interquartile range (box), and tenth percentile limits. Details
of statistical tests are given in Table 2.
146 A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149

However, one of Richard et al.’s (1989) ‘weed’ maca-
ques, Macaca sinica, appears in our High Priority list-
ing, based on human density and geographic range.
That is proper for two reasons. First, Richard et al.
debated on biological grounds whether to classify it as a
‘weed’ species. Second, and illustrative of the value of
adding threat as a criterion, the huge decline in rhesus
numbers between 1960 and 1980 (Richard et al., 1989)
demonstrates how quickly commensals can disappear.
Had human density been an explicit criterion of con-
servation status, perhaps the exploitation of this species
would have been stopped sooner, because its association
with high human density (nearly three times the median
Asian species’ average) would have flagged its Vulner-
able categorization.
A second problem with adding threat as a measure
could be agreement on the measure of threat. We have
used human density here, but the measure that best
correlates with extinction appears to vary with the
taxon considered. Thus Kerr and Currie (1995) showed
that the proportion of avian species at risk correlated
best with human density per country, but the propor-
tion of mammalian species correlated best with a
measure of economic performance of the country, gross
national product.
Nevertheless, we suggest that as a first order approx-
imation of potential risk—which is what the Red Data
Book categories are designed to indicate—human den-
sity is probably the most useful index of threat. Exten-
sive evidence indicates the damaging effects of high
human density (see Section 1), and extensive, precise,
and frequently updated data are available on human
density.
4.3. Red Lists per taxon per continent?
The Red List scheme works by categorizing all animal
species, whether a beetle or a baboon, whether from
Botswana, Brazil, or Britain, according to whether they
cross certain common thresholds of rate of population
decline, or population size, and so on. However, not
only do species differ greatly in their inherent suscept-
ibility to extinction, but continents differ in their com-
plement of taxa, as well as in many aspects of
geography, including in their overall human density
within the geographic range of primates in each con-
tinent, and in the distribution of human densities across
the four categories of conservation status (Fig. 1).
In the present analysis, Asia and Madagascar stand
out as showing, respectively, consistently the highest
and lowest human densities across the geographic extent
of the four classes of conservation status of primates
(Fig. 1). In other words, primates in Asia survive as
Low Risk at far higher human densities than is the case
for the other three continents; and they move to more
threatened conservation status at far higher thresholds
of human density than is the case for the other three
continents. If Madagascar’s threshold human density
for Threatened status were applied to Asia, only three
Asian species would be Low Risk (5%), as opposed to
the present 20 (34%). Asian primates thus appear resis-
tant by comparison with primates from the other
regions, especially Madagascar.
If these differences are real, and especially if they
apply to other taxa than primates, we need to under-
stand why they exist, and possibly refine the Red List
categorizations accordingly. At present we can com-
ment briefly on the differences, but we have no good
general explanation for them.
Extant taxa in general have been argued to be more
resistant to extinction than in the past—because only
the resistant ones have survived the past changes (e.g.
Balmford, 1996). Thus the Pacific islands with the
longest human habitation have experienced the fewest
very recent extinctions, and similarly elsewhere (Mac-
Phee and Marx, 1997; McKinney, 1997). While tropical
Asia has a far higher human population density than
does any other tropical continent (the median density in
forested nations (those that could hold primates) is over
four times the other three continents’ median densities
(data from World Resources Institute, 2000), Asia
might not have had that high density for very long. For
instance, less than a millenium ago, southern China was
perhaps at least half forested, with sufficiently undis-
turbed forest that elephant and tigers were a nuisance
(Marks, 1998); and the Malay Peninsula and especially
Indonesia did not become densely populated until late
in the eighteenth century, since when about half of the
population has been on just Java (Brookfield et al.,
1990).
The arrival of humans in Madagascar about 2000
years ago was soon followed by vegetational changes,
and a peak of extinctions (MacPhee and Marx, 1997).
Resistant species should be left. However, it is also the
case that extremely little forest remains (Harcourt and
Thornback, 1990; Mittermeier et al., 1994; Goodman
and Patterson, 1997), and current ranges of extant spe-
cies are a fraction of their former ranges (Godfrey et al.,
1999). Perhaps, therefore, it is not intensity of threat
that separates the species, for all face the same intense
threat of loss of habitat, but rather only their differing
degree of susceptibility to threat?
Inability to explain these continental differences in the
relationship between human density and status means
that the decision to apply common criteria of conserva-
tion status to all animals might be too ambitious, or
hide too much. Knowing as we do that different taxa
react differently to the same threat, that continents dif-
fer in not only intensity but general nature of threats,
perhaps taxon-by-continent measures should be used,
especially in the absence of good explanations for the
continental differences highlighted here.
A.H. Harcourt, S.A. Parks / Biological Conservation 109 (2003) 137–149 147

5. Conclusion
In conclusion, it is not just a species’ susceptibility to
threat, but also the threat itself that determines whether
a species is going to go extinct. Therefore, we suggest
that the Red List conservation status of taxa should
explicitly include measures of threat, as well as suscept-
ibility to threat. The easiest way of including threat
could be to use human density as an index, and to raise
the status of taxa found in regions of higher than med-
ian density for their continent. More generally, the
classification might be clearer and more usable if the
criteria were explicitly distinguished as, (1) threats
(human density and, perhaps, habitat loss); (2) species’
risk factors (size of population and of geographic
range); and (3) species’ response to threat (declining
population and geographic range)?
Acknowledgements
We thank Andy Purvis for providing an updated pri-
mates phylogeny coded for use by CAIC. For detailed
comments that considerably improved the paper, we
thank Monique Borgerhoff-Mulder, Tim Caro, Geor-
gina Mace, Kelly Stewart, and Truman Young (who
suggested the tripartite division of criteria listed in Sec-
tion 5).
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