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Decline of the Barbary macaque Macaca sylvanus in
the cedar forest of the Middle Atlas Mountains,
Morocco
Els van Lavieren and Serge A. Wich
Abstract The Barbary macaque Macaca sylvanus, catego-
rized as Endangered on the IUCN Red List, is the only
macaque species found outside Asia. Conservation concern
for the species arises from habitat loss, overgrazing, cutting
and collection of firewood and fodder, drought, and the
illegal pet trade. Population estimates since 1975 suggest an
overall decline. Macaques are considered economic pests
in the Middle Atlas of Morocco because they strip cedar
Cedrus atlantica bark. The Moroccan department of Eaux
et Fore
ˆts considers the stripping a serious threat to the
cedar forests and has suggested that the macaque popula-
tion is increasing. The aims of this study were therefore to
determine the current status of the macaque in the Middle
Atlas and to assess the contradictory claim that the Barbary
macaque population is increasing versus the conclusions
of a 2002 study that the population is decreasing. We
conducted 244 km of line transects from June to December
2005 in the Middle Atlas. Our results indicate densities of
12.1–28.2 km
-2
. These estimates are lower than earlier
estimates of 43–70 km
-2
and corroborate the results of the
2002 survey indicating that the macaque population is in
decline. Human-induced habitat loss and capture of infants
for the pet trade appear to be the two main factors driving
the decline. We make recommendations to mitigate these
threats.
Keywords Barbary macaque, decline, density, habitat de-
struction, livestock, Morocco.
Introduction
Once widespread throughout North Africa, the Barbary
macaque Macaca sylvanus, the only macaque species
found outside Asia, is now restricted to forest patches in
northern Morocco and Algeria. Conservation concern for
this macaque has arisen because of habitat loss from
logging, overgrazing of the forest undergrowth and regen-
erating trees by livestock, cutting and collection of firewood
and fodder, drought, and the illegal pet trade (Taub, 1975,
1977; Deag, 1977; Fa, 1984; Camperio Ciani, 1986; Menard &
Vallet, 1993; Van Lavieren, 2004,2008; Waters et al., 2007).
Conservation measures such as restricting access of grazing
animals, zonation with fencing, forest guarding and educa-
tion on sustainable use of the forest have been proposed and
partly implemented (Drucker, 1984; Taub, 1984; Camperio
Ciani et al., 2003,2005; Van Lavieren, 2004,2008). These
measures have not yet mitigated threats to the Barbary
macaque (Van Lavieren, 2004; Camperio Ciani et al., 2005)
and the species continues to decline (Camperio Ciani et al.,
2005). The species is consequently now categorized as
Endangered on the IUCN Red List (IUCN, 2008) and is
listed on CITES appendix II (CITES Trade Database Report,
2006). Estimates of Barbary macaque populations and
densities since 1975, although obtained with different meth-
odologies (Table 1), suggest an overall decline.
Macaques are considered economic pests in the Middle
Atlas because they strip and consume cedar bark. Bark-
stripping behaviour is a survival strategy when water is
scarce (Camperio Ciani et al., 2001) or when the macaques
are in search of minerals or nutrients that are otherwise
unavailable (Menard & Quarro, 1999). Because bark strip-
ping can kill young trees, increase the vulnerability of
trees to disease, and decrease timber quality and volume the
Moroccan department of Eaux et Fore
ˆts considers the strip-
ping to be a serious threat to cedar forests (Jensen, 1995;
M. Chouhani, pers. comm., 2006). Conversations in 2003
and 2004 between EvL and Eaux et Fore
ˆts officials indicated
they believed the macaque population was increasing.
The aim of the study reported here was to determine the
current status of the Barbary macaque in the central Middle
Atlas region to assess the contradictory claim that the
Barbary macaque population in the Middle Atlas is in-
creasing versus the conclusions of a 2002 study (Camperio
Ciani et al., 2005) that the population is decreasing.
Methods
The study took place in the Central Middle Atlas region of
Morocco in the regions of Fore
ˆt d’Azrou, Sidi M’Guild and
Michlife
`ne (Fig. 1). The area consists of high cedar Cedrus
atlantica forest, mixed cedar/oak (Quercus rotundifolia and
Quercus faginea) forests and pure holm oak Quercus ilex
forests. Surveys were carried out over a total of 6months
between June and December 2005, subdivided into three
2-month periods (referred to here as periods 1,2and 3). The
first period covered the birth season of Barbary macaques
and the last partly covered the breeding season.
E
LS VAN
L
AVIEREN
(corresponding author) Erfstraat 23, 6668 AD, Randwijk,
The Netherlands. E-mail elsvanlanlavieren@gmail.com
S
ERGE
A. W
ICH
Great Ape Trust of Iowa, Des Moines, Iowa, USA
Received 9April 2008. Revision requested 4June 2008.
Accepted 12 August 2008.
ª2009 Fauna & Flora International,
Oryx
, 0(0), 1–6 doi:10.1017/S0030605309990172 Printed in the United Kingdom
Line transects were used for the surveys because they are
a systematic, objective and rapid method to compare
population parameters between habitats (Buckland et al.,
2001). Transects previously established by Camperio Ciani
et al. (2001 )
AU1 were surveyed (Fig. 1): Sehb, Michlife
`ne 1and 2,
Affenourir, and Sidi M’Guild. Michlife
`ne 1was surveyed
only twice, in the first period, but not thereafter because we
discovered that shepherds had not observed macaques
there since 2004. These transects were walked at least four
times per 2-month period, in the same direction. In ad-
dition we established the transect Michlife
`ne road (Fig. 1)to
extend the area sampled. In addition to these transects we
chose 27 locations and surveyed them only once using
transects with an average length of 1km; these were added to
extend the area sampled in periods 2and 3. The sample
effort by region, period and transect are given in Table 2.
The total forested area of the three regions surveyed is
386.25 km
2
(M. Chouhani, Eaux et Fore
ˆts, pers. comm.
2005) but A. Camperio Ciani (pers. comm., 2006) believes,
after conducting several surveys in the region, that only
c. 50% of this area is suitable macaque habitat. We therefore
present our calculations of macaque densities based on this
smaller area.
All transects were walked with a Global Positioning
System (GPS) and a compass and, initially, some trees were
sprayed with a small red mark to ensure that the same
routes were followed in subsequent surveys. All transects
were walked by EvL and one of two Moroccan assistants
trained in spotting macaques.
For each macaque sighting we recorded the GPS co-
ordinates, time of day, height above ground of the first
individual observed, perpendicular distance to group cen-
tre, age and sex of all individuals, distance of first individual
to observer, distance of group centre to observer, behav-
iour, habitat type and observation duration. Estimates of
group size were possible because group sizes were relatively
small and all individuals could usually be observed. All
distances were either estimated by eye or with a measuring
tape when undergrowth prevented accurate estimation.
Prior to the surveys EvL, who estimated all distances, un-
derwent a training phase to ensure that estimated distances
corresponded to actual distances (to the nearest metre).
Every individual of each group was recorded, allowing
calculation of both group and individual densities.
FIG. 1 The study area in the Atlas mountains of Morocco,
indicating the locations of the six permanent transects (Table 2).
The shaded rectangle on the inset indicates the location of the
main map in Morocco.
TABLE 1Population and density estimates for the Barbary macaque Macaca sylvanus since 1974.
Location Population/density km
-2
Year of survey Source
Morocco 17,000 Unknown Taub (1975)
10,000 2002 Camperio Ciani et al. (2003)
6,000–10,000 Unknown Ross (2004)
5,000 A. Camperio Ciani, (pers. comm., 2006)
Middle Atlas cedar forest of Morocco 70 km
-2
1968 Deag (1974, 1984)
43 km
-2
1977 Taub (1977)
28 km
-2
1994 Camperio Ciani et al. (2005)
As low as 7–10 km
-2
2002 Camperio Ciani et al. (2005)
Global Up to 21,500 Unknown Taub (1975)
10,000–16,000 1992 Lilly & Mehlman (1993)
15,000 Unknown Von Segesser et al. (1999)
E. van Lavieren and S. A. Wich2
ª2009 Fauna & Flora International,
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, 0(0), 1–6
Transects were not surveyed during heavy rain or snow,
when observation quality would be compromised. Distance
sampling analysis followed National Research Council
(1981), Buckland et al. (2001) and Marshall et al. (2008).
Although repeat transects should in some cases be avoided
(Buckland et al., 2001) we surveyed transects more than
once because we wished to obtain repeated sightings of
groups per transect and thus more than one measure of
perpendicular distance per macaque group for each transect.
Macaque densities were calculated according to the
formula (National Research Council, 1981): d5n/(2ll),
where d5density (km
-2
), n 5total numbers of observa-
tions in the sample (individual group sightings), l5tran-
sect length (km) and l5the effective strip width to the
group centre (km), with lcalculated using Distance
4.1
(Thomas et al., 2004). Following the recommendations of
Buckland et al. (2001) data were truncated and grouped
before analysis. Up to 10% of the most distant perpendic-
ular values were considered for truncation to minimize the
influence of outliers (Buckland et al., 2001). Detection
intervals of perpendicular distances were varied to obtain
the best fit of the detection curve models; histograms were
analysed with cut-off points at 4-, 5-, 6-, 7-, 8- and 9-m
intervals. Five recommended models were used (Buckland
et al., 2001): uniform with cosine expansions, half-normal
with cosine or hermite expansions and hazard rate with
either cosine or simple polynomial expansions. Model
selection was based on Akaike’s information criterion
(AIC); the model that gave the lowest AIC value was used
to estimate l(Buckland et al., 2001). However, when
a model with the lowest AIC value also gave significant
goodness-of-fit values, the model with the second lowest
AIC value was given priority because significant goodness-
of-fit statistics may indicate that the wrong model is being
fitted to the detection histogram (Buckland et al., 2001).
Data from 47 observations were used for estimating l.
Perpendicular distance data from the various regions were
lumped because there were insufficient estimates of lper
region. To calculate the total number of macaques in the
area we calculated the average macaque density per for-
est region (Table 3) and multiplied these by 50% of the
total area.
Results
Table 2shows the number of replicates per transect, the
total transect lengths that were walked and the total num-
bers of individual macaques observed in each forest and
region, by season.
Of the various models to estimate lthe uniform plus
simple polynomial model with cut-off points at 8-m
intervals provided the best fit to the data and yielded a l
of 40.7(95% confidence interval 535.4–47.0). The v
2
value
of the goodness of fit was 4.75 (df 56,P50.576).
The density of macaques by region are given in Table 3.
Extrapolating these densities to 50% of the total surface area
of the three regions indicates that most macaques occur in
the Sidi M’Guild and Fore
ˆt d’Azrou areas, and gives an
TABLE 2Details of transects (Fig. 1) surveyed (both established transects surveyed more than once and short transects surveyed only
once) and number of macaques observed, by region and by 2-month period.
Transect (by region)
No. of replicates,
June–July
(total transect length, km)
No. of replicates,
Aug.–Sep. (total
transect length, km)
No. of replicates,
Oct.–Dec. (total transect
length, km)
Total km
surveyed
1
Fore
ˆt d’Azrou
1, Sehb 6 (36.50) 5 (28.02) 4 (24.99) 89.51
2, Affenourir 6 (10.81) 5 (6.8) 4 (5.84) 23.45
Short (n 55)
2
(9.54) (13.41) 22.95
No. macaques (km surveyed) 84 (47.31) 24 (44.36) 37 (44.24) 135.91
Sidi M’Guild
3, Sidi M’Guild 4 (13.98) 5 (14.05) 4 (11.46) 39.49
Short (n 51)
2
(4.47) 4.47
No. macaques (km surveyed) 16 (13.98) 71 (18.52) 23 (11.46) 43.96
Michlife
`ne
4, Michlife
`ne 1 2 (9.87) 0 0 9.87
5, Michlife
`ne 2 4 (13.56) 4 (13.29) 4 (13.38) 40.23
6, Michlife
`ne road 4 (7.24) 2 (6.60) 0 13.84
No. macaques (km surveyed) 48 (30.67) 70 (19.89) 7 (13.38) 63.94
Total transect length 91.96 82.77 69.08 243.81
Total no. macaques 148 165 67
1
Length of individual transects varied because in cloudy weather or heavy foliage the GPS did not always work accurately. Slight deviations from the
transect were corrected immediately but the extra distances walked due to this were added to the transect length.
2
Each of the short transects (of c. 1 km length) were walked only once.
Barbary macaque in Morocco 3
ª2009 Fauna & Flora International,
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, 0(0), 1–6
estimate of the total number of macaques in the surveyed
region of 4,126 (Table 3).
Discussion
For many wildlife species line transect sampling results
in accurate density estimates, although these methods
can produce consistent over- or underestimates for some
species (Whitesides et al., 1988). Because visual estimation
of distances could lead to overestimates (Brugie
`re & Fleury,
2000) EvL trained in estimating distances until there was
a strong correspondence between actual and estimated
distance, and therefore there were no systematic errors in
distance estimation. An additional concern is that, although
measurements of distance to a group’s centre are required,
these may only be accurate when group sizes are small and
groups are habituated (Marshall et al., 2008). Macaque
groups encountered in our study were small, which should
mitigate problems with accuracy related to group size.
Although variation in habituation might be an additional
concern for accurate group size counts, habituation was
such that groups remained where they were and locations
of individuals did not change greatly as a result of our
presence. This is probably the result of the considerable
human activity in most areas where the macaques occur.
We are unable to directly compare our results with those
of Camperio Ciani et al. (2005) because the methods used
to estimate effective strip width differed. We estimated
distance to the group centre and used Distance to de-
termine the best function to estimate l. Camperio Ciani
et al. (2005) estimated las the average distance to the first
sighting of an animal in each group, which varied for each
habitat type. Nevertheless, the two studies produced a sim-
ilar value: an average of 45 m (Camperio Ciani et al., 2005)
and 40.7m (this study).
Our calculated macaque densities of 12.1–28.2km
-2
(Table 3) are similar to those of Camperio Ciani et al.
(2005): 12 km
-2
(Fore
ˆt d’Azrou) and 20 km
-2
(Sidi M’Guild).
We estimate that the total number of macaques in the area
surveyed is c. 4,000 when the density estimates are extrap-
olated to the total area and taking into consideration that
only c. 50% of these areas contain habitat suitable for
macaques (Camperio Ciani, pers. comm.). According to
Camperio Ciani et al. (2005) only 14% of the total surveyed
area still contains intact forest, with the remaining forest
degraded or highly degraded and the latter unsuitable
habitat for macaques. The macaque densities in degraded
forest was almost half that of densities in intact forest
(Camperio Ciani & Mouna, 2007). Our transects were all
located in areas with relative high macaque densities but
densities differ substantially by region and there are areas
where macaques do not occur (Camperio Ciani et al., 2005).
Thus our extrapolation to the whole region may be an
overestimate.
Although density estimates cannot be compared di-
rectly, both our study and that of Camperio Ciani et al.
(2005) indicate much lower densities than earlier studies
(Deag, 1977; Taub, 1977; Fa, 1984). Taken together, these
results confirm that the macaque population of the Middle
Atlas is decreasing and thus rules out the contradictory
claim of an increasing population. Although our estimates
of macaque density and forest area are now several years
old, there are no more recent estimates of the area of forest
and disturbance continues, making it likely that our esti-
mates of macaque numbers are conservative.
With respect to poaching for the illegal pet trade there is
a role for both Morocco and the European Union. An
estimated 300 infant macaques are smuggled into Europe
annually (Van Lavieren, 2008). The trade needs be tackled
at the source of the problem: the relative ease with which
macaques can be purchased, the lack of control of poaching
in the forest, the open sale of macaques in markets, and the
lack of control at the border between Morocco and Spain.
The national wildlife laws and CITES regulations are in-
sufficiently enforced in Morocco and we recommend that a
sanctuary for confiscated macaques is created in the coun-
try. Any such macaques could form the basis for future
restorations or reintroductions.
TABLE 3Mean group size and density and mean individual density of Barbary macaques, effective strip width (l, with 95% confidence
interval, CI) and total length of the transect surveys (l, from Table 2), and an estimation of the total number of macaques (with 95%
confidence interval) based on the mean individual density extrapolated to 50% of the area potentially inhabitable by macaques (see
Discussion for further details).
Region (area, km
2
)
Mean
group size
Mean group
density (km
-2
)
Mean
individual
density (km
-2
)l(95% CI) l(km)
Total No. of
individuals
(95% CI)
Fore
ˆt d’Azrou (160) 5.8 2.08 12.1 0.0407 (0.0354–0.0470) 135.91 965 (835–1,123)
Sidi M’Guild (220) 9.2 3.07 28.2 0.0407 (0.0354–0.0470) 43.96 3,107 (2,692–3,613)
Michlife
`ne (6.25) 7.2 3.27 23.5 0.0407 (0.0354–0.0470) 63.94 74 (64–86)
Total (386.25) 7 2.8 21.3 0.0407 (0.0354–0.0470) 243.81 4,146 (3,591–4,821)
E. van Lavieren and S. A. Wich4
ª2009 Fauna & Flora International,
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, 0(0), 1–6
The outcome of this study was presented to Eaux et
Fore
ˆts, and a 2-year project (initiated by WWF MedPO and
AAP Sanctuary for exotic animals in The Netherlands) has
commenced that focuses on the recommendations made
here, by Van Lavieren (2008) and by Camperio Ciani &
Mouna (2007). Various actions have been recently taken to
tackle the illegal trade in Barbary macaque.
Acknowledgements
We acknowledge the support of AAP Sanctuary for exotic
animals, in particular David van Gennep, Rikkert Reijnen,
Jack Drenthe, Dana Bezdickova and Ramon Braaf. For
financial support we thank AAP, the Nationale Postcode-
loterij, Holland, and the International Primate Protection
League. For preparation of this research we thank Andrea
Camperio Ciani and Aad van den Berg. For support and
cooperation in Morocco we thank the Institut Scientifique
in Rabat, Morocco, and in particular Prof. Mohamed
Mouna. We also thank Mr Chouhani of Eaux et Fore
ˆts,
Azrou, Morocco, and Karim Ahwash for his help with
fieldwork. For help with analysis we thank Nelly Menard,
Bart van Lavieren, Leoniek Wijngaards and Anna Nekaris.
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Biographical sketches
ELS VAN LAVIEREN is founder of the Moroccan Primate Conserva-
tion foundation and specializes in the care of wild animals in captivity,
wildlife management and primatology. She spent 4years working on
Barbary macaque conservation projects with IUCN, AAP Sanctuary
for exotic animals, and the WWF Mediterranean Programme in
Morocco. SERGE A. WICH has been studying Indonesian and African
primates since 1993. He now focuses on orang-utan research and
conservation, is co-manager of research at the Ketambe Orang-utan
Research Station in Sumatra and a visiting scientist at the Great Ape
Trust of Iowa.
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