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Ecological Indicators 20 (2012) 269–276

Contents lists available at SciVerse ScienceDirect

Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Tracking the effect of climate change on ecosystem functioning using protected


areas: Africa as a case study
Nathalie Pettorelli a,∗ , Aliénor L.M. Chauvenet a,b , James P. Duffy a , William A. Cornforth a ,
Alizée Meillere a , Jonathan E.M. Baillie c
a
Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK
b
Division of Biology, Imperial College London, Silwood Park Campus, Ascot, Berkshire SL5 7PY, UK
c
Conservation Programme, Zoological Society of London, Regent’s Park, London NW1 4RY, UK

a r t i c l e i n f o a b s t r a c t

Article history: Protected areas represent important core ‘units’ for in situ conservation. However, the current static
Received 3 June 2011 system is at risk from the effects of global environmental change. This is especially true in Africa, a
Received in revised form 10 February 2012 biodiversity-rich continent expected to be hit hard by climate change. Focusing on African protected
Accepted 14 February 2012
areas that experience limited human impact (International Union for Conservation of Nature (IUCN)
categories I and II), we tested three hypotheses regarding the impact of climate change on the dynamics
Keywords:
of net primary productivity (NPP). We expected a lower annual NPP and higher seasonality in NPP in
Climate change
Eastern and Southern Africa; changes in NPP dynamics to coincide with changes in precipitation; no
National park
NDVI
correlation between changes in NPP dynamics and human development. To test these expectations, we
Primary productivity used the Normalised Difference Vegetation Index (NDVI) as an index of NPP. Results show that, between
Remote sensing 1982 and 2008, an increased vegetation greenness was observed in 27% of the protected areas monitored
(mostly in Western Africa), and an increased seasonality in 9% of them (mostly in Eastern and Southern
Africa). Our results lend support to current expectations regarding the impacts of climate change, and
demonstrate how protected areas of IUCN categories I and II could be used to track the effect of climate
change on ecosystem functioning in Africa, and possibly elsewhere. The study highlights the need for a
dynamic approach to conservation, where the relevance and efficiency of management actions need to
be regularly evaluated. It also demonstrates that satellite-based approaches offer a cheap, verifiable way
to quickly identify protected areas of concern at a global scale, supporting managers in their effort to
design and apply adaptive management strategies.
© 2012 Elsevier Ltd. All rights reserved.

1. Introduction (Ricketts et al., 2005). But PAs do not just act as a refuge for biodi-
versity. Their value also lies in protection of cultural heritage and
Protected areas (PAs) form the core of most national or regional provision of a range of socio-economic benefits; PAs can supply
biodiversity conservation strategies, with some 120,000 designated ecosystem services such as clean water, wild food, local medicines
PAs currently covering 13.9 per cent of the Earth’s land surface or genetic material; they can help mitigate the impacts of cli-
(Chape et al., 2008; Coad et al., 2009). They are renowned for their mate change through carbon capture and storage, and can act as
ability to act as refuges for species and ecological processes that a buffer against natural disasters; lastly, they can help maintain
cannot persist in intensely managed landscapes and seascapes, as microclimatic or climatic stability (IPCC, 2007; Chape et al., 2008;
well as for their ability to provide space for natural evolution and Dudley et al., 2010). Because PAs represent the cornerstone of global
potential ecological restoration (Dudley et al., 2010). In most cases, conservation efforts (Balmford et al., 2003) and provide multiple
they are the only remaining natural or semi-natural areas in whole ecosystem services to societies, monitoring their efficacy is key
regions and significant numbers of species are found nowhere else for making relevant management decisions in the face of future
environmental change (Gaston et al., 2008).
Africa contains a large proportion of the remaining world bio-
diversity (Groombridge and Jenkins, 2002; UNEP, 2006) and is
∗ Corresponding author. Tel.: +44 020 7449 6334; fax: +44 020 7586 2870.
expected to be hit hard by climate change (Hulme et al., 2001;
E-mail addresses: nathalie.pettorelli@ioz.ac.uk (N. Pettorelli),
IPCC, 2007), with changes in a variety of ecosystems already being
alienor.chauvenet@ioz.ac.uk (A.L.M. Chauvenet), james.duffy@ioz.ac.uk (J.P. Duffy),
william.cornforth@ioz.ac.uk (W.A. Cornforth), alizee.meillere@gmail.com detected (Boko et al., 2007). In such a context, PA monitoring and
(A. Meillere), jonathan.baillie@zsl.org (J.E.M. Baillie). assessment in Africa is crucial; information is required to identify

1470-160X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecolind.2012.02.014
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270 N. Pettorelli et al. / Ecological Indicators 20 (2012) 269–276

areas displaying rapid changes in their functional attributes, and greatest pressure from climate change and potentially in need of
areas that will need to be modified and/or adapted if they are to conservation interventions.
meet the challenges posed by global warming (Hannah et al., 2007).
Effectively monitoring PAs worldwide, however, involves several
2. Materials and methods
technical and financial challenges: monitoring methods need to
be inexpensive, systematic, repeatable, and verifiable. The rele-
2.1. Material
vant metrics of condition should be frequently recordable, available
over a long time-frame, comparable between PAs, as well as offer-
The NDVI is amongst the most intensely studied and
ing a rapid response that allows the early detection of impacts
commonly used vegetation indices (Pettorelli et al., 2005a,
(Alcaraz-Segura et al., 2009). Satellite imagery has the potential
2011). It is derived from the red:near-infrared reflectance ratio
to revolutionise our ability to track changes in PAs throughout the
(NDVI = (NIR − RED)/(NIR + RED), where NIR and RED are the
world, as satellite data can provide valuable information regard-
amounts of near-infrared and red light, respectively, reflected
ing changes in land use, primary productivity or phenology (Kerr
by the vegetation and captured by the sensor of the satellite;
and Ostrovsky, 2003). In particular, it has recently been proposed
Jensen, 2007). Green leaves have high visible light absorption and
that the monitoring of remotely assessed ecosystem functional
high near-infrared reflectance, resulting in NDVI values close to 1.
attributes provide a great opportunity to assess PA performance,
Senescing vegetation, soil, water, cloud and snow will have higher
whether it is in terms of evaluating the effectiveness of man-
near-infrared absorbance, thus driving NDVI values closer to −1
agement practices or tracking the effects of global environmental
(Tucker et al., 1985). For this study, we made use of the long-term
changes (Alcaraz-Segura et al., 2009; Kinyanjui, 2011).
data processed by the Global Inventory Modelling and Mapping
With this study, we aim to test hypotheses regarding the impact
Studies (GIMMS) group (Tucker et al., 2005; Tang et al., 2011). The
of climate change on the dynamics of vegetation in Africa while
spatial resolution is 8 km (pixel size is 64 km2 ) and the dataset
highlighting potential functional changes in the PA network. To
considered spanned from 1 January 1982 to 31 December 2008.
do so, we consider an important functional attribute, namely the
The data were analysed in their original bi-monthly compositing
radiation intercepted by the vegetation (Virginia and Wall, 2001).
period.
Radiation interception is the main control of carbon gains, and, thus,
PA boundaries were obtained from the World Database on Pro-
of net primary productivity (NPP), which is the most integrative
tected Areas (downloaded in February 2009), and information on
indicator of ecosystem functioning (Monteith, 1981; Virginia and
the major land cover types occurring in each PA was obtained
Wall, 2001). This attribute was indexed using the Normalised Dif-
by overlaying the PA boundaries and information on global land
ference Vegetation Index (NDVI; Wang et al., 2004). Because PAs
cover type distribution from the Global Land Cover 2000 Project
minimise land-use conversions, evaluating functional attributes in
(Fig. 1). The Global Precipitation Climatology Project (GPCP) dataset
PAs can help discern the effects of different drivers of environmen-
Version 2.1, produced monthly at 2.5◦ spatial resolution, was
tal change on ecosystem functioning (Garbulsky and Paruelo, 2004).
used for the period 1982–2008 (Herrmann et al., 2005). Human
Specifically, PAs of categories I (a and b) and II are designated to pro-
development was indexed using (1) country-level data on human
tect ecological integrity, hence, focussing on them should maximise
population growth rate and poverty level and (2) information on
our chances of solely detecting climatic signals as human impact
the level of human impact in and around each PA (using buffers;
in these areas is strictly controlled (IUCN, 1994). The following
see Section 2.2). Data on human population growth rate (trend
hypotheses were tested:
in human population growth rate over the period 1982–2008)
and poverty level (average percentage of the population living
(H1) According to reported changes and current projections (Boko
with less than US $2 a day over the period 1982–2008) for each
et al., 2007; Christensen and Hewitson, 2007), seasonal patterns in
African country considered were retrieved from the World Bank
temperature and precipitation are expected to increase in strength
(http://data.worldbank.org/indicator; downloaded in July 2010;
in Eastern and Southern Africa. This should translate into (a)
Table A1 in the Appendix). The human footprint, which is a com-
decreasing levels of vegetation greenness and (b) increasing sea-
posite of transport, night-time lights, urban areas, land cover and
sonality in vegetation greenness in PAs in these regions.
population density layers, normalised by biome (1 km resolution;
(H2) Previous studies have already reported a strong correlation
Sanderson et al., 2002; Leroux et al., 2010) was used to assess the
between vegetation dynamics as indexed using the NDVI and rain-
human impact inside and outside each PA.
fall patterns in Africa (Davenport and Nicholson, 1993; Tucker
and Nicholson, 1999; Chamaille-Jammes et al., 2006; Funk and
Brown, 2006). Therefore, changes in vegetation greenness in pro- 2.2. Methods
tected areas of categories I and II should coincide with changes in
precipitation. NDVI pixels corresponding to the PAs of categories I and II were
(H3) In theory, no resource exploitation is allowed in PAs of cate- extracted from the images of the GIMMS African subset. PAs smaller
gories I and II (IUCN, 1994), hence, changes in NPP in these PAs than the area of a single NDVI pixel were removed from the anal-
(as indexed using the NDVI) should be determined by changes ysis. This meant that out of the 263 possible PAs, only 197 were
in climatic conditions, with no correlation between the spatial considered. Based on previous work (Hartley et al., 2007), a 30 km
distribution of changes in vegetation greenness and human devel- buffer was created for each of those PAs, and their NDVI values
opment. extracted. Buffers which partially included other PAs (IUCN I–VI)
were modified leaving the unprotected areas only for analysis (i.e.,
While testing for these three hypotheses, we provide a descrip- areas of the buffer that overlap another PA were not considered).
tion of the temporal trends in the total amount of and seasonality in Buffer areas located wholly in another PA led to this buffer and its
the radiation intercepted by vegetation over the period 1982–2008. associated PA being eliminated from analysis.
The results are expected to inform the management of PAs in Africa, For each PA and its associated buffer, the average human foot-
by reporting information correlated with recent trends in NPP and print values were calculated. In addition, for each PA and each year,
seasonality across the whole network and by highlighting areas we obtained monthly precipitation data. They were interpolated to
displaying significant changes. It is also hoped that this will help a spatial resolution of 0.02◦ (about 2.2 km) using the Inversed Dis-
identify species and ecosystems in PAs that are likely to be under tance Weighted (IDW) interpolation function in ArcGIS 9.3.1. To do
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N. Pettorelli et al. / Ecological Indicators 20 (2012) 269–276 271

Fig. 1. Map of Africa detailing the major land cover types (information derived from the Global Land Cover 2000 Project) and the locations of the protected areas considered.

so, 4 neighbours and a power of 1 were considered. We chose this attributed these changes to environmental noise, because factors
interpolation method as it is most suitable for the size and nature such as water, clouds and shadow give rise to highly reduced NDVI
of the GPCP dataset (Hartkamp et al., 1999). A high spatial resolu- values (Pettorelli et al., 2005a). Once we had identified all contami-
tion was used so that it was certain each PA would contain a data nated values, they were replaced by the average of the previous and
point. The output monthly raster files were vectorised to points. following values, so as to ‘smooth’ the annual NDVI curve for that
Precipitation data were then intersected with PA boundaries and pixel. If two consecutive ‘drop’ values were present, the average of
averaged to obtain annual precipitation. Trends in precipitations the closest higher NDVI values was calculated; all pixels with 3 con-
for each PA were determined using the Mann–Kendall trend test secutive NDVI values <0 were removed (Garonna et al., 2009). PAs
(Alcaraz-Segura et al., 2010a,b). with more than 50% of their pixels removed were not considered
The next step was to correct for environmental noise (‘smooth- for further analysis.
ing’) in the NDVI data (Pettorelli et al., 2005a). The radiation Based on spatially averaged curves estimated for each PA and
reaching the satellite sensor can be contaminated by atmospheric each year, four parameters capturing important features of ecosys-
variation, and NDVI values may therefore become inexact represen- tem functioning were calculated: (1) annual maximum (MAX),
tations of the vegetation status on the ground (Tanre et al., 1992; (2) annual minimum (MIN), (3) annual integrated NDVI (NDVI-I),
Achard and Estreguil, 1995). This was performed by identifying and (4) annual relative range (RREL = [MAX − MIN]/MEAN, where
rapid changes in NDVI values (of 0.25 or more from one composite MEAN is the annual mean NDVI for the PA considered; Pettorelli
to the next) for each pixel, which were immediately followed by a et al., 2005a; Alcaraz-Segura et al., 2009). As a result, for each sin-
return to the original values or higher (Garonna et al., 2009). We gle PA, we had four datasets (one for each parameter MAX, MIN,
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272 N. Pettorelli et al. / Ecological Indicators 20 (2012) 269–276

NDVI-I, and RREL), each containing 27 values (i.e., one for each Table 1
Number of PAs (out of the 168 PAs considered) displaying significant changes in
year).
annual maximum (MAX) and minimum (MIN) NDVI, annual integrated NDVI (NDVI-
All statistical analyses were performed in the statistical package I) and annual relative range (RREL = [MAX − MIN]/MEAN, where MEAN is the annual
R (www.r-project.org). We searched for significant linear trends mean NDVI for the PA considered). Significance was assessed with Mann–Kendall
over the period 1982–2008 in each of those four datasets for each trend tests (n = 27 years, threshold values = 0.27066 for p = 0.05).
PA. Significance was assessed using the Mann–Kendall trend test Significant increase Significant decrease
(Alcaraz-Segura et al., 2010a,b). Although we performed a large
PA MAX NDVI 21 22
number of tests (n = four parameters × number of PAs), each test
MIN NDVI 41 13
was done on a unique dataset, i.e., no multiple comparisons. As NDVI-I 46 11
a result, we did not need to use any multiple testing correction RREL 15 44
method such as the Bonferroni correction. Buffer MAX NDVI 22 8
Average human footprint inside and outside PAs was compared MIN NDVI 42 11
using ANOVA. To explore correlations between temporal trends NDVI-I 47 18
in NDVI dynamics, human footprint and precipitation, we fitted RREL 15 43

a linear model, where the trend in each parameter (MIN, MAX,


NDVI-I and RREL; as estimated by the Mann–Kendall’s rank cor-
relation coefficient) was modelled as a function of the average According to (H2), changes in NPP should be driven by changes
human footprint value inside and outside each PA, as well as the in precipitation. Indeed, we found positive links between tempo-
Mann–Kendall’s rank correlation coefficient for precipitation in ral trends in precipitation and trends in MAX (slope = 0.37 ± 0.10,
each PA. To explore correlations between temporal trends in NDVI t = 3.89, p < 0.001), RREL (slope = 0.22 ± 0.12, t = 1.87, p = 0.06) and
dynamics, trend in human population growth rate (over the period NDVI-I (slope = 0.18 ± 0.13, t = 1.41, p = 0.16). Such a link was how-
1982–2008) and poverty level (percentage of the population living ever not significant when considering MIN (p = 0.93).
with less than $2 a day), we determined for each country (N = 33) Finally, in accordance with (H3), in most cases we could not
the proportion of PAs displaying significant changes in NDVI-I, MIN find any significant correlation between the proportion of PAs
and MAX. These proportions were arcsine square root-transformed (per country) displaying temporal changes in vegetation greenness
(Sokal and Rohlf, 1995) before fitting a linear model (with trend in and human development indices such as the trend in popula-
human population growth rate or log (poverty level) as factors) tion growth rate (over the period 1982–2008) or poverty level
weighed by the number of PAs for each country. (average percentage of the population living with less than US $2
a day over the period 1982–2008) (all p > 0.05). However, coun-
tries with increasing human population growth rate had a higher
proportion of PAs with significant decrease in MAX within their
3. Results boundaries (slope = 0.29 ± 0.12, t = 2.46, p = 0.02). These countries
were also associated with a smaller proportion of PAs with signifi-
Environmental noise correction led to a significant drop in the cant increases in RREL (slope = −0.25 ± 0.10, t = −2.41, p = 0.02). We
number of pixels and PAs that could be considered for analy- were unable to report any significant link between the probability
sis. Using the aforementioned selection criteria meant that only to display a negative trend in MIN or MAX and the human footprint
168 PAs (12,679 pixels) out of the original 263 PAs were put inside or outside PAs (all p > 0.15).
forward for analysis. Average PA size was 75 pixels, standard
deviation being 152 pixels. Ten of these PAs were of category I, 4. Discussion
the rest were category II. These 168 PAs covered 33 countries
(Fig. 1). Average NPP as indexed by NDVI-I over the 27 years This study addressed the role of PAs as reference areas to eval-
considered varied greatly across PAs, with average NDVI-I values uate the impact of global change on natural ecosystems. The focus
ranging from 1.5 in Elba National Park (NP, Egypt) to 18.78 in was on PAs in Africa, since this continent offers an adequate sce-
Tsaratanana NP (Madagascar). Likewise, the annual relative range, nario in relation to: (a) the number of PAs; (b) the availability of
which constitutes a normalised descriptor of seasonality, ranged regional evaluations of the impact of climate change and human
from 0.24 in Tassili N’Ajjer NP (Algeria) to 1.50 in Dinder NP pressure, and (c) the high diversity of ecosystems where to test
(Sudan). Trends in MIN, MAX, NDVI-I and RREL from pixels within the proposed hypotheses. In general, our predictions were met, as
the PAs were highly correlated to trends in these parameters in (1) we reported a trend towards lower annual NPP (as indexed
pixels from associated buffers (MIN: slope = 0.85 ± 0.04, R2 = 0.73, using NDVI-I) and higher seasonality (as indexed using RREL) in
p < 0.001; MAX: slope = 0.83 ± 0.06, R2 = 0.57, p < 0.001; NDVI-I: Eastern and Southern Africa; (2) we demonstrated a link between
slope = 0.79 ± 0.04, R2 = 0.71, p < 0.001; RREL: slope = 0.86 ± 0.04, changes in rainfall and changes in vegetation greenness across
R2 = 0.74, p < 0.001). However, the average human footprint index the continent; (3) in most cases we could not report any signif-
was significantly higher outside PAs than inside PAs (F1,334 = 5.54, icant correlation between the spatial distribution of significant
p = 0.02). changes in vegetation greenness dynamics and human develop-
Forty-six out of the 168 PAs considered displayed a significant ment or poverty levels. Our last prediction (namely, that changes
increase in average NDVI-I, as opposed to 11 that displayed a sig- in NPP dynamics in PAs of categories I and II should be solely deter-
nificant decrease (Table 1). Three of the 46 PAs were of category I, mined by changes in climate) was based on the assumption that PAs
and 1 out of the 11 PAs displaying a significant decrease in NDVI- of categories I and II are described as being mostly, if not totally,
I belonged to that same category. In accordance with (H1a), the protected from direct human impact, e.g., illegal logging, graz-
11 PAs displaying a significant decrease in NDVI-I were primarily ing, or agriculture. This was a reasonable assumption considering
located in Eastern and Southern Africa (Fig. 2). Fifteen PAs displayed that those PAs encompass strict nature reserves, wilderness areas
a significant increase in average seasonality (none of them being of or NPs, with natural, unmodified habitat where human impact is
category I), while 44 PAs (5 of them being of category I) showed strictly controlled (IUCN, 1994). Contrary to expectations, however,
a significant decrease in average seasonality. In accordance with countries with increasing human population growth rate were
(H1b), most of the PAs displaying an increased seasonality were associated with a higher proportion of PAs with significant decrease
located in Eastern and Southern Africa (Fig. 3). in the level of maximum vegetation greenness. This might indicate
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N. Pettorelli et al. / Ecological Indicators 20 (2012) 269–276 273

Fig. 2. Spatial distribution of the protected areas displaying a significant increase in the satellite-based index of annual net primary productivity (NDVI-I) and a significant
decrease in NDVI-I.

that some PAs of categories I and II are subjected to some levels monitoring approaches based on NDVI, namely that they cannot
of human pressure and human exploitation, potentially interfering help remotely identify the main factors (e.g., climate, soil quality,
with the link between climate and NDVI dynamics in these areas. megaherbivore density, illegal activities) locally driving changes in
Interestingly, several trends reported at the individual PA scale NPP dynamics.
also corroborate results from previous local assessments: for exam- Other limitations are linked to the nature of the NDVI: this
ple, our approach highlighted (a) an increased seasonality and a satellite-based index is a crude estimate of vegetation health
reduced annual NPP in the Serengeti and Masai Mara NPs, which is (Goward and Prince, 1995), and its ability to monitor variation in
supported by recent assessment of the ecosystem (where increased NPP can sometimes be reduced (Markon and Peterson, 2002). In
fire occurrence and an increased elephant population have been tropical ecosystems, the radiation reaching the satellite sensor can
suggested to correlate with a decreased tree coverage; Sinclair be contaminated by atmospheric variations such as cloud cover and
et al., 2008); (b) degrading conditions in Mweru-Wantipa NP where smoke, and NDVI values may become inexact representations of the
the reported increased seasonality and a reduced annual NPP vegetation status on the ground (Achard and Estreguil, 1995). NDVI
also matches reports of human encroachment and forest clear- is moreover known to have only a weak ability to detect NPP varia-
ing activities in the park (Almond, 2000); (c) degrading conditions tion in very dense canopies, as the linear correlation between NDVI
in Rwanda, a country where civil war in the nineties is known to and the leaf area index (LAI) does not hold in very densely vegetated
have had an ecological impact on PAs (see e.g., Havugimana, 2009). areas (Huete, 1988; Pettorelli et al., 2005a). It can also be expected
This set of local examples illustrates a possible shortcoming of PA that the likelihood to detect a trend in NDVI dynamics is influenced
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274 N. Pettorelli et al. / Ecological Indicators 20 (2012) 269–276

Fig. 3. Spatial distribution of the protected areas displaying a significant increase in the satellite-based index of annual seasonality (annual relative range, RREL) and a
significant decrease in seasonality.

by the level of variability in climatic conditions, although this was changes in NPP has been shown to correlate with animal move-
not the case in our study (no significant correlation between the ment, distribution and performance (Pettorelli et al., 2005a,b;
coefficient of variation in rainfall and the likelihood of picking up Boone et al., 2006; Bro-Jørgensen et al., 2008). Based on these
a trend in MIN, MAX, NDVI-I and RREL). Altogether, such limita- studies, it can be safely assumed that reduced annual NPP or
tions could have hampered our ability to detect changes in NPP increased seasonality in NPP (as indexed using the NDVI) are likely
dynamics in areas with high vegetation cover, low climatic variabil- to affect animal biodiversity. The possible mechanisms by which
ity and high cloud cover (see Fig. 1A in the Appendix), highlighting such changes can impact biodiversity are varied, depending on the
the importance of considering NDVI-based approaches as being a species under study, ranging from affecting the temporal match
component of a possible monitoring framework for PAs at a global between resource availability and breeding season or arrival of
scale. migrant species (Durant et al., 2005), to affecting carrying capac-
Several studies conducted at various spatial scales and in vari- ity (Pettorelli et al., 2009). Although reduced vegetation greenness
ous types of environment have now linked NDVI-based estimates can be expected to negatively impact animal biodiversity, increased
of NPP to wildlife distribution and abundance (see recent reviews vegetation greenness cannot be systematically expected to posi-
in Pettorelli et al., 2009, 2011). Likewise, information on temporal tively impact animal biodiversity. For example, while NPP might
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N. Pettorelli et al. / Ecological Indicators 20 (2012) 269–276 275

have increased in PAs across Western Africa, highlighting, among Appendix A. Supplementary data
other things, a possible change in precipitation regime (IPCC, 2007;
our results) or a positive effect of management actions in this part Supplementary data associated with this article can be found, in
of the continent, such a result precludes providing any generaliza- the online version, at doi:10.1016/j.ecolind.2012.02.014.
tion about PA management efficiency when it comes to preventing
biodiversity loss (Redford, 1992; Craigie et al., 2010). References
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