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Restating the Case for a Sharp Population Decline in Lemur catta

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Abstract

As with many other species in the primate order, ring-tailed lemurs (Lemur catta) are threatened with extinction. Our articles documented declines in wild ring-tailed lemur populations and noted that fewer than 2,500 wild ring-tailed lemurs are known to persist in 32 [Gould and Sauther: Primate Conservation 2016; 30: 89-101] and 34 [LaFleur et al.: Folia Primatologica 2017; 87: 320-330] sites. A criticism of our articles [Murphy et al.: International Journal of Primatology 2017; 38: 623-628] suggested that we have inadequately sampled ring-tailed lemur populations and habitats, and misused the literature. We disagree, and provide both a detailed rebuttal and responses to specific critique points herein. Moreover, we restate our case outlining a dramatic decline of ring-tailed lemurs resulting from anthropogenic pressures (deforestation, severe habitat fragmentation, extraction for the pet and bushmeat trades). We pose several thought-provoking questions as to when is the appropriate time for researchers to "sound the alarm" about a species' decline, and remain committed to understanding the drivers of unsustainable exploitation of this emblematic lemur, and preventing their extinction in the wild.
Short Communication
Folia Primatol 2018;89:295–304
DOI: 10.1159/000489676
Restating the Case for a Sharp Population
Decline in Lemur catta
Marni LaFleur a Lisa Gould b Michelle Sauther c Tara Clarke d
Kim Reuter e
a Department of Anthropology, University of California San Diego, La Jolla, CA, USA;
b Department of Anthropology, University of Victoria, Victoria, BC, Canada; c Department
of Anthropology, University of Colorado Boulder, Boulder, CO, USA; d Evolutionary
Anthropology Department, Duke University, Durham, NC, USA; e Africa Field Division,
Conservation International, Gaborone, Botswana
Keywords
Ring-tailed lemur · Conservation · Population decline · Madagascar · Extirpation ·
Extinction
Abstract
As with many other species in the primate order, ring-tailed lemurs (Lemur catta)
are threatened with extinction. Our articles documented declines in wild ring-tailed le-
mur populations and noted that fewer than 2,500 wild ring-tailed lemurs are known to
persist in 32 [Gould and Sauther: Primate Conservation 2016; 30: 89–101] and 34 [LaFleur
et al.: Folia Primatologica 2017; 87: 320–330] sites. A criticism of our articles [Murphy et al.:
International Journal of Primatology 2017; 38: 623–628] suggested that we have inade-
quately sampled ring-tailed lemur populations and habitats, and misused the literature.
We disagree, and provide both a detailed rebuttal and responses to specific critique
points herein. Moreover, we restate our case outlining a dramatic decline of ring-tailed
lemurs resulting from anthropogenic pressures (deforestation, severe habitat fragmen-
tation, extraction for the pet and bushmeat trades). We pose several thought-provoking
questions as to when is the appropriate time for researchers to “sound the alarm” about
a species’ decline, and remain committed to understanding the drivers of unsustainable
exploitation of this emblematic lemur, and preventing their extinction in the wild.
© 2018 S. Karger AG, Basel
Received: September 19, 2017
Accepted after revision: April 26, 2018
Published online: July 25, 2018
Marni LaFleur
9500 Gilman Dr.
La Jolla, CA 92122 (USA)
E-Mail marni.lafleur @ gmail.com
© 2018 S. Karger AG, Basel
www.karger.com/fpr
E-Mail karger@karger.com
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Introduction
In two published articles [Gould and Sauther, 2016; LaFleur et al., 2017], we used
published and novel data to tally the numbers of ring-tailed lemurs (Lemur catta)
within multiple localities at 32 and 34 sites, respectively, in regions where they persist
within southern Madagascar. Our objective was to provide a snapshot of population
trends and threats to this endangered species [Andriaholinirina et al., 2014] and to
tally the number of individuals remaining in the locations for which data exist. Our
implicit assumptions were that a large proportion of the remaining wild ring-tailed
lemurs were found within these sites, and that the ring-tailed lemur habitat is becom-
ing increasingly fragmented. We also argued that many populations of L. catta
throughout this species’ geographic range are in rapid decline or have become lo-
cally extirpated due to habitat destruction (decline of lemurs [Sussman et al., 2003;
Kelley et al., 2007], habitat decline [Brinkmann et al., 2014]), hunting [Goodman,
2003; Moniac and Heitmann, 2007; Siers, 2007; Gardner and Davies, 2014], and live
capture [LaFleur et al., 2015; Reuter and Schaefer, 2016; LaFleur et al., in prep.].
Murphy et al. [2017] presented several serious accusations in claiming that we
have inadequately sampled ring-tailed lemur populations and habitats, and misused
the literature. We respond to each of their allegations here. Furthermore, we raise
several points with respect to the future of conserving primate species and preventing
extinctions.
Both of our previous articles used count data to sum the total number of known
ring-tailed lemurs remaining at the locations described. These methods do not ac-
count for all lemurs existing in the locations, but only those that have been counted,
and thus underestimate the total number of individuals that exist, as we stated
[Gould and Sauther, 2016; LaFleur et al., 2017] and our critics pointed out [Murphy
et al., 2017]. We have not extrapolated count data to estimate the total number of
ring-tailed lemurs present because (a) extrapolations are not appropriate when ex-
traction pressures are present [see Sussman et al., 2006] and (b) extraction pressures
are now known in approximately 44% of the locations outlined.
Extrapolations are not appropriate in areas where animals are being harvested.
Zombitse-Vohibasia National Park is a largely intact forest parcel of 368.52 km2, and
part of the historical range of L. catta [Goodman et al., 2006]. If we were to estimate
how many ring-tailed lemurs are present in this park, based on known densities for
ring-tailed lemurs in dry spiny and mixed gallery forest (90 individuals/km2 [Suss-
man, 1991]; 100–500 individuals/km2 [Jolly et al., 2006]), our estimate would range
between 33,165 and 184,250 animals for this area. However, the lemurs in the Zom-
bitse-Vohibasia National Park have been subject to significant hunting pressure, and
in 2005, only one ring-tailed lemur was seen after 150 km of transect walks [Siers,
2007]. Moreover, in 2016, MNP (Madagascar National Park) officials released park
inventory records to M.L. and T.C. noting a total of 10 individual ring-tailed lemurs
within Zombitse-Vohibasia. Similar hypothetical examples, wherein large numbers
of ring-tailed lemurs could be erroneously estimated within “empty forest” locations,
despite evidence of significant decline due to hunting pressure, could also be made
for Kirindy Mitea, Mikea, and Ranobe-PK32. In fact, of the 32 locations outlined in
LaFleur et al. [2017], nearly 33% had “known exploitation pressures” such as hunting
or wild capture. Recent preliminary genetic data [LaFleur et al., unpublished data]
and personal communications also suggest that animals are being extracted from
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Isalo National Park (INP) and Tsimanampesotse National Park (TNP), respectively,
for the illegal pet trade. Moreover, a fire at INP in November 2017 resulted in deaths
of some of the ring-tailed lemurs (communication from anonymous reviewer).
Neither INP or TNP were listed as locations with “known exploitation pressures”
[LaFleur et al., 2017], as these were not known at the time of publication, but further
illustrate the point that ring-tailed lemur populations are declining and individuals
are being extracted throughout much of their habitat (44% of the 32 locations out-
lined by LaFleur et al. [2017]), which makes extrapolations or modelling based on
density ranges in unaffected habitats invalid.
In addition to the number of individuals, based on count data, we also outline
areas where ring-tailed lemurs have gone “locally extinct” (no evidence that animals
persist) or are “near locally extinct” (10 animals or fewer known), where they were
previously present [LaFleur et al., 2017]. These designations apply to 11 of the 32 lo-
cations and likely represent a significant decrease in the range that ring-tailed lemurs
occupy in southern Madagascar, when compared to their historical range [Goodman
et al., 2006] (Fig.1).
16012080400 200 km
Records of Lemur catta
Provinces
Protected areas
Historical range
Cities
Legend: historical range
Current rangeHistorical range
Extinct
Locally or near locally extinct
Present
Provinces
Protected areas
Cities
Legend: current range
Fianarantsona Fianarantsona
Toliary
Toliary
Toliara
Tolanaro Tolanaro
Toliara
Tolanaro
Toliary
Antananarivo
Toamasina
Mahajanga
Antsiranana
Morondava
Toliara
a b
Fig. 1. Historical range (a) and estimated current range (b) for ring-tailed lemurs, including areas
where populations are present, locally extinct, or likely or near locally extinct. a Data are from
Goodman et al. [2006] and Andriaholinirina et al. [2014]. b References are from Table 1 in
LaFleur et al. [2017]. Reproduced with permission.
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Furthermore, ring-tailed lemur populations at 15 of the 34 sites reported by
Gould and Sauther [2016] were categorized as “precarious” or “likely extirpated.”
These designations are based on counts from sites containing only few ring-tailed le-
murs remaining (e.g., 15 or fewer individuals, and in 5 cases, between 1 and 8 indi-
viduals) and/or sites where heavy hunting pressure has been reported and where ring-
tailed lemurs have not been observed for several years. Gould and Sauther [2016] also
illustrate the decreased geographic range of L. catta, and note sites where Goodman
et al. [2006; pp 93–95, Fig.4–7] had indicated geographic boundaries, but where an-
imals are no longer found.
In sum, there is ample evidence that ring-tailed lemurs have declined dramati-
cally within the sampled locations. Count data were used, as extrapolations are large-
ly invalid due to animal extractions. Not all animals present were counted, as noted
in our publications [Gould and Sauther, 2016; LaFleur et al., 2017], but the trend of
dramatic declines of ring-tailed lemurs are clear.
Murphy et al. [2017] provided a list of 45 “known localities” (with 53 citations)
where ring-tailed lemurs persist that they claimed were not included in our articles,
and use this as evidence to suggest we have inadequately sampled ring-tailed lemur
populations. Of the 53 citations, many (n = 21) are unpublished “personal observa-
tions” made solely by the co-authors (Gardner, Ferguson), of which there were no
observation dates or data included (Table 1; see online Supplement 1; for all online
suppl. material, see www.karger.com/doi/10.1159/000489676). Moreover, many
(n = 11) of the other citations were from unpublished student reports or “gray lit-
erature” that span up to 14 years prior to the present. Without being published, it
is impossible for us to know about these potential localities. Furthermore, personal
observations and unpublished reports are not publicly accessible, have not with-
stood the scrutiny of peer review, and in some cases, are likely outdated as local
environmental conditions have changed dramatically in the last decade or more.
Recently collected, readily available, and, ideally, published data regarding popula-
tion sizes or densities (and area of habitat) of L. catta are necessary for any designa-
tion to be made regarding the conservation status of this species. The IUCN docu-
mentation standards relating to species assessments state that “current population
trend” refers to trends over a period of ca. 3 years around the present [IUCN, 2013,
p. 21]. Whenever possible, we adhered to criteria including the most recent infor-
mation available.
Table 1. Categorizing the “known localities” cited by Murphy et al. [2017]
Category n%
Unpublished personal observations with no date or data 23 43
Unpublished report: gray literature 11 21
No count data on ring-tailed lemurs 10 19
Included in our article(s) 7 13
No information about this location located in citation 1 2
Refers to illegal lemur pets 1 2
Total 53 100
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Additional “known localities” pointed out by Murphy et al. [2017] are also prob-
lematic. The first entry in their table [Ganzhorn and Randriamanalina, 2004] referred
to pet ring-tailed lemurs; one offered for sale to researchers at camp and another in a
nearby village. A further 3 of the authors’ personal observations referred to lemurs in
village settings, which were also likely pets. Their last entry [Gardener et al., 2008]
listed L. catta as present at Ankodida (Table 1) without further reference to the spe-
cies in the article. To tally the number of remaining ring-tailed lemurs, and under-
stand declines and local extirpations, recently collected quantitative population in-
formation is imperative.
Our tallies suggested that fewer than 2,500 individual ring-tailed lemurs [Gould
and Sauther, 2016; LaFleur et al., 2017] are known to persist within the sampled loca-
tions. We recognize here and stated in our publications that not all ring-tailed lemur
habitats have been sampled, nor have all ring-tailed lemurs been counted within some
of the included habitats; however, exact counts were made at a number of these sites.
Much of the data included in our papers focused on very recent or relatively recent
population counts and estimates (i.e., 2010–2016) to reflect the current or near-cur-
rent status of the populations covered. Applying such criteria is important, because
declines in forest cover or animal abundances can occur rapidly. For example, Brink-
mann et al. [2014] noted a strong decline in forest cover in a region of Madagascar’s
southwest (within the population distribution of L. catta) between 2001 and 2006,
and a threefold increase in savannization and severe fragmentation in the southwest
between 1973 and 2013. In some instances, such as that with Kirindy Mitea, we have
relied on some of the older scientific literature [e.g., Goodman, 2003] in conjunction
with knowledge of local people and researchers, and our own well-documented ob-
servations, to build a case for the likely status of ring-tailed lemurs within certain re-
gions. To illustrate, ring-tailed lemurs historically ranged in the region of Kirindy
Mitea [Goodman et al., 2006], although in 2003 Goodman reported certain areas were
remarkably devoid of diurnal lemurs due to persistent hunting pressure. LaFleur et
al. [2017] visited other protected and unprotected areas of Kirindy Mitea and found
no evidence of ring-tailed lemurs (no visual sightings, calls, footprints, scat, spur/
gouge marks, food trash) during rapid assessment surveys, but did find multiple de-
caying meat drying racks and fire pits within forested locations and were candidly
told by numerous local people and park officials (in several office locations) that ring-
tailed lemurs no longer ranged there because they were hunted out, using slingshots
and dogs. This statement does not mean that there are no ring-tailed lemurs remain-
ing in Kirindy Mitea. Certainly primates, including lemurs, can adapt their behaviors
and become extremely cryptic in response to heavy predation pressure [Standford,
2002], which can make their detection difficult [Williamson and Feistner, 2003].
However, the dearth of evidence here, including our personal extensive expertise in
detecting these animals and signs that they persist in an area, and inability to identify
any signs of ring-tailed lemurs at identified former sleeping sites and home ranges
[LaFleur et al., 2017], suggested that heavy hunting pressure may have led to localized
extirpation, and that further extensive surveys with rigorous methods may not be
fruitful here. In fact, the last confirmed sighting of L. catta at Kirindy Mitea occurred
in 2012 and only 2 individuals were observed [R. Lewis, pers. commun., in Gould and
Sauther, 2016]. Thus, the trend remains: ring-tailed lemurs have experienced signifi-
cant range reductions and populations have been extirpated. These trends are not
sustainable and threaten the wild existence of the species in all but a few very well-
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protected areas (e.g., Berenty Private Reserve, Anja Community Reserve and Bezà
Mahafaly).
To summarize, many of the “known locations” suggested by Murphy et al. [2017]
are problematic as evidence for assessing the presence of wild populations of ring-
tailed lemurs, as they simply noted that a ring-tailed lemur or lemurs exist (or did
exist) outside the areas that we surveyed, something that our articles [Gould and Sau-
ther, 2016; LaFleur et al., 2017] already acknowledged.
Murphy et al. [2017] suggested that we have misused literature in several in-
stances. We detail our responses to each claim in what follows.
Gardner et al. [2009]
Both LaFleur et al. [2017] and Gould and Sauther [2016] cited Gardner et al.
[2009] among other authors [Gardner and Davies, 2014] to build a case that ring-
tailed lemurs have likely been extirpated from the region of PK-32-Ranobe over a
period of about three decades. Gardner et al. [2009] noted 4 individual L. catta in the
entire PK-32 area (although they pointed out that this small number of observations
does not constitute extirpation); however, according to the criteria of LaFleur et al.
[2017] and Gould and Sauther [2016], 4 individuals means, essentially, locally or near
locally extinct. Furthermore, Gardner and Davies [2014, p. 10, Table 1] stated that the
species “no longer exists” in the PK-32 area.
Gould and Sauther [2016] further cited Gardner et al. [2009] along with two
other references, in relation to threatened and extirpated populations of ring-tailed
lemurs along the west coast, and again, along with three further references, in relation
to the Toliara Sands mining project, where we noted “This project will have major
negative impacts on local people and wildlife, including the potential destruction of
sacred forests, heightened exposure to radiation from mine tailings, and the destruc-
tion of vast areas of forest [Gardner et al., 2009; Environmental Justice Atlas, 2015,
Lemur Conservation Network, 2015; Huff 2016].” The information included here was
taken from the listed references.
Semel and Ferguson [2013]
The information regarding ring-tailed lemurs at the Ifotaka Community Forest,
reported in Gould and Sauther [2016, p. 96], was obtained directly from Semel and
Ferguson [2013, p. 5]: “One group of approximately 15 individuals was repeatedly
observed sleeping on the cliff face on the south side of the river, opposite the camp
(Fig.1; Site 2). Two other troops also were observed to use vertical cliff faces as sleep-
ing sites on several occasions.” Further information on the situation in this area, that
dogs often chased the lemurs and that work was halted in 2013 due to a serious threat
by cattle thieves, was obtained from a personal communication between Semel and
Gould in 2016. We saw no reason to exclude this information because the aim of the
original study [Semel and Ferguson, 2013] was to characterize cliff use by the lemurs,
as is implied by Murphy et al. [2017].
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Irwin [2005]
LaFleur et al. [2017] cited both Irwin et al., 2004 and 2005 with the footnote stat-
ing the data are used as negative evidence. This citation was done on the advice of one
of the papers’ co-authors [pers. commun., P. Wright] to demonstrate that the animals
are at least very rare at these sites. We had in fact included Pic d’Ivohibe in our refer-
ence to Irwin et al. [2004].
Moniac and Heitmann [2007]
The LaFleur et al. [2017] reference to Moniac and Heitmann [2007] was an error
and should have referred to one of the two references cited within that article, name-
ly: Raharivololona BM, Ranaivosoa V (2000). Suivi écologique des Lémuriens diurnes
dans le Parc National d’Andohahela à Fort Dauphin. Lemur News 5: 8–11.
Conclusions
Generally, we find that Murphy et al. [2017] cannot “see the forest for the
trees.” Murphy et al. [2017] agreed with us that “there is ample evidence that the
ring-tailed lemur has suffered population declines, local extinctions, and an overall
range contraction in recent decades.” They then, however, listed several reasons as
to why we should not be concerned by this decline. They suggested that the species
is found in numerous protected areas, but listed areas where ring-tailed lemurs have
likely been extirpated (e.g., Kirindy-Mitea, Mikea, and Ranobe-PK32), and sug-
gested that ring-tailed lemurs are largely protected by cultural norms (fady/faly)
that prevent the consumption of this species by people. We disagree and suggested
that it is naïve to believe that fady/faly are completely effective, even in protected
areas. For example, Moniac and Heitmann [2007] document a fire pit filled with
ring-tailed lemur remains on the boundary of Andohahela, and in 2013, Youssouf
and Sauther observed remains of a ring-tailed lemur at Bezà Mahafaly, which had
been intentionally killed for food by a newly arrived outsider to the region. Ongo-
ing human migration in Madagascar results in influxes of people who do not share
local traditions against lemur consumption and forest use [e.g., Kelley et al., 2007].
Furthermore, such fady cannot mitigate ongoing powerful threats such as defores-
tation, droughts, economic instability, and famines, all of which lead to reduced
populations of L. catta. Additionally, ring-tailed lemurs are the number one most
reported pet lemur in Madagascar [Reuter and Schaefer, 2016], all of which are
wild-captured. There is no evidence to suggest that fady protects lemurs from live
capture for the pet trade.
In a separate online post, Murphy [2017] condemned our research for lacking
rigor without providing sufficient counter-evidence or having any experience with
ring-tailed lemur ecology. Additionally, Ferguson (one of the Murphy et al. [2017]
co-authors) was quoted as saying that “zero conservation funding should be allocated
to ring-tailed lemur conservation” [Reed, 2017]. We disagree with these authors’
views on the gravity of the well-documented declines of ring-tailed lemurs, and point
out that the community of primate scientists also disagree; ring-tailed lemurs have
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been included in the IUCN Primate Specialists Group’s listing of the World’s 25 Most
Endangered Primates for 2016–2018 [Schwitzer et al., 2017].
The puzzling sentiments from Murphy et al. [2017], Murphy [2017], and Fer-
guson [Reed, 2017] raise several important questions. At what point in a species’
decline is conservation warranted? After continued species’ decline, including
marked unsustainable extraction and large localized extirpations, should we not
raise the alarm? When is Endangered sufficiently endangered? And perhaps most
importantly, what contributions are being made to further scientific knowledge or
conserve a species?
Nonhuman primates are experiencing significant declines globally as a result of
anthropogenic pressures [Estrada et al., 2017]. The decline of primates negatively
impacts many of the ecosystems where they persist [e.g., Caughlin et al., 2015], and
also likely negatively impacts revenue potential in primate ecotourism locations such
as Madagascar [see Schwitzer et al., 2014]. Moreover, primates inhabiting highly
fragmented habitats may be unable to disperse and genetic bottlenecks may occur in
small populations [Frankel, 1974], which threatens their ability to adapt to new pres-
sures, including climate change. Ring-tailed lemurs, an endangered and iconic spe-
cies of Madagascar, have experienced significant declines to their range and popula-
tions [Sussman et al., 2006; Kelley et al., 2007; Gould and Andrianomena, 2015;
Gould and Sauther, 2016; LaFleur et al., 2017]. These declines have been observed,
recorded and documented by those who conduct in-depth and long-term studies of
this species.
More research addressing ring-tailed lemur presence/absence and abundance
are needed to understand how many individuals and viable populations remain in the
wild. Since the publication of LaFleur et al. [2017] and Gould and Sauther [2016], we
have learned of two new populations of ring-tailed lemurs. The first is an unusual
discovery of rainforest-dwelling ring-tailed lemurs that total 40 individuals from four
groups [P. Wright, pers. commun.]. Studies to examine the ecology of these lemurs
and their “lost forest” habitat are underway [P. Wright, pers. commun.; G. Buono,
pers. commun.]. The location is not currently legally protected and at risk of fire due
to slash-and-burn (tavy) agricultural practices. The Rainforest Trust is working to-
wards protection of this habitat and has built several fire breaks. Additionally, resi-
dents have indicated interest in protecting this forest, and will be working with the
Malagasy association MICET to help realize this goal. There are also plans to recruit
20 residents to train as forest rangers [Rainforest Trust, 2017]. The second population
of ring-tailed lemurs is at Amoron’i Onilahy, a small gallery forest pocket on the
northern edge of the Onilahy River. A census team from WWF Madagascar in early
2017 counted 197 ring-tailed lemurs. The habitat is managed by local communities
and suffers from high levels of wood extraction for charcoal production. The com-
munity is motivated to protect the unhabituated ring-tailed lemurs, as they would like
to develop ecotourism as a source of revenue; however, hunting of ring-tailed lemurs
is reported from this area and thus habituation may be difficult and unethical. We
remain guardedly optimistic about these “discoveries;” more lemurs in new locations
is good news, but the populations are isolated, facing deforestation threat, and in the
case of the “lost forest” are in unprotected habitat.
Urgent conservation efforts to prevent even more local extinctions of these
threatened primates is of paramount importance, as is further research on presence/
absence and abundance of ring-tailed lemurs remaining in the wild. We remain com-
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mitted to both scientific research and conservation actions specific to ring-tailed le-
murs and their habitats, and after witnessing their rapid declines first hand, we know
that now is the time to act if we are to save the iconic ring-tailed lemur in the wild.
Acknowledgements
We wish to thank the journal editor, Prof. Anna Nekaris, for her support and feedback. We
also thank the anonymous reviewers for their insight and for strengthening this article.
Disclosure Statement
We have no conflict of interests to declare.
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... The ring-tailed lemur (Lemur catta) is Endangered [Andriaholinirina et al., 2014], despite being Madagascar's best known and studied species, and is the most commonly reported lemur in illegal captivity [LaFleur et al., 2015;Reuter and Schaefer, 2016a, b]. Estimates from the years 2016 and 2017 indicate that sharp and continued declines threaten L. catta populations [Gould and Sauther, 2016;LaFleur et al., 2017LaFleur et al., , 2018; but see Murphy et al., 2017]. L. catta face many of the same threats as all other lemurs and have suffered localized extirpation for bushmeat hunting [Gardner and Davies, 2014], extraction for the pet trade [Andriaholinirina et al., 2014;LaFleur et al., 2015;Reuter and Schaefer, 2016], and continued and rapid habitat loss particularly in the southernmost dry forests of Madagascar [Brinkmann et al., 2014]. ...
... L. catta face many of the same threats as all other lemurs and have suffered localized extirpation for bushmeat hunting [Gardner and Davies, 2014], extraction for the pet trade [Andriaholinirina et al., 2014;LaFleur et al., 2015;Reuter and Schaefer, 2016], and continued and rapid habitat loss particularly in the southernmost dry forests of Madagascar [Brinkmann et al., 2014]. These have taken a significant cumulative toll on abundance and distribution of L. catta [Goodman and Raselimanana, 2003;Sussman et al., 2006;Kelley et al., 2007;Gould and Sauther, 2016;LaFleur et al., 2017LaFleur et al., , 2018; but see Murphy et al., 2017]. ...
... Results obtained with transition matrix data report that the extraction rates documented here (i.e., 184 individuals between 2011 and 2016) are not likely to impact remaining L. catta; however, there are a number of additional factors that must be considered that are likely to falsify these interpretations. First, although there are thought to be several thousand L. catta remaining in the wild, populations are patchily distributed and isolated from one another [Gould and Sauther, 2016;LaFleur et al., 2017LaFleur et al., , 2018Murphy et al., 2017). In fact, we only know of seven locations where there are more than 100 individuals, and one location where there are more than 500 individuals (LaFleur et al., 2018). ...
Article
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Lemur catta is the most reported illegal captive lemur. We document 286 L. catta that were held in illegal captive conditions in Madagascar. Coastal tourist destinations are “hot spots” for sightings. Many of the L. catta reported were in businesses (49%) and were perceived to be held captive for the purpose of generating income (41%). Infant/juvenile L. catta were overwhelmingly observed annually in December (41%) and may suffer high mortality rates given that they are not weaned during this month of the year. Population growth modeling suggests that known capture rates may be sustainable in all but small populations of 500 individuals and when infants/juveniles are targeted. However, of the seven remaining populations of L. cattawith more than 100 individuals, only one is known to contain more than 500 animals, and we present evidence here that infants/juveniles are targeted. Moreover L. catta face significant other threats including habitat loss, bushmeat hunting, and climate change. Several actions could reduce the illegal capture and ownership of L. catta in Madagascar such as tourist behavior change initiatives, enforcement of laws, and alternative livelihoods for local people. These interventions are urgently needed and could be adapted to protect other exploited wildlife in the future.
... Smaller populations, such as the ring-tailed lemurs of the Tsimanampetsotsa spiny forest, have similar ranges of nine to 14 adult individuals (LaFleur et al. 2014). Furthermore, ring-tailed lemur populations have experienced a notable decline in recent decades, which can lead to smaller, more-fragmented social groups (Gould and Sauther 2016;LaFleur et al. 2016LaFleur et al. 2018. In the present study, the two social groups discussed contain five (Windmill group) and seven (East Road group) individuals. ...
... Our descriptive results on IGEs among small groups of ring-tailed lemurs have important implications for future conservation efforts for this endangered species. Wild L. catta has experienced a significant reduction in both geographic ranges and population sizes due to anthropogenic deforestation, capture for bushmeat consumption, and the illegal pet trade, including several instances of local extinction (Gould and Sauther 2016;LaFleur et al. 2016LaFleur et al. , 2018. Reduced geographic ranges can potentially lead (Morris-Drake et al. 2022) to higher rates of conflict over limited resources. ...
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Primate species exhibit considerable variation in behavior and outcomes during intergroup encounters (IGEs). Social group characteristics, like group size, and individual traits, such as sex, rank, and reproductive status, within those groups can influence both IGE engagement and outcomes. To better understand the impact of group heterogeneity on IGEs, we must examine individual strategies to elucidate individual costs and benefits of engaging in these interactions. Here, we present a descriptive study of the IGEs between two small social groups of ring-tailed lemurs (Lemur catta) on St. Catherines Island, GA, USA. We distinguish between dyadic and multiple-individual interactions between groups to compare collective and individual agonistic engagement. All encounters occurred when the East Road group (N = 7 individuals) traveled from the center of their home range to the boundary with Windmill group's (N = 5 individuals) home range, indicating that East Road might have been actively testing this boundary for access to food resources, sleeping trees, and mating opportunities. We also found notable individual variation in participation during IGEs. The daughters of the highest-ranking females were the most-engaged in dyadic intergroup and intragroup aggression, had high "win" rates during intergroup dyadic encounters, and engaged in intergroup multiple-individual interactions at high levels. These findings indicate that they might value their home range more as "potential alphas" compared to other group members. Dominant females were the most engaged in multiple-individual interactions, suggesting that they contribute heavily to collective action that might result in a gain or loss of access to resources. Finally, these two small groups might be equally matched despite the two-individual group size disparity due to individual free-riding strategies. Future research should focus on individual strategies during IGEs to characterize the complex decisions and trade-offs that influence participation.
... It is also clear that conservation programming must consider which species are most affected by pet lemur ownership. Some species, like L. catta, appear to be disproportionately affected, both in terms of their popularity as pets and in terms of the impacts the illegal pet lemur trade could have on the species (on top of existing threats such as habitat degradation and hunting) [13,14]. There are probably other species-like the Critically Endangered Hapalemur alaotrensis (Alaotran gentle lemur)-where even just a small amount of localized live extraction for pet ownership would be enough to cause localized population extinctions over time. ...
... This is an added pressure to animals already facing rapid loss of habitat, and for some species or locations, unsustainable hunting for bushmeat [8]. Large and important areas for biodiversity conservation in Madagascar have experienced recent illegal clearings for agriculture [37] or mining purposes [38], and/or are devoid of lemurs because of illegal over-hunting and possibly extraction for the pet [12,14], despite the animals being present as recently as a decade ago. These trends of targeted biodiversity loss resulting from illegal activity needs to be urgently addressed by the government of Madagascar [39]. ...
Article
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Primates are extracted from the wild for the pet trade across the world. In Madagascar, lemurs are kept as illegal pets and an understanding of lemur pet ownership at the national level is lacking. In 2013 and 2016, we undertook a national survey in 11 of Madagascar’s 22 administrative regions (n = 28 towns) with 1,709 households. To our knowledge, this is the first national survey of the household ownership of pet primates in a country where they are endemic. In the 1.5 years prior to being surveyed, 8% ± 4% (towns as replicates) of respondents had seen a captive lemur while a further 0.7% ± 0.5% of respondents had owned one personally. We estimate that 33,428 ± 24,846 lemurs were kept in Malagasy households in the six months prior to our survey efforts, with 18,462 ± 12,963 of these pet lemurs estimated in urban household alone. Rates of lemur ownership did not differ by province but increased with the human population of a town and with the popularity of the town on Flickr (a proxy indicator for tourism). We found that the visibility of pet lemur ownership did not differ across the country, but it did increase with the size of the town and popularity with tourists. Areas with visible pet lemurs were not always the areas with the highest rates of pet lemur ownership, highlighting that many pet lemurs are hidden from the general public. Our study highlights the need for conservation programs to consider both the proportion of inhabitants that own pet lemurs and the total number of lemurs that are potentially being kept as pets in those towns. We close by noting that for some species, even just a small amount of localized live extraction for pet ownership could be enough to cause localized population extinctions over time. Moreover, an urgent response is needed to combat a recent and alarming rise in illegal exploitation of biodiversity across Madagascar.
... The Mahafaly peoples who live around BMSR have taboos, called fady against harming lemurs, which are seen as ancestors, and lemurs at BMSR have traditionally had a culturally protected status (Loudon et al., 2006). However, individuals moving into the area from other cultural groups for which bushmeat hunting of lemurs is not fady may not share the same cultural restrictions (LaFleur et al., 2018). Location of remains also tended to be near lemur "hot spots" based on the high presence of camera trap pictures of lemurs around and on Red West Trail, which is where our single picture of fosa is also located. ...
Article
Introduced species can negatively impact endemic flora and fauna. Studies have primarily utilized camera trap observations and occupancy modelling to better clarify the presence/absence and temporal overlap of endemic and exotic predators. Longitudinal data from field research sites are important as they can provide a finer understanding of predator dynamics and their effects on endemic species. One such site is the Bezà Mahafaly Special Reserve, in southern Madagascar. Protected since the 1970s, the local human population around Bezà Mahafaly Special Reserve has greatly expanded, leading to habitat disturbance in the surrounding forests and increased contact between local wildlife, people and their livestock and dogs. Here we use a combination of scat sampling, field observations of successful and attempted predations, locations of scat samples with identifiable lemur remains, and camera trap data to better assess the predator ecology at Bezà Mahafaly Special Reserve. Our results indicate that forest cats ( Felis catus ), are effective predators of both adult and infant lemurs and appear to be a constant mammalian predator, utilizing mammal prey more than dogs. Dogs are both predators and scavengers of lemurs. Civets focus on small prey, such as insects and rodents as well as plant material. The fosa, Cryptoprocta ferox , are also present but may not hunt in the area continuously. The killing of an adult ring-tailed lemur by two men from outside the area indicate culturally imposed taboos against lemur killing may no longer be effective given that new arrivals may not share the same local cultural restrictions. Scat sampling of exotic predators is one way to expand our understanding of exotic and endemic predator impact on lemur populations, and long-term studies with multiple assessments of predation can provide a clearer understanding of how non-endemic and endemic predators affect endangered species survival.
... Increased rates of deforestation in Madagascar, primarily driven by the need to meet economic and subsistence needs at the household level, have resulted in high degrees of habitat fragmentation (Schwitzer et al., 2013a). Fragmented, patchy areas lead to increased encounters with lemurs, increases in hunting opportunities (e.g., to meet subsistence needs, supply wildlife trade), and in turn potential disease transmission (C2; C7; C9; D1) (Barrett and Ratsimbazafy, 2009;Gilles and Reuter, 2014;LaFleur et al., 2016LaFleur et al., , 2018LaFleur et al., , 2019. The decline in the populations of red-collared brown lemurs (Eulemur collaris) in Saint Luce (southeast Madagascar) is attributed to hunting, although a population persists in the littoral forest fragments of the area (Roberts et al., 2019/20). ...
Article
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Globally, non-human primates face mounting threats due to unsustainable harvest by humans. There is a need to better understand the diverse drivers of primate harvest and the complex social-ecological interactions influencing harvest in shared human-primate systems. Here, we take an interdisciplinary, systems approach to assess how complex interactions among primate biological and ecological characteristics and human social factors affect primate harvest. We apply our approach through a review and synthesis of the literature on lemur harvest in Madagascar, a country with one of the highest primate species richness in the world coupled with high rates of threatened primate species and populations in decline. We identify social and ecological factors affecting primate harvest, including the characteristics of lemurs that may make them vulnerable to harvest by humans; factors describing human motivations for (or deterrents to) harvest; and political and governance factors related to power and accessibility. We then discuss social-ecological interactions that emerge from: (1) the prevalence of informal institutions (e.g., cultural taboos), (2) adoption of human predatory strategies, (3) synergies with habitat use and habitat loss, and (4) interactions among regional- and local-scale factors (multi-level interactions). Our results illustrate that social-ecological interactions influencing lemur harvest in Madagascar are complex and context-specific, while influenced by a combination of interactions between species-specific characteristics and human social factors. These context-specific interactions may be also influenced by local-level cultural practices, land use change, and effects from regional-level social complexities such as political upheaval and food insecurity. We conclude by discussing the importance of identifying and explicitly accounting for nuances in underlying social-ecological systems and putting forth ideas for future research on primate harvest in shared human-primate systems, including research on social-ecological feedbacks and the application of Routine Activities Theory.
... Despite the sustainable captive population, wild L. catta populations saw a 20% decrease between 1985 to 2000 (Sussman, et al., 2006) and further local extinctions suspected a decline rate of over 50%, estimating the current population between 2000 to 2400 individuals (Andriaholinirina, et al., 2014;LaFleur, et al., 2017LaFleur, et al., , 2018. The result reflected previous population trends; seeing the species upgraded from Near Threatened to Endangered on the IUCN Red List (Andriaholinirina, et al., 2014;Gould & Sauther, 2016), and being identified as one of the world's top 25 endangered primates (Schwitzer, et al., 2017). ...
Article
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Environmental education programs focus on improving the public’s knowledge and support of conservation motives, improving polices, and making decisions which have an overall positive effect on the natural world . Zoological establishes zoos are in a critical position for providing educational opportunities to the public, as both direct and indirect approaches. Using a simple survey to collate data, this study assess the learning experiences available at zoos and their retrospectively quality in terms of knowledge retention using a well known captive species; Lemur catta. This study found that visitors who have been exposed to more focused education experiences will have greater general knowledge regarding lemur species and L. catta in particular, as there were significant positive correlations between learning categories. With this in mind, establishments should aim to continue providing regular talks and review the content and species targeted to maximise effectiveness.
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Anthropogenic activities are negatively affecting the flora and fauna of Madagascar, including its Endangered flagship lemur species, the ring-tailed lemur Lemur catta . Population numbers at some sites are rapidly declining, yet much of the species' habitat is insufficiently surveyed. Because widespread population assessments are critical to guiding conservation management strategies, additional data are needed to monitor L. catta population trends and to identify the limits of their geographical range. Here we report survey results confirming the presence of this species at 65 of 83 sites in southern and south-western Madagascar, including three subpopulations that were previously considered likely to be locally extinct. We identified a minimum of 792 L. catta individuals (summing only maximum group sizes at each site) and as many as 1,221 individuals (using estimated population counts). These findings help refine the distribution of L. catta and reaffirm their presence in areas of their historical geographical range. Identifying species occupancy at sites such as these provides valuable data to support species conservation, but also highlights the need for additional surveys throughout the range of the species.
Chapter
Habitat loss and degradation are currently the main anthropogenic causes of species extinctions. The root cause is human overpopulation. This unique volume provides, for the very first time, a comprehensive overview of all threatened and recently extinct mammals, birds, reptiles, amphibians, and fishes within the context of their locations and habitats. The approach takes a systematic examination of each biogeographic realm and region of the world, both terrestrial and marine, but with a particular emphasis on geographic features such as mountains, islands, and coral reefs. It reveals patterns useful in biodiversity conservation, helps to put it all into perspective, and ultimately serves as both a baseline from which to compare subsequent developments as well as a standardization of the way threatened species are studied.
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Cardiac disease has been recognized as a major cause of death in captive nonhuman primates, which necessitates diagnostic (imaging) techniques to screen for and diagnose preclinical and clinical stages of possible cardiac conditions. Echocardiography is currently the most commonly used diagnostic tool for evaluation of cardiac anatomy and function. Complete with thoracic radiography and blood levels of two cardiac biomarkers, N-terminal probrain natriuretic peptide (NT-proBNP) and cardiac troponin T (cTnT), it gives an extensive examination of the cardiorespiratory system. The purpose of this cross-sectional cohort study is to describe normal thoracic anatomy using thoracic radiography, and to provide normal values for echocardiographic measurements in 20 ring-tailed lemurs (Lemur catta). Additionally, cardiac biomarkers were determined. Three radiographic projections of the thoracic cavity and a complete transthoracic echocardiography were performed in 20 clinically healthy ring-tailed lemurs during their annual health examinations. Similar standard right parasternal and left apical echocardiographic images were obtained as described in dogs and cats and normal values for routine two-dimensional (2D-), time-motion (M-) and Doppler mode measurements were generated. Furthermore, a noninvasive smartphone base ECG recording and blood concentrations of cardiac biomarkers were obtained. Other radiographic measurements are provided for the skeletal and respiratory systems such as the trachea to inlet ratio and tracheal inclination. Knowledge of the normal radiographic thoracic and echocardiographic anatomy and function are fundamental for the diagnosis and follow-up of cardiac disease in affected individuals and for species screening, and will be of added value in future research in and conservation of this endangered species.
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Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats— mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture , large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world's primates and the costs of their loss to ecosystem health and human society is imperative.
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Overhunting in tropical forests reduces populations of vertebrate seed dispersers.If reduced seed dispersal has a negative impact on tree population viability, overhunting could lead to altered forest structure and dynamics, including decreased biodiversity. However, empirical data showing decreased animal-dispersed tree abundance in overhunted forests contradict demographic models which predict minimal sensitivity of tree population growth rate to early life stages. One resolution to this discrepancy is that seed dispersal determines spatial aggregation, which could have demographic consequences for all life stages. We tested the impact of dispersal loss on population viability of a tropical tree species, Miliusa horsfieldii, currently dispersed by an intact community of large mammals in a Thai forest. We evaluated the effect of spatial aggregation for all tree life stages, from seeds to adult trees, and constructed simulation models to compare population viability with and without animal-mediated seed dispersal. In simulated populations, disperser loss increased spatial aggregation by fourfold, leading to increased negative density dependence across the life cycle and a 10-fold increase in the probability of extinction. Given that the majority of tree species in tropical forests are animal-dispersed, overhunting will potentially result in forests that are fundamentally different from those existing now. http://rspb.royalsocietypublishing.org/content/282/1798/20142095.short
Chapter
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Field biologists adopted the term habituation from physiology, as the relatively persistent waning of a response as a result of repeated stimulation that is not followed by any kind of reinforcement (Thorpe, 1963). Repeated neutral contacts between primates and humans can lead to a reduction in fear, and ultimately to the ignoring of an observer. Historically, the techniques and processes involved were rarely described, as habituation was generally viewed as a means to an end (Tutin & Fernandez, 1991). As we become increasingly aware of the potential effects of observer presence on primate behaviour, and especially the potential risks of close proximity with humans, it behoves us to measure as much about the habituation process as possible. However, most recent studies that have quantified primate behaviour in relation to habituators have focussed on great apes (see, for example, Ando et al., 2008; Bertolani & Boesch, 2008; Blom et al., 2004; Cipolletta, 2003; Doran-Sheehy et al., 2007; Sommer et al., 2004; Werdenich et al., 2003), with little information available for other primate taxa (but see Jack et al., 2008).
Article
The ring-tailed lemur (Lemur catta) was once widely distributed throughout the south-central, far south, and southwest regions of Madagascar. This species is known for its marked ecological plasticity and ability to survive in a variety of habitats. Over the past decade, however, habitat destruction, forest fragmentation, hunting for subsistence or the illegal bushmeat trade, and live capture for the illegal pet trade have increased, resulting in extirpation or drastic reduction of populations throughout its geographic range. Recent mining activities in one region have resulted in further serious threats to remaining populations. In this paper, we discuss (1) population numbers and information on population extirpations, gathered over approximately the past six years, to illustrate the alarming decline of this well-known lemur, and (2) how the formerly accepted geographic range of L. catta now requires considerable revision. Population information was collected via on-the-ground surveys and censuses, or from reports by researchers at 34 sites where L. catta is or was recently present. Only three sites are known to contain populations of more than 200 animals. At 12 sites, populations number 30 or fewer individuals, and at 15 sites, L. catta has been recently extirpated, or populations are highly precarious and may become extinct in the very near future. Populations at three previously designated range limits have been extirpated. Many populations are surviving in small, isolated forest fragments, allowing for no male dispersal. With an estimate of just 2, 000-2, 400 individuals remaining in Madagascar, this iconic lemur may well become extinct in the wild in the near future, or at the very least, exist at only two or three widely dispersed sites.
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Live extraction of wildlife is a threat to biodiversity and can compromise animal welfare standards. Studies of the captive environments and welfare of pet primates are known, but none has focused on Madagascar. We aimed to expand knowledge about the captive conditions of pet lemurs in Madagascar. We hypothesized that captive le- murs would often be kept in restrictive settings, including small cages, would be fed foods inconsistent with their natural diets and, as a result, would be in bad physical or psychological health. Data were collected via a web-based survey (n = 253 reports) and from the websites and social media pages of 25 hotels. Most lemurs seen by respon- dents were either kept on a rope/leash/chain or in a cage (67%), though some lemurs were habituated and were not restrained (28%). Most of the time (72%) cages were con- sidered small, and lemurs were rarely kept in captivity together with other lemurs (81% of lemurs were caged alone). Pet lemurs were often fed foods inconsistent with their natural diets, and most (53%) were described as being in bad health. These findings point to a need to undertake outreach to pet lemur owners in Madagascar about the captivity requirements of primates.
Article
The south-central highland region of Madagascar is largely deforested, except for rare, small forest fragments scattered across the landscape. Some of these fragments are now being managed by local community conservation associations, after village residents have seen, first hand, how decades of deforestation and, more recently, climate change in the region have affected their agricultural crops. Furthermore, ecotourism is becoming more common in this area, with the two largest fragments, Anja Community Reserve and the Tsaranoro Valley forest, frequently receiving both Malagasy and foreign visitors. The combination of revenue from such tourism and the prospects of greater food security (by conserving and expanding existing fragments, leading to better soil conditions for nearby crops and rice fields) has resulted in increased fragment preservation over the past few years. We surveyed seven of these fragments in August and September, 2013, with two goals: (1) to evaluate the viability of ring-tailed lemur populations in each fragment in relation to food and water resource availability; and (2) to discuss, with village conservation association leaders, the goals of each association regarding fragment conservation and benefits to local residents. Anja Reserve, operating since 1999, is highly successful, and the association's ecotourism and community development projects have won them national and international recognition. In 2012, village associations Sakaviro Miray, FI.MI.VA Samisorany, and Antokinihoavy-Andranobe received NGO funding to help build a tourism presence in the region, and infrastructure for such activities had begun when we visited these sites in 2013. The Tsaranoro Valley, where three of the fragments are located, is an adventure tourism destination; however, much of the tourism revenue goes to the owners of the trekking camps, although a portion of the funds are donated to the local Association Tantely each year, and these camps also provide jobs for local villagers. Recent efforts are underway to expand these three fragments via reforestation, and to create a corridor between two of them in order to assist with the dispersal of L. catta males, and thus assist with potential population gene flow.
Article
South-western Madagascar has experienced large reductions in forest cover over the last decades. However, there are major uncertainties in the total extent of the country’s deforestation and particularly in understanding the anthropogenic impact on land cover changes (LCC). Based on satellite image classifications, spatial bio-physical data and socio-economic data from village-level interviews, we therefore explored the role of settlement characteristics in LCC and forest fragmentation processes in the Mahafaly region during the past 40 years. For this study, a time-series of Landsat satellite images from 1973 to 2013 was classified using a supervised approach, and deforestation and LCC trends were identified for different time periods. The studied settlements were classified according to their geographic location, socio-economic activities and economic status. The factors that directly affect deforestation processes, underlying socio-economic, and bio-physical contributors to deforestation trends were investigated at the settlement level through regression analysis. Over the past 40 years forest losses amounted to 45% and led to increasing savannization and forest fragmentation, whereby the rates of deforestation were not constant through time. Deforestation was strongest at remote locations, and near to small settlements that are poorly connected to infrastructure and main markets and are relatively young. The causes of this diffuse deforestation pattern in the Mahafaly region changed through space and time, but one major driver is the ‘clandestine pioneer-agriculture’ often practiced by immigrant farmers.