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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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