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Rapid Decrease in Populations of Wild Ring-Tailed Lemurs (Lemur catta) in Madagascar

Authors:
  • Franklin Scholars

Abstract and Figures

Lemurs are the most threatened group of mammals on earth. Lemur catta (ring-tailed lemur) represents one of the most iconic lemur species and faces numerous an-thropogenic threats in the wild. In this study, we present population estimates from 32 sites across the range of L. catta , collected from primary and secondary data sources, to assess the number of ring-tailed lemurs left in the wild. We estimate that there are approximately 2,220 individual L. catta remaining in the 32 sites considered. We note local extinctions of populations of L. catta in at least 12 of the 32 sites examined, and that significantly more extinctions occurred in areas without some form of protection. This decrease in extant populations could represent a decrease of more than 95% of all ring-tailed lemurs in Madagascar since the year 2000. While these results should be considered preliminary, we stress the rapid decline of the species and note that habitat loss, bush-meat hunting and the illegal pet trade are driving populations to local extinction. Based on the data presented here, urgent and immediate funding and conservation action are crucial to ensure the viability of the remaining wild populations of ring-tailed lemurs.
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Short Communication
Folia Primatol 2016;87:320–330
DOI: 10.1159/000455121
Rapid Decrease in Populations of
Wild Ring-Tailed Lemurs ( Lemur catta ) i n
Madagascar
Marni LaFleur a Tara A. Clarke b Kim Reuter c Toby Schaeffer d
a Department of Anthropology, University of California San Diego, La Jolla, CA , and
b Evolutionary Anthropology Department, Duke University, Durham, NC , USA;
c Africa Field Division, Conservation International, and d Independent Consultant
(pro bono), Nairobi , Kenya
Keywords
Ring-tailed lemur · Madagascar · Extinction · Bushmeat · Pet trade ·
Population decline · Lemur catta
Abstract
Lemurs are the most threatened group of mammals on earth. Lemur catta (ring-
tailed lemur) represents one of the most iconic lemur species and faces numerous an-
thropogenic threats in the wild. In this study, we present population estimates from 32
sites across the range of L. catta , collected from primary and secondary data sources, to
assess the number of ring-tailed lemurs left in the wild. We estimate that there are ap-
proximately 2,220 individual L. catta remaining in the 32 sites considered. We note local
extinctions of populations of L. catta in at least 12 of the 32 sites examined, and that sig-
nificantly more extinctions occurred in areas without some form of protection. This de-
crease in extant populations could represent a decrease of more than 95% of all ring-
tailed lemurs in Madagascar since the year 2000. While these results should be considered
preliminary, we stress the rapid decline of the species and note that habitat loss, bush-
meat hunting and the illegal pet trade are driving populations to local extinction. Based
on the data presented here, urgent and immediate funding and conservation action are
crucial to ensure the viability of the remaining wild populations of ring-tailed lemurs.
© 2017 S. Karger AG, Basel
Introduction
Lemurs are the most threatened group of mammals on earth and are endemic to
Madagascar, a biodiversity hotspot [Schwitzer et al., 2014]. Lemurs face numerous
threats, including habitat loss due to deforestation and climate change [Brown and
Received: August 29, 2016
Accepted after revision: December 14, 2016
Published online: January 13, 2017
Marni LaFleur
Department of Anthropology
University of California San Diego
Campus Box 0532, La Jolla, CA 92093 (USA)
E-Mail marni.lafleur
@ gmail.com
© 2017 S. Karger AG, Basel
0015–5713/17/0875–0320$39.50/0
www.karger.com/fpr
E-Mail karger@karger.com
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DOI: 10.1159/000455121
Yoder 2015], hunting [Schwitzer et al., 2014], and the illegal pet trade [Reuter et al.,
2016]. Lemurs have been described as “the single highest primate conservation prior-
ity in the world” [Schwitzer et al., 2013, p. 5].
Ring-tailed lemurs ( Lemur catta ) are a flagship species for conservation, and are,
perhaps, Madagascar’s best-known primate. These lemurs are characterized by their
behavioural flexibility, in that their sociality (e.g., dominance/rank relationships, ag-
gression) and activity budgets vary according to environmental conditions [Sauther
et al., 1999], and ecological plasticity, in that they can inhabit a plethora of habitat
types [Goodman et al., 2006] and rebound from environmental perturbations [Gould
et al., 1999]. The first large-scale population estimates of wild ring-tailed lemur hab-
itats and individuals estimated a 9.5% habitat and 20% population decrease between
1985 and 2000 (population estimated at 751,251 in the year 2000 [Sussman et al.,
2006]). Since then, census attempts of specific sites have continued [e.g., Kelley, 2013;
Dimilahy et al., 2015; Gould and Andrianomena, 2015], yielding evidence of localized
ring-tailed lemur extinctions [Gardner and Davies, 2014] and a suspected population
decline rate of over 50% over a 3-generation period [Andriaholinirina et al., 2014].
P o p u l a t i o n d e c l i n e s o f L. catta are driven by various threats. Ring-tailed lemurs
represent 28% of individuals kept as in-country illegal pets [Reuter and Schaefer, 2016],
and are sometimes killed and consumed by their human owners [Reuter and Schaefer,
in press]. This species also faces direct hunting pressure [e.g., Goodman 2003], signifi-
cant habitat loss [Brinkmann et al., 2014], and population declines resulting from the
effects of climate change [Brown and Yoder, 2015]. As a result, L. catta is now restricted
to isolated fragments [Sussman et al., 2003] with relatively low population densities
[Kelley 2013; Andriaholinirina et al., 2014; Gould and Andrianomena, 2015], and its
survival in the wild at most locations remains perilous [but see Dimilahy et al., 2015].
In this study, we present a population estimate for ring-tailed lemurs across 32
locations within their natural and historical range across south-western Madagascar.
Moreover, we discuss the consequences of our findings and propose next steps to en-
sure the long-term viability of remaining wild populations.
Methods
Estimating Population Numbers at Known Sites
We assessed the status of populations of L. catta at 32 locations where they are known to
occur ( Fig.1 ; Table1 ). Similar to a census of chimpanzees ( Pan troglodytes ) by Plumptre and Cox
[2006], we collected primary and secondary data regarding the largest known and/or protected
habitat fragments in which L. catta is found to estimate the total number of individuals left in the
wild. L. catta is found at locations outside of these 32 known sites [Goodman et al., 2006, map
approx. 100 records of wild populations of L. catta ); however, these 32 sites likely comprise the
largest remaining populations of L. catta , as many of the previously mentioned “known” sites are
now deforested or devoid of animals [Sussman et al., 2006; Gardner and Davies, 2014].
To assess the status of populations of L. catta at these 32 sites, we used a mixture of methods:
in-person site visits (M.L. and T.A.C.), personal communication with other researchers, and in-
formation gleaned from the published literature ( Table1 ). We could not visit all 32 field sites due
to time and budget limitations; for in-person site surveys, we prioritized locations where previous
researchers suggested that populations of L. catta were under significant extraction pressure [e.g.,
Kirindy Mitea Sud hunting pressure, Goodman, 2003; Andohahela hunting pressure, Siers, 2007].
For in-person site surveys ( n = 10 sites, Table1 ), M.L. and T.A.C. spent a minimum of 2
days at each site in June-August 2016 and used rapid assessment methods [Gilles and Reuter,
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322 LaFleur/Clarke/Reuter/Schaeffer
2014] to confirm or fail to confirm the presence of L. catta . Since we aimed to confirm the pres-
ence of ring-tailed lemurs in the locations visited, we took steps to increase the chances of detect-
ing animals. These included speaking to local officials and villagers in order to understand where
animals had been seen in the recent past, or where ring-tailed lemur troops’ sleep sites or fre-
quently used trees may be located. Once target areas were identified, we then walked on both
forest trails and off-trail locations for between 5 and 12 km/day, while trying to detect the pres-
ence of ring-tailed lemurs. Confirmation of the presence of L. catta included hearing calls or ob-
serving animal(s), or indirect indicators of presence such as seeing footprints, spur markings on
vegetation, bite marks on plants/foods, and/or presence of faeces. Indirect indicators of animal
presence are reliable when efforts are standardized and consistent [Macdonald et al., 1999], and
can be used to detect population changes in wildlife [Gese, 2001]. At all sites where the presence
of L. catta could not be confirmed, M.L. and T.A.C. spoke with park managers, tour guides, and/
or local community members to understand when and how many L. catta had last been seen at
that site, and whether the animals had faced any known threats in the past. At 7 out of 10 sites,
M.L. and T.A.C. were unable to confirm the presence of L. catta and therefore consider these
populations to be locally extinct unless otherwise noted ( Table1 ). At the remaining 3 sites (Isalo
Historical range (a)
Records of Lemur catt a
Provinces
Protected areas
Historical range
Cities
Current range (b)
Extinct
Locally or nearly locally extinct
Present
Provinces
Protected areas
Cities
04080120160200km
Fig. 1. Historical range ( a ) and estimated current range ( b ) for L. catta , including areas where
populations are present, locally extinct, or likely or nearly locally extinct. a Data are from Good-
man et al. [2006] and Andriaholinirina et al. [2014]. b References are available from Table1.
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Table 1. Locations of known populations of L. catta included in the scope of this paper
Location name Coordinates Protected status Population category Number
of
animals
Size of forest
fragment or
protected
areaa, km2
Year of
assess-
ment
Source of
information
Days of
rapid
sampling
Citation (most recent
known)
Ambatotsirongorongo
Forest
25°04.70 S,
46°47.24 E
Protected area Present 50 0.25 2010 Literature Razafindramanana,
2011
Ambinany (Berenty region) 24°59.53 S,
46°18.07 E
Private reserve Present 65 2015 Literature Dimilahy et al., 2015
Andohahela 24°08.72 S,
43°49.74 E
National park Present*82 760 2000 Literature Moniac and Heitman,
2007
Andranobe (Ambolavoa
region)
21°57.78 S,
46°56.73 E
Community-level
association
Present 36 0.381 2013 Literature Gould and
Andrianomena, 2015
Andringitra 22°06.76 S,
46°55.38 E
National park Present 106 31,134 1995 Literature Rakotoarisoa, 1999
Anja Miray (Ambalovoa
region)
21°51.12 S,
46°50.40 E
Community-level
association
Present 210 0.36 2013 Literature Gould and
Andrianomena, 2015
Anjapolo (Berenty region) 24°57.66 S,
46°15.06 E
Private reserve Present 151 2015 Literature Dimilahy et al., 2015
Bealoka (Berenty region) 25°00.59 S,
46°18.51 E
Private reserve Present*163 1 2009 Literature Dimilahy et al., 2015;
Sussman et al., 2006
Berenty (Berenty region) 24°59.88 S,
46°19.87 E
Private reserve Present 562 2 2010 Literature Dimilahy et al., 2015
Beza Mahafaly Parcel 1 23°42.00 S,
44°32.33 E
Special reserve Present 124 0.8 2014 Pers. commun. Sauther, pers. commun.
Beza Mahafaly Parcel 2 23°42.00 S,
44°34.33 E
Special reserve Present 205 5.2 2014 Pers. commun. Sauther, pers. commun.
Cap Sainte-Marieb 25°35.75 S,
45°08.35 E
Special reserve Locally or nearly
locally extinct*
50 0.18 2008 Literature Kelley, 2013
Chameleon (Tsaranoro
Valley)
Unknown Community-level
association
Present 28 0.08 2013 Literature Gould and
Andrianomena, 2015
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324 LaFleur/Clarke/Reuter/Schaeffer
Location name Coordinates Protected status Population category Number
of
animals
Size of forest
fragment or
protected
areaa, km2
Year of
assess-
ment
Source of
information
Days of
rapid
sampling
Citation (most recent
known)
Ifaty 23°08.71 S,
43°36.95 E
Unprotected Extinct*0 – 2015;
2016
Literature; pers.
observation
–, 2 LaFleur et al., 2015
Isalo (Maki canyon)c22°29.26 S,
45°22.73 E
National park Present 118 0.5 1995;
2016
Literature; pers.
observation
–, 1 Hawkins, 1999
Isalo (Namaza circuit)c23°31.82 S,
43°46.01 E
National park Present 1995;
2016
Literature; pers.
observation
–, 1 Hawkins, 1999
Kalambatritra 23°20.50 S,
46°28.66 E
Special reserve Locally or nearly
locally extinct*
0 282.55 2005 Literature Irwin et al., 2005d
Kirindy Mitea 20°44.38 S,
44°10.32 E
National park Extinct*0 722 2016 Pers. commun.;
pers. observati-
on
–, 1 Lewis B., pers.
commun.;
Goodman, 2003
Kirindy Mitea de sud 20°44.23 S,
44°00.07 E
Unprotected Extinct*0 2016 Pers. observati-
on
–, 2 Goodman, 2003
Mangily (Reniala Private
Reserve)
23°07.59 S,
43°36.80 E
Unprotected Extinct*0 0.6 2015 Literature; pers.
observation
–, 2 LaFleur et al., 2015;
Gardner and Davies,
2014
Marody (Tsaranoro Valley) 22°05.57 S,
46°47.65 E
Community-level
association
Present 15 0.028 2013 Literature Gould and
Andrianomena, 2015
Petriky 25°04.31 S,
46°53.10 E
Unprotected Locally or nearly
locally extinct*
4 11.8 2012 Literature Malone et al., 2013
Pic d’Ivohibe 22°30.00 S,
46°59.00 E
Special reserve Locally or nearly
locally extinct*
0 34.5 2005 Literature Irwin et al., 2004d
PK 32-Ranobe 22°59.82 S,
43°40.20 E
Protected area Extinct*0 200.46 2010 Literature Gardner and Davies,
2014
Sakarivo Miray
(Ambolavoa region)
21°47.01 S,
46°52.07 E
Community-level
association
Present 30 0.142 2013 Literature Gould and
Andrianomena, 2015
Samisoramy
(Ambalavoa region)
21°47.18 S,
24°49.83 E
Community-level
association
Present 21 0.203 2013 Literature Gould and
Andrianomena, 2015
Table 1 (continued)
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Location name Coordinates Protected status Population category Number
of
animals
Size of forest
fragment or
protected
areaa, km2
Year of
assess-
ment
Source of
information
Days of
rapid
sampling
Citation (most recent
known)
Tsaranoro (Tsaranoro
Valley)
22°05.18 S,
46°46.32 E
Community-level
associations
Present 78 0.46 2013 Literature Gould and
Andrianomena, 2015
Tsimanampetsotsa
(northern boundary)
24°05.40 S,
43°49.80 E
National park Present 67 2016 Pers. observati-
on
10 (including
research for a
larger, ongoing
project on
ring-tailed
lemur ecology)
Tsimanampetsotsa
(southern boundary)
24°37.98 S,
43°55.98 E
National park Present 40 2015 Pers. commun. Louis E.E., pers.
commun.
Tsinjoriake (Moringa
circuit)b23°31.31 S,
43°45.28 E
Protected area Locally or nearly
locally extinct*
5 50 2016 Pers. commun.;
pers. observati-
on
–, 3 Youssouf J., pers.
commun.
Tsinjoriake (southern
mangrove area)
23°32.18 S,
43°44.68 E
Protected area Locally or nearly
locally extinct*
0 2016 Pers. observati-
on
–, 3
Zombitse-Vohibasiae22°50.50 S,
44°40.91 E
National park Locally or nearly
locally extinct*
10 0.36 2016 Pers. commun.;
pers. observati-
on
–, 2 Madagascar National
Parks, pers. commun.;
Siers, 2007
Total 2,220
An asterisk indicates known exploitation pressures (e.g., hunting) at the location against L. catta. “Personal observation” indicates that we collected data during a site visit in 2016.
a These area estimates should be interpreted with caution as they were often not reported alongside density estimates but have been extracted from various, publicly available documents.
b Kelley [2013] reports a range of 35 50 individual ring-tailed lemurs at Cap Sainte-Marie. Similarly, although we failed to detect the presence of animals, a student of Dr. Youssouff reported seeing a
range of 4–5 animals in Tsinjoriake (Moringa circuit) in August 2016. For the purposes of this paper, we used the larger value for the number of individual lemurs at both sites.
c We confirmed the presence of ring-tailed lemurs at Isalo but were unable to sample all known groups. We thus used data from Hawkins [1999] to estimate the total number of animals. Hawkins [1999]
does not differentiate between the 2 populations of ring-tailed lemurs present, and thus we cite 1 value here for all of Isalo.
d Irwin et al. [2004] conducted extensive censuses at Pic d’Ivohibe and Kalambatritra. Their censuses do not report the presence of ring-tailed lemurs, and here we use these data to infer the absence of
the species.
e We failed to detect animals, but the Madagascar National Parks ecological monitoring team reported the presence of 10 animals in March 2016 (3 months previously).
Table 1 (continued)
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326 LaFleur/Clarke/Reuter/Schaeffer
Maki canyon, Namaza circuit, Tsimanampesotse northern boundary), we estimated how many
L. catta were likely present by counting animals in known groups. More specifically, at Isalo
(Maki canyon), we walked a circuit until we encountered ring-tailed lemur groups and then fol-
lowed the animals for a minimum of 1 h, in order to ascertain how many animals were travelling
with the group. At Isalo (Namaza circuit), we remained in a tourist picnic spot, and when ring-
tailed lemur groups came through we monitored/followed individuals to determine the group
size and identity. At Tsimanampesotse, we monitored known groups and detailed any intergroup
encounters with neighbouring/unknown groups. For sites not visited in person ( n = 22), we col-
lected data from the literature and from colleagues who had visited these sites ( Table1 ).
Given the variations in sample size, methodological approach, sampling effort, and date of
assessment, our compiled data largely violate assumptions of parametric and non-parametric
statistics. Thus, the majority of our analyses are descriptive in nature. We present the mean,
range, and median numbers of ring-tailed lemurs present at each of the 32 study sites, and com-
pare the likelihood of local extinction between protected and unprotected areas (Fisher exact test,
p = 0.05). We recognize that the data presented here are limited and must be treated with caution.
Both over- and underestimations are possible in the data presented here. Overestimations are
possible in the data that were collected several years ago [Gould and Andrianomena, 2015], as
animals may no longer be present. Underestimates are also possible in areas where sampling ef-
fort has not been sufficient, such as large protected areas without extensive monitoring (i.e., Tsi-
manampesotse National Park, Isalo National Park). Despite these limitations, the data presented
here are still informative in understanding decreasing population trends and the urgent conser-
vation threats faced by ring-tailed lemurs.
Results
Parameters of the Data Set
We sourced data for 84% of the sites ( n = 27 out of 32) from information made
public in 2010 or thereafter ( Table1 ). Ring-tailed lemurs’ historical range covers
roughly 100,000 km
2 throughout southern Madagascar, although this generalized es-
timate includes both habitable (e.g., forested) and uninhabitable (e.g., rivers, cities)
areas [Sussman et al., 2006]. The sites assessed here covered the habitable area of ap-
proximately 33,208 km
2 ( Table1 ).
Estimated Population Size across 32 Sites
We estimate the presence/absence and total number of animals remaining at the
32 sites considered in this study. L. catta were deemed locally extinct or nearly lo-
cally extinct (i.e., we were unable to detect the animals’ presence; fewer than 5 animals
remaining at last known sighting) in 37.5% of the sites included in this study ( n = 12
of 32, Table1 ). A higher percentage of areas with some form of protection or man-
agement status (69% of n = 29 sites) had extant ring-tailed lemur populations, when
compared to unprotected areas (0% of n = 3 sites, Fisher exact test, n = 32, p = 0.0444,
sites with extinct and likely extinct populations grouped together).
The sites had an average of 72 ± 110 (mean ± SD; range: 0–562; median 36) in-
dividuals of L. catta per site ( Table1 ). In 2 instances the numbers of animals were
reported as a range including 35–50 individual ring-tailed lemurs at Cap Sainte-Ma-
rie [Kelley, 2013] and 4–5 individual ring-tailed lemurs at Tsinjoriake [Youssouff,
pers. commun.]. For these 2 instances we included the high estimates of the number
of animals present ( Table1 ). Only 8 of 32 sites had populations of more than 100 in-
dividuals ( Table1 ). Sites with some protection ( n = 28 sites) had an average of 79 ±
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113 individuals, while sites without protection ( n = 3 sites) had an average of 3 ± 1
individuals left at the site. From the sum of all sites examined, we estimate that there
are approximately 2,220 ring-tailed lemurs remaining in the sites included in this
study ( Table1 ).
Discussion
We estimate that there are 2,220 L. catta remaining at the 32 sites included in this
study. This estimate may not account for all small forest fragments where ring-tailed
lemurs could persist or all possible groups of animals in unmonitored areas of large
National Parks (i.e., Tsimanampesoste, Isalo), and thus could underestimate the total
number of animals remaining. Alternatively, the estimate could include animals that
have been extirpated very recently, and thus be inflated. Given that the previous esti-
mates for individual wild ring-tailed lemurs were 2 orders of magnitude larger (i.e.,
751,251 [Sussman et al., 2006]), we are confident that there has been a rapid decrease
in the numbers of animals living in the wild in Madagascar. Though we acknowledge
that both ours and the population estimates of Sussman et al. [2006] were calculated
with caveats, this sharp decline is concerning. Both complete deforestation of land
parcels and decline of their lemur inhabitants [e.g., Kelley et al., 2007, Antserana-
nomby Forest] and localized extirpations of ring-tailed lemurs without forest clearing
(e.g., Ranobe area [Gardner and Davies, 2014]) have been previously documented.
Current and detailed data regarding the numbers of ring-tailed lemurs persisting in
all of their habitats are urgently needed to understand fully the dramatic decline in
wild ring-tailed lemurs and prevent complete extinction in the wild.
The rapid decline in populations of L. catta has implications for conservation of
the species. First, we found only 1 site with a population of >500 L. catta ( Table1 ). In
Uganda, sites with <500 chimpanzees ( Pan troglodytes ) are of conservation concern
as smaller populations are not able to sustain genetic viability in the long term
[Plumptre and Cox 2006]. In the case of L. catta , Clarke et al. [2015] found that ring-
tailed lemur populations with fewer than 500 individuals in the central highlands
maintain moderate levels of genetic diversity. These populations, however, are likely
exhibiting a time lag response whereby genetic diversity will decrease substantially in
the future due to continued population fragmentation and associated impacts [Clarke
et al., 2015]. Both the low numbers of individuals at isolated sites (and the individu-
als’ potential inability to find mates), and the consequences of low genetic diversity
are problematic for ring-tailed lemurs’ long-term survival in the wild. Second, we
found that unprotected areas are more likely to experience population extinctions of
ring-tailed lemurs. The general effectiveness of protected areas in maintaining species
presence has been documented globally [see Naughton-Treves et al., 2005], and with-
in the order Primates [see Pusey et al., 2007], although effective management of pro-
tected areas is also necessary, as has been noted for lemur species specifically [Schwit-
zer et al., 2014]. Madagascar has been plagued with political turmoil, yet even during
times of crisis, conservation threats are more significant outside protected areas
[Schwitzer et al., 2014]. The combination of higher levels of genetic diversity within
larger populations and better survivorship within protected areas suggests that con-
servation priorities for ring-tailed lemurs should include areas with more animals and
established protection ( Table1 ).
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328 LaFleur/Clarke/Reuter/Schaeffer
A t t h e g l o b a l s c a l e , p o p u l a t i o n e x t i n c t i o n s a r e a m o r e s e n s i t i v e i n d i c a t o r o f t h e l o s s
of biodiversity than species extinctions [Ceballos and Ehrlich, 2002]. Likewise, because
L. catta i s k n o w n f o r i t s e c o l o g i c a l f l e x i b i l i t y [ S a u t h e r e t a l . , 1 9 9 9 ] , i t c o u l d b e a p r o x y
for biodiversity loss as its population decline underscores the difficulty that other, less
adaptable species have in overcoming a multitude of threats. As a well-known and fre-
quently encountered species (i.e., globally in zoos, and at select popular tourist sites in
Madagascar), the overarching perception is that L. catta i s n o t g l o b a l l y t h r e a t e n e d , n o r
in imminent threat of extinction. A primate species’ prevalence in the media has been
associated with the belief that wild populations are stable and not threatened by extinc-
tion [Leighty et al., 2015; Nekaris et al., 2016]. This false impression that ring-tailed
lemurs are not threatened with extinction could be devastating for the species (and
larger communities of biodiversity in Madagascar) as it may impede the ability to se-
cure funding for rapid conservation action. That being said, L. catta i s c u r r e n t l y u n d e r
consideration for inclusion in the 2016–2018 “World’s 25 Most Endangered Primates”
listing, which is published bi-annually by the IUCN/SSC Primate Specialist Group
[IUCN, 2016]. Inclusion of ring-tailed lemurs in this list will highlight the threats these
animals are facing and inform the larger conservation community about the fact that
even adaptable, flexible species such as ring-tailed lemurs can experience rapid decline.
Several urgent conservation actions should be considered with regard to protect-
ing L. catta from extinction in the wild. First, it has been suggested that primate pop-
ulations threatened with extinction should be regularly monitored using routine site
visits [Plumptre and Cox, 2006]. For L. catta this monitoring is especially necessary
at sites that have large remaining populations and in areas that are data deficient; a
complete site-based census of L. catta sites is recommended. Second, long-term ge-
netic viability is greater in populations with more individuals [Plumptre and Cox,
2006]. Since there are likely only 8 ring-tailed lemur populations remaining that have
more than 100 individual animals ( Table1 ), these populations should be targeted for
protection in order to maintain genetic diversity of the species. Additionally, reintro-
duction of captive ring-tailed lemurs, particularly those confiscated from the illegal
pet trade [LaFleur et al., 2015] could be used as a mechanism to increase wild genetic
diversity and to repopulate forested areas where populations are now extinct. Rein-
troductions are not without risks however, and comprehensive assessments of both
prospective animals and release sites would need to be carried out, as per IUCN re-
introduction guidelines [IUCN/SSC, 2013]. Third, live capture for the within-coun-
try pet trade poses a significant threat to many lemur species. More than 28,000 le-
murs were kept in illegal captivity between 2010 and mid-2013, and of these ring-
tailed lemurs were the most prevalent, comprising 28% of reported animals [Reuter
et al., 2016]. Information regarding drivers and locations of capture, trade routes, and
absolute numbers of ring-tailed lemurs in the illegal pet trade is imperative to future
conservation initiatives [Reuter and Schaefer, 2016].
Madagascar is one of the world’s poorest countries, and poverty is a significant
predictor of extinction for primate species [Estrada, 2013]. The primary threats to
ring-tailed lemurs, including deforestation and capture for the bushmeat and pet
trades, can each be linked to poverty in that subsistence living depends heavily on
natural resource exploitation [Brimont et al., 2015] and that forest products, includ-
ing lemurs, can be sold to generate income [Gardner and Davis, 2014]. It is critical to
link conservation efforts with social and economic development projects, in order to
ensure that both Madagascar’s human population and wildlife thrive.
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Lemur catta Rapid Population Decrease
329
Folia Primatol 2016;87:320–330
DOI: 10.1159/000455121
Acknowledgements
The authors thank the Government of Madagascar, Ministry of the Environment and Ecol-
ogy of Forests, Madagascar National Parks, the University of Toliara, and MICET, for their per-
missions and facilitations of our research. We also wish to thank Lydia Greene and Holly Schnei-
der-Brown for their dedication to forwarding lemur conservation and awareness. Additionally,
we thank Dr. Anna Nekaris and 3 anonymous reviewers for their feedback, which significantly
improved this paper. Funding was provided by the Margot Marsh Biodiversity Foundation, Mar-
got Marsh Primate Action Fund, Duke University’s Arts and Sciences Council: Committee on
Faculty Research Grant (awarded to T.A.C.), and Lemur Love Inc. private donors.
Disclosure Statement
We understand Folia Primatologica ’s declaration of interests and declare that we have no
competing interests.
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... This study aims to assess the learning experiences available at zoos and their retrospectively quality in terms of knowledge retention: using a well-known species as a case-study: the ringtailed lemur (Lemur catta). Lemurs are the most threatened mammal group (LaFleur, et al., 2017, Estrada, et al., 2017, and are "the single highest conservation priority in the world" (Schwitzer, et al. 2013). ...
... Acting as a flagship species for Madagascar, the ringtailed lemur is the most common lemur kept in captivity (Andriaholinirina, et al., 2014;LaFleur, et al., 2017), with a current captive population totalling 2,500 individuals (ISIS, 2006, in Andriaholinrina, et al., 2014. ...
... 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). ...
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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.
... Ring-tailed lemurs are under severe conservation pressure; they are classified as "endangered" by the International Union for Conservation of Nature (IUCN) [8], resulting primarily from deforestation, hunting, and capture for the pet trade. A recent population census has revealed a dramatic population decline, with as few as 2,200 individuals remaining in the wild [9]. Of further concern, the species is distributed across a highly fragmented range with only 8 populations of ≥100 individuals remaining [9]. ...
... A recent population census has revealed a dramatic population decline, with as few as 2,200 individuals remaining in the wild [9]. Of further concern, the species is distributed across a highly fragmented range with only 8 populations of ≥100 individuals remaining [9]. Despite this near-term population decline, a recent microsatellite analysis indicates that the genetic diversity of L. catta populations could be exceptionally high, with evidence of genetic isolation by distance throughout their geographic range [6]. ...
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Background: The ring-tailed lemur (Lemur catta) is a charismatic strepsirrhine primate endemic to Madagascar. These lemurs are of particular interest, given their status as a flagship species and widespread publicity in the popular media. Unfortunately, a recent population decline has resulted in the census population decreasing to <2,500 individuals in the wild, and the species's classification as an endangered species by the IUCN. As is the case for most strepsirrhine primates, only a limited amount of genomic research has been conducted on L. catta, in part owing to the lack of genomic resources. Results: We generated a new high-quality reference genome assembly for L. catta (mLemCat1) that conforms to the standards of the Vertebrate Genomes Project. This new long-read assembly is composed of Pacific Biosciences continuous long reads (CLR data), Optical Mapping Bionano reads, Arima HiC data, and 10X linked reads. The contiguity and completeness of the assembly are extremely high, with scaffold and contig N50 values of 90.982 and 10.570 Mb, respectively. Additionally, when compared to other high-quality primate assemblies, L. catta has the lowest reported number of Alu elements, which results predominantly from a lack of AluS and AluY elements. Conclusions: mLemCat1 is an excellent genomic resource not only for the ring-tailed lemur community, but also for other members of the Lemuridae family, and is the first very long read assembly for a strepsirrhine.
... conservation genetics, Madagascar, microsatellites, strepsirrhines have lost over 45% of their habitat (Brinkmann, Noromiarilanto, Ratovonamana, & Buerkert, 2014;LaFleur, Clarke, Ratzimbazafy, & Reuter, 2017a); and by 2080, it is estimated that 63% of their remaining range will shift due to climate change alone (Brown & Yoder, 2015). Furthermore, there has been a recent uptick in exploitation for the illegal pet trade, causing severe population declines, and in some cases local extinctions, throughout their remaining geographic range (Gardner & Davies, 2014;Gould & Sauther, 2016;LaFleur, Clarke, Reuter, Schaefer, & ter-Horst, 2019;LaFleur, Clarke, Reuter, & Schaeffer, 2017b;LaFleur & Gould, 2009;Reuter et al., 2019;Reuter & Schaefer, 2016). At present, there are estimated to be fewer than 2,400 individuals within sampled locations (Gould & Sauther, 2016;LaFleur et al., 2017b), though population estimates are still lacking throughout much of their range (e.g., Murphy, Ferguson, & Gardner, 2017). ...
... Furthermore, there has been a recent uptick in exploitation for the illegal pet trade, causing severe population declines, and in some cases local extinctions, throughout their remaining geographic range (Gardner & Davies, 2014;Gould & Sauther, 2016;LaFleur, Clarke, Reuter, Schaefer, & ter-Horst, 2019;LaFleur, Clarke, Reuter, & Schaeffer, 2017b;LaFleur & Gould, 2009;Reuter et al., 2019;Reuter & Schaefer, 2016). At present, there are estimated to be fewer than 2,400 individuals within sampled locations (Gould & Sauther, 2016;LaFleur et al., 2017b), though population estimates are still lacking throughout much of their range (e.g., Murphy, Ferguson, & Gardner, 2017). ...
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Madagascar's ring‐tailed lemurs (Lemur catta ) are experiencing rapid population declines due to ongoing habitat loss and fragmentation, as well as increasing exploitation for bushmeat and the illegal pet trade. Despite being the focus of extensive and ongoing behavioral studies, there is comparatively little known about the genetic population structuring of the species. Here, we present the most comprehensive population genetic analysis of ring‐tailed lemurs to date from across their likely remaining geographic range. We assessed levels of genetic diversity and population genetic structure using multilocus genotypes for 106 adult individuals from nine geographically representative localities. Population structure and F ST analyses revealed moderate genetic differentiation with localities being geographically partitioned into northern, southern, western and also potentially central clusters. Overall genetic diversity, in terms of allelic richness and observed heterozygosity, was high in the species (AR = 4.74, H O = 0.811). In fact, it is the highest among all published lemur estimates to date. While these results are encouraging, ring‐tailed lemurs are currently affected by ongoing habitat fragmentation and occur at lower densities in poorer quality habitats. The effects of continued isolation and fragmentation, coupled with climate‐driven environmental instability, will therefore likely impede the long‐term viability of the species.
... Among other issues were the status of Lemur catta and Propithecus verreauxi and of Lepilemur leucopus in the south of Madagascar. While L. catta and P. verreauxi have a large area of distribution, the actual presence of Lemur catta at many sites within this area of distribution is uncertain and thus the area of occupancy might be substantially smaller that suggested by maps showing the area of distribution (Gould and Sauther, 2016;LaFleur et al., 2016;Murphy et al., 2017). ...
... 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). ...
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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.
... Where disagreements among researchers and those in the conservation community have been unresolved, they have in some cases undermined the list's potential desired impact. For example, ring-tailed lemurs ( Lemur catta ) were included in the 2016-2018 edition following worrying signs of rapid population declines due to drought ( Vyawahere, 2020 ), habitat degradation, and the pet trade ( Gould & Sather, 2016 ;LaFleur, Clarke, Reuter, & Schae er, 2017 ). Ring-tailed lemurs, a fl agship species for the Madagascar tourism industry, have a large range in the country's south. ...
... It seems, however, that the trade in galagos as pets in general is only small scale and often opportunistic, as has been found for the nocturnal pottos and angwantibos (Svensson and Friant 2014). Capture and trade of wild ring-tailed lemurs (Lemur catta) is similarly opportunistic but, once believed to be wide ranging and common, they were estimated to have suffered a population decline of nearly 95% since 2000, mainly driven by bushmeat and the pet trade (LaFleur et al. 2016). ...
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Primates are traded yearly in the tens of thousands for reasons such as biomedical research, as trophies and pets, for consumption and to be used in traditional medicine. In many cases, this trade is illegal, unsustainable and considered a major impediment to primate conservation. Diurnal primates make up the vast majority of this trade, but recent studies have found that the trade in nocturnal primates is more common than previously thought, and among them are the galagos. There are currently 19 galagos recognized but there is still a dearth of research on these species and subspecies. The purpose of our study was to provide a more comprehensive picture of the trade in galagos within and across their African range countries, to help determine whether it is illegal or its sustainability needs to be assessed, and to provide baseline data and management recommendations to better regulate this trade, including strengthening policy, enforcement and conservation interventions. We gathered information on trade and use of galagos using an online questionnaire (May-August 2020), and on country-specific legislation relating to wildlife trade, hunting and legal protection of galagos, and looked at each range country's Corruption Perception Index score to gain an understanding of the obstacles in the way of effective law enforcement. We received 140 responses to our online questionnaire, from 31 of the 39 galago range countries. Respondents from 16 of these countries reported on first-hand observations of galagos being traded or used. Out of these, 36% reported seeing galagos sold or used for consumption, 33% as pets and 25% had observed them sold or used for traditional practices (including medical and magical purposes and for witchcraft). Most reports came from West Africa followed by Central Africa, East Africa and Southern Africa. We found that the number of reports on galagos being traded was higher in countries with higher numbers of galago species. Countries with more restrictive legislation experienced a higher number of reports of trade. Galagos observed in the pet trade was more common in East Africa, whilst reports of them in the bushmeat trade were more common in Central and West Africa. Galagos observed in the trade for traditional practices was by far most common from West Africa. We found that all galago range countries have some level of legal protection for some or all of their native galago species. It is evident that use and trade of galagos occurs throughout their range, albeit localized to certain areas. We urge galago range countries to adequately protect all species and to ensure legal trade is effectively regulated. Range countries that prohibit the use and trade in galagos must ensure legislation is adequately enforced. Further research into the drivers behind the use and trade of galagos should be initiated in countries with high levels of use and trade to further inform conservation and policy actions and to catalyze enforcement actions against poaching and illegal trade.
... The dry forests of Madagascar's southern regions have been reported as the most seriously fragmented forest type in the country, and such fragmentation has occurred due to factors such as extensive slash and burn practices for cattle grazing, charcoal production, and various forms of agriculture (Bodin, Tengo, Norman, Lundberg, & Elmqvist, 2006;Harper, Steininger, Compton, Tucker, & Hawkins, 2007;Sauther et al., 2013;Scott et al., 2006). Such habitat loss, as well as illegal bushmeat hunting for local consumption (Borgerson, McKean, Sutherland, & Godfrey, 2016;Golden, 2009) and capture for the illegal pet trade (LaFleur, Clarke, Reuter, Schaefer, & terHorst, 2019;Reuter, Gilles, Wills, & Sewall, 2016) have resulted local extinctions or drastic reductions of ring-tailed lemur populations in many areas of southern Madagascar where they are or were previously reported (Gould & Sauther, 2016;Kelley, Sussman, & Muldoon, 2007;LaFleur, Clarke, Reuter, & Schaeffer, 2016;Sauther et al., 2013;Sussman et al., 2006). ...
Article
Habitat fragmentation is an increasingly serious issue affecting primates in most regions where they are found today. Populations of Lemur catta (ring-tailed lemur) in Madagascar's south-central region are increasingly restricted to small, isolated forest fragments, surrounded by grasslands or small-scale agriculture. Our aim was to evaluate the potential for population viability of L. catta in nine forest fragments of varying sizes (2-46 ha, population range: 6-210 animals) in south-central Madagascar, using a set of comparative, quantitative ecological measures. We used Poisson regression models with a log link function to examine the effects of fragment size, within-fragment food availability, and abundance of matrix resources (food and water sources) on L. catta population sizes and juvenile recruitment. We found a strong association between overall population size and (a) fragment size and (b) abundance of key food resources Melia azedarach and Ficus spp. (per 100 m along transect lines). Juvenile recruitment was also associated with fragment size and abundance of the two above-mentioned food resources. When the largest population, an outlier, was removed from the analysis, again, the model containing fragment size and abundance of M. azedarach and Ficus spp. was the best fitting, but the model that best predicted juvenile recruitment contained only fragment size. While our results are useful for predicting population presence and possible persistence in these fragments, both the potential for male dispersal and the extent of human disturbance within most fragments play crucial roles regarding the likelihood of long-term L. catta survival. While seven of the nine fragments were reasonably protected from human disturbance, only three offered the strong potential for male dispersal, thus the long-term viability of many of these populations is highly uncertain.
... Current wild ring-tailed lemur populations are facing several anthropogenic threats, with multiple recent studies establishing a severe drop in numbers across 32-34 sites, with at least 12 showing local extinctions of populations LaFleur et al., 2016). An earlier study in 2012 found suggestions of a recent genetic bottleneck, further supporting the concern that ring-tailed lemur populations could become critically endangered (Parga et al., 2012). ...
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Lemurs are naturally endemic to the island of Madagascar. Captive lemur diets generally consist of commercial dry pellets supplemented with vegetables and forages. The dry pellets given are their main source of fibre and are key to ensuring all nutritional requirements are met in a man-made setting. These are often the blandest and least desirable part of the diet, and therefore usually fed first, separately to more palatable foods, and ad lib. Incorrect feeding in captivity for lemurs is a prominent issue seen in many institutions. Enrichment feeds have proven to have a beneficial effect on encouraging natural behaviours, such as grooming and foraging. However, there is minimal research on whether enrichment can be used to affect feed intake. Three species of lemur, the red ruffed lemur (Varecia rubra), the black and white ruffed lemur (Varecia variegate), and the ring-tailed lemur (Lemur catta) were given three different feeding enrichments. Two aims were being investigated: 1) whether presenting dry pellets through enrichment devices changes the overall feed intake in three species of lemur, and 2) whether different enrichment items have different effects on pellet consumption. Results presented no significant change in pellet consumption when fed through enrichment devices for ring-tailed lemurs (p>0.05), which was also the case for both ruffed lemur species (p>0.1). They also distinguished no significant difference between feeding enrichments in pellet intake in any of the three species of lemur. This study helped identify the possibility of using enrichment for pellet consumption in zoos, but showed that the devices used didn’t have a significant enough effect to suggest future implementation of enrichments for the sake of nutrition. Further research is needed to fully understand whether the application of enrichment can be beneficial for encouraging adequate diets in lemurs, and more factors need to be considered, such as species difference in locomotion and enclosure use.
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