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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.
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Original Research Article
Folia Primatol 2019;90:199–214
DOI: 10.1159/000496970
Illegal Trade of Wild-Captured Lemur catta
within Madagascar
Marni LaFleur a Tara A. Clarke b Kim E. Reuter c Melissa S. Schaefer d
Casey terHorst e
a Department of Anthropology, University of California San Diego, La Jolla, CA, USA;
b Department of Evolutionary Anthropology, Duke University, Durham, NC, USA;
c African Field Division, Conservation International, Nairobi, Kenya; d Department of
Anthropology, University of Utah, Salt Lake City, UT, USA; e Department of Biology,
California State University, Northridge, CA, USA
Keywords
Strepsirrhine · Ring-tailed lemur · Pet · Wildlife trafficking · Conservation
Abstract
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. catta with 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 inter-
ventions are urgently needed and could be adapted to protect other exploited wildlife
in the future. © 2019 S. Karger AG, Basel
Received: May 14, 2018
Accepted after revision: January 14, 2019
Published online: May 8, 2019
Marni LaFleur
Department of Anthropology, University of San Diego
5998 Alcala Park
San Diego, CA 92110 (USA)
E-Mail marni.lafleur @ gmail.com
© 2019 S. Karger AG, Basel
www.karger.com/fpr
E-Mail karger@karger.com
Folia Primatol 2019;90:199–214
200 LaFleur/Clarke/Reuter/Schaefer/terHorst
DOI: 10.1159/000496970
Introduction
Approximately 60% of all nonhuman primate species are threatened with extinc-
tion [Graham et al., 2016; Estrada et al., 2017, 2018]. Primate species decline and local
extirpation are attributed to anthropogenic pressures on primates (bushmeat hunt-
ing, capture for biomedical experimentation, exotic pet trade) and their habitats (ex-
tractive industries and agriculture), along with anthropogenic disease transmission
(e.g., Ebola) and climate change [Estrada et al., 2017, 2018; Kalbitzer and Chapman,
2018]. Since human-induced pressures are likely to continue in future, the conserva-
tion status of primates remains precarious, although primate experts are hopeful that
these trends can be reversed [Estrada et al., 2017, 2018; Chapman et al., 2018].
Although the pet trade has long been recognized as a threat to haplorrhine pri-
mates (specifically monkeys and apes) [Soini, 1972; Duarte-Quiroga et al., 2003; Stiles
et al., 2013], these threats have only relatively recently been acknowledged for strep-
sirrhines (lemurs [Reuter et al., 2016], lorises [Nekaris and Jaffe, 2007], and galagos
[Svensson et al., 2015]). Slow lorises are among the most commonly traded primates
in Indonesian areas [Shepherd et al., 2004; Nijman et al., 2017], with several thousand
individuals for sale in certain markets per year [Nijman, 2010]. Moreover, slow lo-
rises gained popularity as pets after a youtube video “Tickling slow loris” went viral
in 2009 [Nekaris et al., 2013]; they are now traded across Asia and beyond [Nekaris
and Jaffe, 2007; Nekaris et al., 2010]. Additionally, the trade of African lorisiforms
(galagos, pottos, angwantibos) appears to be widespread, as a recent online survey
reports records from at least 24 African countries [Svensson et al., 2015]. Similarly,
within Madagascar, an estimated 28,000 lemurs were kept as illegal pets in urban ar-
eas across the island between 2010 and mid-2013 [Reuter et al., 2016].
Lemurs are the most threatened group of mammals on earth, with 94% of lemur
species at risk of extinction [Schwitzer et al., 2014]. A variety of direct actions and
indirect circumstances have led to most lemur species being threatened with extinc-
tion. Direct actions include extensive habitat destruction [Mittermeier et al., 2006],
bushmeat hunting [Barrett and Ratsimbazafy, 2009], and the pet trade [Reuter et al.,
2016, 2017]. Circumstances contributing to the decline of lemurs include widespread
poverty, which leaves millions of people dependent on forest resources for survival
[Schwitzer et al., 2014], political instability, corruption, and lack of effective environ-
mental law enforcement [Reuter et al., 2017].
Tourism is an important source of revenue for Madagascar [Schwitzer et al.,
2014]. Several national parks, protected areas, and private reserves are within an
hour’s drive of Madagascar’s capital city, Antananarivo, which enables thousands of
tourists to view lemurs per year [see Mittermeier et al., 2006]. Common tourist ac-
tivities, such as direct contact with lemurs for photo opportunities, take place in the
vicinity of these parks and reserves and may be detrimental to lemur populations
[Reuter and Schaefer, 2016a, b; Reuter et al., 2017], as these animals are likely wild-
caught. Furthermore, lemurs are often illegally wild-caught in order to supply some
resorts and roadside zoos with “added value attractions”, wherein naïve tourists sup-
port the practice through direct payment or by patronizing establishments keeping
lemurs [Reuter and Schaefer, 2016a, b]. Wild-captured animals are then no longer
providing ecosystem services to their native forests (e.g., seed dispersal) or contrib-
uting to wild populations through reproduction, both of which are important to spe-
cies facing extinction. Few entities in Madagascar hold permits to legally keep lemurs
Illegal Pet Lemur catta
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DOI: 10.1159/000496970
in captivity, and no existing regulations require legal facilities to display permissions
to patrons.
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 Schae-
fer, 2016a, b]. Estimates from the years 2016 and 2017 indicate that sharp and con-
tinued declines threaten L. catta populations [Gould and Sauther, 2016; LaFleur et al.,
2017, 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 particu-
larly 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., 2017, 2018; but see Murphy et al., 2017].
We examined interviews and web-based surveys specific to the trade of L. catta
within Madagascar. We specifically focus on illegal captivity, which excludes facilities
such as Tzimbazaza Zoo, Park Ivoloina, Lemurs’ Park, and others with express per-
mission to capture and/or keep lemurs within Madagascar. Based on our observa-
tions, we made several predictions about the circumstances under which L. catta
would be found. For example, since pet lemurs are often associated with tourists, we
predict that they will be reported more frequently in tourist destinations, associated
with businesses catering to tourists, and kept for the purposes of generating income
resulting from tourists. Moreover, based on our personal experiences of seeing pet
lemurs in Madagascar, we expect that owners of lemurs will be Malagasy. Addition-
ally, because of the costs associated with caring for a pet, we expect that lemur owners
will be perceived as wealthy by respondents. We also expect that the trade in L. catta
has increased over time and use modeling data along with other known threats to as-
sess the sustainability of live extraction of this species. L. catta conservation will de-
pend on these data, as the information can aid in determining motivations for cap-
ture, ownership, and sale. Subsequently, targeted conservation action can be deployed
which addresses root causes of the trade.
Methods
We collected data in two ways, via: (1) in-person interviews and (2) the Pet Lemur Survey
(www.petlemur.com), a web-based survey for sightings of pet lemurs [Reuter and Schaefer 2016a,
b; Reuter et al., 2016]. We carried out the in-person interviews at households in central, western,
and northern Madagascar in 2013, and households in central, eastern, and southern Madagascar
in 2016. Both the in-person interviews and web-based surveys broadly asked the same basic ques-
tions regarding pet lemurs in Madagascar, and the full methods and data collection protocols are
described in Reuter et al. [2016] and Reuter and Schaefer [2016a, b].
By 2016, the combined data set consisted of 1,374 reports of captive lemur sightings, includ-
ing lemurs from 32 species. Most of these captive lemur sightings were reported by individuals
who did not own the lemur. Therefore, some of the information recorded in this database (such
as whether or not the owner of the lemur was wealthy) was subjective.
Within the database of 1,374 reports, 232 reports were specific to L. catta, though it is clear
that some of these reports are of the same captive lemur (despite being reported by different re-
spondents). This risk of “double-counting” of lemurs within the data set was noted in Reuter and
Folia Primatol 2019;90:199–214
202 LaFleur/Clarke/Reuter/Schaefer/terHorst
DOI: 10.1159/000496970
Schaefer [2016b] and in Reuter et al. [2016]. Therefore, we took several steps to identify and
eliminate duplicate reports in our data set. This included first removing any reports that did not
have the following data with reference to the L. catta sighting: year, town, environment (business,
residence, other), and method of confinement (cage, tether, etc.). The remaining 180 reports were
then carefully analyzed and compared to determine which records likely described unique L.
catta sightings. We considered the aforementioned variables (year, town, environment, method
of confinement), as well as other factors, when applicable. These included the name of the hotel
or business, the number of animals observed together, the animals’ age (juvenile or adult), and/
or the purpose of the pet lemur (personal pet, to make money from tourists, etc.). If we could not
ascertain that a report represented a unique animal with reasonable certainty, the account was
removed from the data before further analyses were performed. Sample sizes vary between certain
aspects of survey information, because respondents could choose to not respond to any question
asked.
Of the pet L. catta identified we examined the relative numbers of individuals according to
the following variables: location, purpose of lemur, nationality and perceived wealth of owner,
and trends and sustainability of the trade. We used the χ2 test to check the goodness of fit of our
actual and expected sightings of pet lemurs each month of the year. We further used the F distri-
bution (two-tailed) to analyze variance between the adult and juvenile L. catta sightings by envi-
ronment type (business, residence, other), mechanism of confinement (cage, tether, no cage or
tether, other), and the purpose of the lemur (personal pet, to make money, no purpose, other).
Respondents were not explicitly asked whether a lemur was a juvenile/infant or an adult; this in-
formation was recorded only when it was offered by the respondent (n = 18). p values were set to
0.05 in all cases.
We use a stage-structured transition matrix (i.e., Leftkovitch matrix) to determine the ef-
fects of capture of L. catta females [Bradford and Hobbs, 2008]. There are six biologically mean-
ingful (i.e., those known to affect survival and reproduction) stages in our matrix including: in-
fant/juvenile (under 1 year of age), 1-, 2-, 3-, 4-year-olds, and adults (5–15 years old). In order to
understand the effects of population size, we use the hypothetical population sizes of 500, 2,500,
5,000, and 10,000 individual L. catta.
We base the number of individuals in each stage on the hypothetical population sizes, stage-
specific survivorship and reproduction [Koyama et al., 2001, 2002; Gould et al., 2003], and extrac-
tion rates from the years 2011–2016 (detailed here). The dominant eigenvalue of our matrix rep-
resents the population growth rate, λ. Values of λ greater than 1 indicate an increasing popula-
tion; values less than 1 indicate a decreasing and unsustainable population.
Results
We determined that 180 reports detailing 286 individual L. catta were likely
unique (Fig.1). The reports of these animals had unique characteristics that did not
match any other reports. To illustrate, they may have been held at a certain named
business location with a specified method of confinement, and these characteristics
were not found in any other report.
Location and Purpose of Lemurs
Most L. catta were observed in Toliara (62, 22%), Anakao (49, 17%), and Fort
Dauphin (34, 12%) (Fig.2). Others were reported in Ambalavao (16, 6%), Antsirabe
(3, 1%), Antananarivo (11, 4%), Fianarantsoa (16, 6%), and all other locations
throughout the island (95, 33%). Juvenile lemurs were most reported in Anakao (9
out of 17 records of juveniles, 53%) (Fig.2). Nearly half of the L. catta (140, 49%) were
viewed in businesses (e.g., hotel resort, restaurant, etc.), while the rest were observed
in residences (110, 38%) and other locations (36, 13%), which included “on the
Illegal Pet Lemur catta
203
Folia Primatol 2019;90:199–214
DOI: 10.1159/000496970
1,374
reports
232
reports
476
individuals
180 reports
Unique ring-tailed lemurs
Ring-tailed lemurs
Pet Lemur Survey:
in-person interviews and web-based surveys
286 individuals
2,201
lemurs
from 32
species
Fig. 1. Overview of Pet Lemur
Survey including the num-
bers of reports and individual
Lemur catta identified.
Antsiranana Antsiranana
Mahajanga Mahajanga
Toamasina Toamasina
Antanarivo Antanarivo
Toliara Toliara
Fianarantsoa Fianarantsoa
0 100 200 300 400 km
Sightings of captive juvenile
Lemur catta
Provinces
Sightings of captive Lemur catta
1
2
3
Provinces
Fig. 2. Maps of Madagascar showing locations of captive Lemur catta. Numbers 1–3 indicating
the locations with the most lemurs (1, Toliara; 2, Anakao; 3, Fort Dauphin). Dots are sized in
proportion to the number of L. catta with larger dots indicating more lemurs.
Folia Primatol 2019;90:199–214
204 LaFleur/Clarke/Reuter/Schaefer/terHorst
DOI: 10.1159/000496970
beach”, “on the street”, and simply “other” nonbusiness or residential locations. The
purpose for keeping the L. catta was reported as income generation (117, 48%, both
direct and indirect income generation), as a personal pet (113, 46%), or that it did not
serve a purpose (13, 5%). In 15% (37) of responses, the purpose of the lemur was not
specified.
Nationality and Perceived Wealth of Lemur Owners
When respondents reported the nationality of the owners (178, 63%), these were
most often Malagasy (132, 73%), while some were foreigners (46, 26%), and a small
percentage were reported as being both Malagasy and foreigner (2, 1%), for example,
when the lemur was owned by a couple in which one individual was Malagasy and
the other was a foreigner. In addition, owners of L. catta were perceived by respon-
dents as being wealthy (140, 77%), although some were said to have “middle” wealth
(5, 4%), and some were not thought of as wealthy (6, 19%).
Trends and Sustainability of Lemur Trade
The year when an L. catta was witnessed by a respondent was reported in 286
cases (100%) and L. catta sightings were examined. Most L. catta were reported from
the years 2011–2016 (184, 64%), then 2005–2010 (57, 20%), and finally prior to 2005
(45, 16%) (Fig.3). The month in which an L. catta was spotted was known for 77 of
the sightings. The majority of juvenile L. catta (7 of 17 records, 41%) were witnessed
by respondents in the month of December, while the largest percentage of adults were
observed in July (13, 17%) (Fig.4).
Respondents indicated that many of the pet L. catta were still owned or still alive
in captivity (49, 43%). Some L. catta had been disposed of in some way (27, 34%; es-
caped, sold, released into the wild), died (14, 17%; natural and intentional deaths), or
Ambalavao
(Fianarantsoa)
Anakao
(Toliara)
Antsirabe
(Antananarivo)
Antananarivo
(Antananarivo)
Fianarantsoa
(Fianarantsoa)
Fort Dauphin
(Toliara)
Toliara
(Toliara)
Other
town/village
100
%
90
80
70
60
50
40
30
20
10
0
Before 2005 2005–2010 2011–2016
Sum of the number of lemurs by town
Fig. 3. Location (by town and province) of captive Lemur catta reported to the Pet Lemur Survey
before 2005, from 2005 to 2010, from 2011 to 2016, and the sum of all reported lemurs regardless
of date.
Color version available online
Illegal Pet Lemur catta
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DOI: 10.1159/000496970
were confiscated by authorities (4, 5%). Individuals with a history of aggression (33,
33%) were less likely to be still owned by the same person (χ2 test, df = 1, p value
<0.001) (Fig.5).
As expected, larger population sizes have higher population growth rates. Ad-
ditionally, increased capture rates slow overall population growth. In all but one sce-
nario (with the smallest population, below), populations were still able to grow de-
spite “captures”; however, the growth rate depends on the population size, extraction
age class focus, and extraction rate in these instances. Population decline occurred
only in the smallest population (n = 500) which had 10% extraction that targeted in-
fant/juvenile animals (Table 1).
January
February
March
April
May
June
July
August
September
October
November
December
14
n
12
10
8
6
4
2
0
Adult (n = 77) observed Juvenile (n = 17) observed
Fig. 4. Month of sighting for adult and juvenile Lemur catta.
Color version available online
Still owns
46.7
10.5
Doesn’t own
89.5
100
%
90
80
70
60
50
40
30
20
10
0
No aggression Aggression
53.3
Fig. 5. Percentage of ring-
tailed lemurs that are or are
not still cared for by the same
owner, according to reported
incidences of aggression (still
owned by owner, n = 16; no
longer owned, n = 33).
Color version available online
Folia Primatol 2019;90:199–214
206 LaFleur/Clarke/Reuter/Schaefer/terHorst
DOI: 10.1159/000496970
Discussion
Our database documents 286 different L. catta in captivity in Madagascar of
which 184 unique individuals were reported between 2011 and 2016. In addition, our
database includes 18 juvenile animals (17 are included in analyses, as one of the juve-
niles did not have a location within the report), some of which undoubtedly died
shortly after being observed by Pet Lemur Survey respondents (see below). Our da-
tabase does not include an exhaustive list of all L. catta kept in illegal captivity in
Madagascar and is therefore an underestimation of the total number of L. catta that
have been extracted from the wild for the pet trade in recent years.
Hot spots for pet L. catta included Toliara, Anakao, and Fort Dauphin. Each of
these locations are popular tourist destinations within the natural range of L. catta
[Goodman et al., 2006]. Illegal trafficking of primates for the purposes of tourist in-
teractions have been documented with slender lorises (Loris spp.) in India [Kanaga-
vel et al., 2013], tarsiers (Carlito syrichta) in the Philippines [Yang-Martinez, 2011],
barbary macaques (Macaca sylvanus) in Morocco [Bergin and Nijman, 2014], and
white-handed gibbons (Hylobates lar) in Thailand [Grey, 2012; Osterberg et al.,
2015]. In these locales, tourists often seek encounters with wildlife, including pri-
mates, so that they can take photographs for sharing via social networks [Osterberg
and Nekaris, 2015]. Using primates as photo props for tourists has presented threats
to primates in the past [Clark, 1997] but may be increasing in popularity and can be
lucrative for primate traffickers [Goodman, 1993; Svensson and Friant, 2014; Oster-
berg and Nekaris, 2015; Nijman and Healy, 2016].
In our study, we found that half (49%) of the L. catta reported in our database
were observed in businesses (e.g., hotels, restaurants) and were perceived to serve the
purpose of generating income. In comparison, when all lemur species were aggre-
gated together, they were kept for money-making purposes just 20% of the time
[Reuter and Schaefer, 2017]. It may be that L. catta are used for money-making pur-
poses more often than other lemur species because they are well known and easily
recognizable. L. catta are commonly kept in zoos globally and are an iconic species in
Madagascar and are often used on billboards and other advertisements targeting
Table 1. Population growth rates for ring-tailed lemurs for differing population sizes
Ring-tailed lemurs captured per year λ
(n = 500)
λ
(n = 2,500)
λ
(n = 5,000)
λ
(n = 10,000)
None 1.24 1.69 1.93 2.22
1.5% of population 1.23 1.66 1.90 2.19
10% of population (any age class) 1.12 1.52 1.74 2.00
10% of population (adult age class only) 1.18 1.60 1.83 2.12
10% of population (infant/juvenile age
class only) 0.83*1.11 1.26 1.43
n = 500, 2,500, 5,000, and 10,000 and scenarios with capture rates ranging from none to 10% of known remaining
populations, per year, noting differences in adult and infant/juvenile age classes at 10% extraction. *Indicates popula-
tion decline.
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tourists [M.L., pers. observation]. Recognition of this charismatic species likely makes
them attractive to tourists and, in turn, local entrepreneurs.
Captive L. catta can be a source of both direct and indirect income. For example,
patrons (including foreign tourists) may pay directly to interact with the animal
(sometimes with the promise of photo opportunities) [LaFleur et al., 2015] or may
simply patronize businesses, such as restaurants, that keep captive L. catta [Good-
man, 1993; Reuter and Schaefer, 2016a, b]. People who own L. catta charge between
30 cents and 3 USD for photos or a chance for an up-close interaction [LaFleur et al.,
2015]. Keeping illegal captive lemurs can be especially profitable for hotels; hotels
in Madagascar that advertised having captive lemurs on their websites or social me-
dia pages, charged an average of USD 25.69 more per night than those that did not
[Reuter and Schaefer, 2016b].
In addition to income generation or business promotion, L. catta are also kept
as personal pets. Nonhuman primates are kept as pets globally, for a variety of reasons
including for religious beliefs [see Nijman and Healy, 2016], as a symbol of wealth
and status [Svensson and Friant, 2014], or because they are considered companions
or are generally pleasing to be around [Duarte-Quiroga and Estrada, 2003; Reuter and
Schaefer, 2017]. Most of the L. catta owners identified here were Malagasy and were
perceived as being relatively wealthy. This suggests that having lemurs may demon-
strate wealth or social status, as was indicated by some respondents of Pet Lemur
Survey. It may also indicate that people without relative wealth may not be able to
keep captive lemurs, given the expenses associated with keeping and feeding these
animals.
L. catta having a history of aggression were far less likely to continue to be owned
by the same person. Aggressive and other abnormal behaviors are common in wild-
caught captive L. catta, particularly after the animals reach sexual maturity (3–4 years
of age) [LaFleur et al., 2015]. These aggressive animals often become a nuisance to
their owners and the owners’ neighbors, as they may bite or lunge at those living in
close proximity [LaFleur et al., 2015]. Aggressive lemurs may be given away, released,
caged, abused, or even killed for their perceived bad behavior. Anecdotally we have
been told of L. catta having tails or fingers amputated, or bones intentionally broken,
as a result of aggressive behavior, and have also observed rescued L. catta with indica-
tions of amputations/abuse. Physical repercussions by owners for biting humans or
aggressiveness towards humans have also been noted for wild-caught capuchins (Ce-
bus apella margaritae) in Venezuela [Ceballos-Mago and Chivers, 2010], and wild-
caught spider and howler monkeys (Ateles geoffroyi, Alouatta pigra, and A. palliata)
in Mexico [Duarte-Quiroga and Estrada, 2003].
Restricted annual reproduction in L. catta results in births during late September
and early October of each year, while weaning generally takes place in February and
March [Sauther et al., 1999] but can be as late as May [M.L., pers. observation]. Juve-
nile captive L. catta were (42% of 17 sightings) witnessed in the month of December.
This could be because (1) infants being targeted for extraction at or before the peak
of the tourist season in December, (2) more respondents are viewing and reporting
the infants during this high season for tourism. Anecdotal reports indicate that when
cruise ships dock in Anakao, men from the village make day trips to forested areas,
such as Tsimanampesotse National Park, to collect infant L. catta. This suggests that
infants are specifically targeted but should be investigated further to disentangle the
effect of increased respondent presence. Captured infants may be unlikely to survive
Folia Primatol 2019;90:199–214
208 LaFleur/Clarke/Reuter/Schaefer/terHorst
DOI: 10.1159/000496970
because they are dependent upon their mothers for milk until at least the month of
February. In fact, several respondents noted poor condition of the juvenile lemurs
and used the following words to describe the juvenile lemur’s condition: “dehydrat-
ed”, “dirty”, “floppy”, and “near death”. Although we expect increased mortality in
wild-captured infants who are not yet weaned, this will be important to explore in
future, as we do not currently have evidence to support this claim directly. Targeted
infant extractions can have negative implications for threatened species, as they can
disrupt the normally occurring age and sex structures of populations and thus impede
population growth or maintenance [Ceballos-Mago and Chivers, 2010].
Our transition matrix data suggest that extraction of up to 10% of L. catta popu-
lations (with 500, 2,500, 5,000, and 10,000 individuals) per year will still allow for
positive population growth. Population growth is significantly curtailed when in-
fants/juveniles are targeted and becomes negative in the case of the smallest popula-
tion (n = 500). 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., 2017, 2018; Murphy 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). Thus, if animals are being taken from populations
with 500 or fewer individuals remaining (which the vast majority likely are), and in-
fants/juveniles are targeted (which we have presented evidence for here), even extrac-
tion of 10% will prohibit population growth in each of the populations. Second, ex-
traction rates are likely higher than what we have documented, simply because our
sample effort is insufficient and also because captured infant lemurs may die within
the first week following capture [see Reuter et al., 2016] and are thus not likely to be
observed (and subsequently reported, for the purposes of this study). Third, live cap-
ture for the pet trade is not the only threat that L. catta are facing. L. catta populations
have experienced dramatic declines in the last three decades [Goodman and Rase-
limanana, 2003; Sussman et al., 2006; Kelley et al., 2007; Gould and Sauther, 2016;
LaFleur et al., 2017, 2018; but see Murphy et al., 2017], resulting from habitat degra-
dation and destruction [Brinkmann et al., 2014], bushmeat hunting [e.g., Sussman et
al., 2006], and live capture for the pet trade [LaFleur et al., 2015; LaFleur et al., 2017,
2018]. The combination of small isolated remaining populations along with existing
threats L. catta is facing may simply be more than they can persist under, despite be-
ing a resilient species.
What Can Be Done?
Educating Tourists and Promoting Primate-Friendly Tourism
Many tourists who visit Madagascar seek up-close experiences with lemurs, yet
few are aware of the negative impacts that their actions may have on wildlife [Moor-
house et al., 2015]. Tourists, who may have little knowledge of the conservation status
of nondomestic animals, often rely on the information provided by destination guides
or staff assuming that regulating bodies oversee wildlife interactions [Moorhouse et
al., 2017]. Destination guides and/or staff may not have correct information or might
be willing to share information that they believe tourists want to hear, and regulating
Illegal Pet Lemur catta
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Folia Primatol 2019;90:199–214
DOI: 10.1159/000496970
bodies may not be in place or effective at protecting wildlife. Moreover, L. catta and
other iconic animals that are prevalent in media are less likely to be thought of as
threatened by extinction [Leighty et al., 2015; Courchamp et al., 2018]. This combina-
tion of factors wherein tourists are motivated to seek close encounters with wildlife,
yet have little information on the negative effects their interactions may have, can
significantly impact the conservation of certain species, such as L. catta.
Given the apparent link between L. catta extraction from the wild and tourism,
it is important to decrease the tourist demand to interact with wildlife in nonnatural
environments [Sablich, 2016]. Steps have already been taken at the international
scale; for example, TripAdvisor [2018] – a popular travel-booking service – an-
nounced in October 2016 that it would stop selling tickets for wild animal attractions
involving endangered species [Sablich, 2016]. At the national scale, no outreach cam-
paigns have targeted foreign and/or domestic tourists, other than our recent pilot
project entitled “keeping lemurs wild”. Tourist education and awareness initiatives
are imperative for decreasing demand for direct human-lemur interactions, and
therefore indirectly decreasing the illegal capture of lemurs from the wild. Ideally,
outreach campaigns would ensure that tourists cease to patronize establishments that
are exploiting lemurs and stop paying to interact or take photographs of/with ille-
gally held captive lemurs. Moving forward, information on ethical interactions with
lemurs should be made widely available, even before a tourist arrives in Madagascar
(e.g., via guidebooks, on websites such as TripAdvisor, on in-flight magazines). Post-
ers and leaflets would also be useful at large international entry points (such as air-
ports), from the Madagascar Office of Tourism, and through tourist-centric print and
digital media.
Educating Locals, Mobilizing Law Enforcement, and Caring for Confiscated
Lemurs
Many people in Madagascar seem to be aware that having a captive lemur is il-
legal [Reuter et al., 2016] but enforcement of the law is low; this is notable given that
three quarters of the owners of L. catta were Malagasy. Knowledge alone is not a suf-
ficient deterrent to harboring illegal lemurs and neither are the current enforcement
mechanisms, which are unlikely to be changed in the coming years (national enforce-
ment of lemur hunting bans is considered unlikely) [Sommerville et al., 2010]. Mala-
gasy people generally believe that lemurs are plentiful and not threatened by extinc-
tion, despite the fact that policymakers at national and international levels believe
lemurs to be under extreme danger of extinction [Gore et al., 2016]. This low per-
ceived threat by local people is a barrier to effective management, and important to
address in communications, outreach, and/or education activities [Britt et al., 2004].
Decreasing extraction of wild caught lemurs in this context requires a multi-pronged
approach that includes: (1) general outreach to the public; (2) outreach and capacity
building within government and enforcement agencies; and (3) increased enforce-
ment and prioritization of this issue by the government (including not just enforce-
ment of the law, which can include fines, jail time, and confiscation of the lemur, but
also planning for lemur well-being after confiscation).
Although increased enforcement is necessary to reduce the illegal trade of wild
lemurs, very few legal captive facilities in Madagascar are capable of hosting confis-
cated lemurs and, to our knowledge, none of these entities has successfully released
L. catta back into the wild. This may be because captive lemurs (who were likely cap-
Folia Primatol 2019;90:199–214
210 LaFleur/Clarke/Reuter/Schaefer/terHorst
DOI: 10.1159/000496970
tured at a young age) are not likely to possess the skills necessary for wild survival
[Britt et al., 2004] and because reintroduction into the wild requires significant invest-
ment of resources. Moreover, since only a few captive facilities in Madagascar care
for confiscated or abandoned captive lemurs (ONG Reniala Lemur Rescue Center;
Reniala at SIB Mahajanga), a large number of newly confiscated animals could not
realistically be accommodated by existing facilities. Therefore, while reintroduction
of rehabilitated captive lemurs (i.e., those that have acquired the skills necessary for
wild survival) could be a viable solution for some confiscated animals, this is a long
and expensive process that will likely have only limited success. Efforts should be con-
centrated on preventing further wild capture, given the complications and difficulties
associated with rehabilitation and reintroduction of former pets.
Alternative Means of Income Generation
Madagascar is plagued with extreme poverty, particularly in the southwestern
regions of the country, where drought and famine are common. Alternative and sus-
tainable mechanisms of income generation may be a viable means of offsetting lost
opportunities to individuals who would otherwise capture or purchase L. catta for the
purpose of earning money. In Zambia, individuals specifically responsible for high
levels of natural resource depletion were trained in alternative income generation
(food production and sale), which led to increased biodiversity conservation [Lewis
et al., 2011]. Possible alternatives could include training in the production of sustain-
able handcrafts, specifically those with a low skill entry point and that require little
upfront investment. The production and sale of beaded craft items by Maasai have
been effective in conserving wildlife in Kenya [van Vliet, 2011].
For businesses that keep lemurs, a different strategy is required, since owners are
not likely to be motivated by earning relatively small amounts of money. One poten-
tial solution that has been proposed by Lemur Love, an NGO working in Madagascar
(M.L. is affiliated with this NGO), is a “Lemur Alliance” whereby businesses volun-
tarily pledge to not keep illegal lemurs, in exchange for listings in “lemur-friendly”
business directories. As tourists become more aware, they could seek out and primar-
ily patronize businesses that are listed, thus giving the businesses a competitive ad-
vantage through their Lemur Alliance membership. TripAdvisor has implemented a
program to help potential patrons identify eco-friendly hotels [TripAdvisor: Green
Leaders, 2018]. To our knowledge no such program exists to help tourists identify
businesses that protect wildlife, but this has the potential to be a significant motivator
for certain clientele.
Conclusions
Primates face many anthropogenic threats to their survival. Strepsirrhines are
wild-captured and kept in captive environments. Wild capture both for income gen-
eration and personal ownership poses threats to many lemur species, and particu-
larly L. catta, which are the most frequently reported pet lemur. L. catta have experi-
enced dramatic declines in their range and population numbers and extirpations in
the wild [Goodman and Raselimanana, 2003; Sussman et al., 2006; Kelley et al., 2007;
Gould and Sauther, 2016; LaFleur et al., 2017, 2018; but see Murphy et al., 2017],
animals may suffer low survivorship after capture (although this should be confirmed
Illegal Pet Lemur catta
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DOI: 10.1159/000496970
with future research) [LaFleur et al., 2015], and among those surviving, many have
poor-quality lives and may not be suitable for wild release [Reuter and Schaefer,
2016b]. Conservation actions focused on tourist education, enforcement of Malagasy
law, and development of alternative economic livelihoods at the individual and busi-
ness levels are promising directions for reducing the illegal capture and trafficking of
lemurs. These interventions are urgently needed and could be adapted to protect
other exploited wildlife in the future.
Acknowledgments
We first thank all of the individuals who voluntarily provided information for this study.
The authors thank the Government of Madagascar, Ministry of the Environment and Ecology of
Forests, Madagascar National Parks, the University of Toliara, and MICET, for their permissions
and facilitations of our research. Many thanks to GERP (Groupe d’étude et de recherche sur les
primates de Madagascar), Association Mitsinjo, the Sainte Luce Reserve, and to Conservation
International for facilitating research in some of the towns visited in 2016 survey efforts. We also
wish to thank Lydia Greene and Holly Schneider-Brown for their dedication to forwarding lemur
conservation and awareness, and Toby Schaeffer for the production of maps for this manuscript.
Additionally, we thank Anna Nekaris (academic editor), and anonymous reviewers for their feed-
back, which significantly improved this paper.
Statement of Ethics
We followed international standards of research ethics, and research protocols were re-
viewed and approved by an ethics oversight committee (University of Utah Institutional Review
Board). All researchers completed ethics training through the Collaborative Institutional Train-
ing Initiative. This research did not involve work on animals. All laws relevant to the survey of
adult populations were followed.
Disclosure Statement
The authors have no conflicts of interest to declare.
Funding Sources
Funding for this project was generously provided by the Margo Marsh Biodiversity Founda-
tion (ML 2016–2017, TAC 2017–2018) and the National Geographic Society (KER C313-15).
Author Contributions
Author contributions are as follows: conception (K.E.R.); data collection, analyses, and in-
terpretation (all authors), drafting manuscript (M.L.), critical revision and final approval (all au-
thors).
Folia Primatol 2019;90:199–214
212 LaFleur/Clarke/Reuter/Schaefer/terHorst
DOI: 10.1159/000496970
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... bcftools/bcftools.html) and masked repetitive regions (3). We performed genotypic resistance testing using Mykrobe Predict version 0. 8 Human TB isolates in the region of Toliara most frequently belong to lineage 1 (Institut Pasteur de Madagascar, unpub. data). ...
... However, lineage 3 isolates were previously isolated in humans from other regions of Madagascar (7). Pet lemurs are transported over vast distances (8,9); this lemur may have originated or been transferred from another region of Madagascar. The Malagasy lineage 3 profile shares similarities with strains found in Tanzania and the Indo-Pakistanese subcontinent (7). ...
... Illegal trade of wild-captured lemurs is rampant in Madagascar (8,9). Moreover, humans are frequently in close contact with pet or tourist facility-based lemurs. ...
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Tuberculosis (TB) is an ancient disease affecting a plethora of domestic and wild animals, including humans. In primates, TB can cause severe multisystemic disease. The prevalence of TB in lemurs within Madagascar is unknown; the most recent documented case occurred in 1973 (1). Reverse zoonotic transmission of TB can occur when nonhuman primates are in close contact with humans (1). We report a clinical case and genomic analysis of TB infection in a female subadult ring-tailed lemur (Lemur catta) held at a nongovernmental organization facilty in southwestern Madagascar. The University of San Diego (San Diego, CA, USA) provided ethics authorization (no. IACUC 0619-01).
... Such inconsistencies raise questions about the commonly held view that greater alpha diversity is both a hallmark of wild individuals and a proxy for a healthier gut community [78][79][80][81][82]. Although we did not assess gut health, we note that pet lemurs are prone to disease [83][84][85]. Often housed solitarily indoors, in close contact with people and domestic animals, pet lemurs are fed diets of rice and fruit; yet, their gut consortia were as diverse as those of wild lemurs living at the relatively pristine setting, IVO. Moreover, C U.S. lemurs from the DLC and NCZ had diverse gut consortia, on par with that seen in the most diverse W M lemurs (e.g., in BEZ lemurs). ...
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Background Inter-population variation in host-associated microbiota reflects differences in the hosts’ environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes—an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur ( Lemur catta ; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used microbial source tracking to examine covariation between the two types of consortia. Results The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or environmental condition. Variation in microbial composition was inconsistent both with a single, representative gut community for wild conspecifics and with a universal ‘signal of captivity’ that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between gut and soil microbiota. Conclusions As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple ‘captive vs. wild’ dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.
... 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.
... With the increasing occurrence of illegal incidents such as meat fraud and adulteration or illegal trade of protected animals (Cawthorn et al., 2013;Tibola et al., 2018;LaFleur et al., 2019), it is fundamentally important in forensic genetics to be able to identify the animal species in an unknown sample. Compared to morphological observation and protein-based method, DNAbased method is regarded as one of the most suitable techniques for species identification due to their tolerance for heat or other environmental influences. ...
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New genomic technologies have already had an immense impact on the study of all areas of human genetic diversity including forensics. Major improvements in diverse forensic areas ranging from prenatal parentage testing to biographic ancestry determination are now within our grasp. The new generation of sequencing technologies has allowed additional information to be gleaned from traditional forensic genetic markers (STRs, mtDNA, Indels, SNPs) and their analyses. For example, SNP-based microhaplotypes are a new type of marker made possible by sequencing. These new technologies and knowledge being accumulated allow accurate DNA-based inference of key physical traits of a given individual. Not only DNA analyses already allow the unique assignment of a given sample to a single individual, but now also they enable estimation of the basic physical characteristics (eye/hair/skin color, age, etc.) and ethnic/biographic ancestry of that individual. Thus, the concept of the biological witness has emerged, where the initial determination of the offender’s phenotype may help steer the forensic investigation in the right direction when no case-specific reference samples are available. Ongoing research is improving the amount and accuracy of the potential inferences that can be drawn from a given DNA sample. For example, the need to have reference databases of normal/control individuals has led to an increase in the amount of genetic data available on many dozens of populations from around the globe, and this wealth of data also had a positive impact on molecular anthropology. The growing number of allele frequency data for diverse reference populations has, in turn, facilitated better estimates of biogeographic ancestry of individuals. The denser global coverage of haplotypes has also led to a better understanding of human population genetics. Many facets of human identification in a forensic context overlap with aspects of human population genetics and molecular anthropology. This overlap is an active research area and this Research Topic to bring together manuscripts on many current and emerging trends.
... Across their natural range, ring-tailed lemurs live along a gradient of disturbance from near-pristine forests, that have minimal human activity, to degraded habitats with heavy human encroachment, including logging, agricultural land use, and hunting. Similarly, captive ring-tailed lemurs live under conditions that range from naturalized settings (e.g., social housing in natural habitat enclosures) to artificial settings, some even living solitarily, as pets, in human dwellings, where they experience consistent human contact and substandard conditions (Reuter et al., 2015;Reuter and Schaefer, 2016;LaFleur et al., 2019). ...
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The overuse of man-made antibiotics has facilitated the global propagation of antibiotic resistance genes in animals, across natural and anthropogenically disturbed environments. Although antibiotic treatment is the most well-studied route by which resistance genes can develop and spread within host-associated microbiota, resistomes also can be acquired or enriched via more indirect routes, such as via transmission between hosts or via contact with antibiotic-contaminated matter within the environment. Relatively little is known about the impacts of anthropogenic disturbance on reservoirs of resistance genes in wildlife and their environments. We therefore tested for (a) antibiotic resistance genes in primate hosts experiencing different severities and types of anthropogenic disturbance (i.e., non-wildlife animal presence, human presence, direct human contact, and antibiotic treatment), and (b) covariation between host-associated and environmental resistomes. We used shotgun metagenomic sequencing of ring-tailed lemur (Lemur catta) gut resistomes and associated soil resistomes sampled from up to 10 sites: seven in the wilderness of Madagascar and three in captivity in Madagascar or the United States. We found that, compared to wild lemurs, captive lemurs harbored greater abundances of resistance genes, but not necessarily more diverse resistomes. Abundances of resistance genes were positively correlated with our assessments of anthropogenic disturbance, a pattern that was robust across all ten lemur populations. The composition of lemur resistomes was site-specific and the types of resistance genes reflected antibiotic usage in the country of origin, such as vancomycin use in Madagascar. We found support for multiple routes of ARG enrichment (e.g., via human contact, antibiotic treatment, and environmental acquisition) that differed across lemur populations, but could result in similar degrees of enrichment. Soil resistomes varied across natural habitats in Madagascar and, at sites with greater anthropogenic disturbance, lemurs and soil resistomes covaried. As one of the broadest, single-species investigations of wildlife resistomes to date, we show that the transmission and enrichment of antibiotic resistance genes varies across environments, thereby adding to the mounting evidence that the resistance crisis extends outside of traditional clinical settings.
... Tourism seems to be a vital threat to the Philippine tarsier, a problem shared with other iconic primate species, such as catta lemurs (Lemur catta), which are kept in businesses for income generation in Madagascar (LaFleur, Clarke, Reuter, Schaefer, & terHorst, 2019), and slow lorises (Nycticebus spp.), which are used as photo props in Thailand (Osterberg & Nekaris, 2015). Currently, three tourist establishments in Bohol are legally permitted to display tarsiers: one in Corella, and two in Bilar. ...
Article
Investigating the local people’s perception of the primate species in question, as well as the impressions of and experiences with conservation measures in their neighbourhood, is important in order to devise an appropriate conservation strategy. Here, we provide our findings on the knowledge of the Bilar local community about the Philippine tarsier (Tarsius [Carlito] syrichta) and its population endangerment risk. From October 2016 to November 2017 we conducted interviews with 325 residents from five villages in Bilar, Bohol Island, the Philippines. Tarsiers, though correctly recognized as such by the majority of interviewees, were infrequently sighted in the area, mainly by men, local resource suppliers and villagers in forested areas. Despite a high general knowledge of the species, its ecology and conservation are less well known, with word-of-mouth and personal experience being important sources of information. The species is generally not perceived by locals as endangered, and positive conservation attitudes prevail. Nevertheless, hunting in the area is widespread, and tarsiers are captured either for sale, to be kept as pets or trafficked to tourist facilities or foreigners. The Philippine tarsier, as a charismatic animal, has the potential to be an effective ‘flagship species’ for promoting conservation efforts. To strengthen the species’ conservation, we recommend involving forest resources suppliers in research activities and wildlife tour services, continuing teacher training to ensure that school education emphasizes the ecological and aesthetic values of the Philippine tarsiers, and enhancing the image of this primate, particularly in the digital context, to improve tarsier welfare in captivity.
... With the increasing occurrence of illegal incidents such as meat fraud and adulteration or illegal trade of protected animals (Cawthorn et al., 2013;Tibola et al., 2018;LaFleur et al., 2019), it is fundamentally important in forensic genetics to be able to identify the animal species in an unknown sample. Compared to morphological observation and protein-based method, DNAbased method is regarded as one of the most suitable techniques for species identification due to their tolerance for heat or other environmental influences. ...
Article
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Species identification of unknown biological samples is of fundamental importance for forensic applications, especially in crime detection, poaching, and illegal trade of endangered animals as well as meat fraud. In this study, a novel panel was developed to simultaneously identify 10 different animal species (Gallus domesticus, Anas platyrhynchos domesticus, Ovis aries, Sus scrofa domesticus, Bos taurus, Equus caballus, Columba livia domestica, Rattus norvegicus, Mus musculus, and Canis lupus familiaris) and human beings by amplifying 22 short tandem repeat (STR) loci in a multiplex PCR using a set of five fluorescently labeled dyes. This novel 22-STR panel was validated by optimization of PCR conditions as well as species specificity, sensitivity, reproducibility, precision, DNA mixture, and tissue/organ consistency. The results of developmental validation showed that the 22-STR loci achieved high species specificity among 10 animal species and human beings, and the sensitivity of this panel was 0.09 ng. This 22-STR panel identified different meats in mixed samples, and the minimum detected mixture ratio in the current test was 10% (0.1 ng/1 ng). This sensitive, accurate, and specific 22-STR panel can be used for forensic species identification and the detection of meat fraud and adulteration.
... The ring-tail lemur (Lemur catta) is the best studied lemur species in the world, and is recognizable as a prominent species used to promote lemur conservation (LaFleur et al., 2017). Despite being the most common primate species in captivity, the rapidly dwindling wild populations of L. catta are highly threatened by anthropogenic changes to their landscape, such as habitat loss, agricultural intensification, and mining enterprises in addition to the illegal wildlife pet trade (Andriaholinirina et al., 2014;Estrada et al., 2018;Gould & Sauther, 2016;LaFleur et al., 2019). Researching this species to better understand their behavioural ecology can contribute to current knowledge of the evolution of primate behaviour broadly, in addition to better conservation action to protect this endangered species from extinction in the wild (see LaFleur & Gould, 2020). ...
Thesis
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The study of multimodal communication in primatology has increased only recently. At present, there are no on-going investigations of multimodal communication in ring-tailed lemurs (Lemur catta), despite the body of research on this species. I investigated how different modes of L. catta inter-individual multimodal communication are socially coordinated and integrated by examining frequencies of occurrence within four potential biological and social factors: age, troop affiliation, sex, and dominance rank. Research was conducted over four months at the Duke Lemur Center, Durham, NC, on 14 individuals from three separate troops of captive, free-ranging L. catta. Results demonstrate communicative variation in unimodal, but not multimodal, signals correlating to sex and rank in this species. Dominant females appear to utilise visual signal components more frequently than males, while males rely more on auditory means of communicating, consistent with troop spatial organization. This research provides a baseline for future investigations into primate multimodal communication.
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Background Inter-population variation in host-associated microbiota reflects differences in the hosts’ environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes – an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur ( Lemur catta ; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used source-sink ecological theory to examine covariation between the two types of consortia. Results The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or condition. Variation in microbial composition was inconsistent with either a single, representative gut community for wild conspecifics or a universal ‘signal of captivity’ that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemurs within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities were most distinct between the two continents, and there was significant and context-specific covariation between lemur gut and soil microbiota. Conclusions As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple ‘captive vs. wild’ dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.
Article
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In much of the tropics, the proportion of the land covered by regenerating forest surpasses than in primary forest, thus protecting regenerating forest could offer a valuable conservation opportunity, but only if those lands promote faunal recovery. Chapman et al. documented the recovery of populations of six primate species over up to 45 years in Kibale National Park, Uganda and discovered that in preexisting forest, populations of all species grew, except blue monkeys. Populations (except blue monkeys) also increased by colonizing regenerating forests at previously cleared sites. In many cases, populations in these regenerating areas were of comparable size to those in old-growth forest, and there was little evidence that this population increase corresponded with a decline in neighboring old-growth forests. This research demonstrates the potential for management of regenerating forest to be an effective conservation tool and illustrates the importance of conducting and funding long-term monitoring.
Article
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Primates occur in 90 countries, but four-Brazil, Madagascar, Indonesia, and the Democratic Republic of the Congo (DRC)-harbor 65% of the world's primate species (439) and 60% of these primates are Threatened, Endangered, or Critically Endangered (IUCN Red List of Threatened Species 2017-3). Considering their importance for global primate conservation, we examine the anthropogenic pressures each country is facing that place their primate populations at risk. Habitat loss and fragmentation are main threats to primates in Brazil, Madagascar, and Indonesia. However, in DRC hunting for the commercial bushmeat trade is the primary threat. Encroachment on primate habitats driven by local and global market demands for food and non-food commodities hunting, illegal trade, the proliferation of invasive species, and human and domestic-animal borne infectious diseases cause habitat loss, population declines, and extirpation. Modeling agricultural expansion in the 21st century for the four countries under a worst-case-scenario, showed a primate range contraction of 78% for Brazil, 72% for Indonesia, 62% for Madagascar, and 32% for DRC. These pressures unfold in the context of expanding human populations with low levels of development. Weak governance across these four countries may limit effective primate conservation planning. We examine landscape and local approaches to effective primate conservation policies and assess the distribution of protected areas and primates in each country. Primates in Brazil and Madagascar have 38% of their range inside protected areas, 17% in Indonesia and 14% in DRC, suggesting that the great majority of primate populations remain vulnerable. We list the key challenges faced by the four countries to avert primate extinctions now and in the future. In the short term, effective law enforcement to stop illegal hunting and illegal forest destruction is absolutely key. Long-term success can only be achieved by focusing local and global public awareness, and actively engaging with international organizations, multinational businesses and consumer nations to reduce unsustainable demands on the environment. Finally, the four primate range countries need to ensure that integrated, sustainable land-use planning for economic development includes the maintenance of biodiversity and intact, functional natural ecosystems.
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A widespread opinion is that conservation efforts disproportionately benefit charismatic species. However, this doesn’t mean that they are not threatened, and which species are “charismatic” remains unclear. Here, we identify the 10 most charismatic animals and show that they are at high risk of imminent extinction in the wild. We also find that the public ignores these animals’ predicament and we suggest it could be due to the observed biased perception of their abundance, based more on their profusion in our culture than on their natural populations. We hypothesize that this biased perception impairs conservation efforts because people are unaware that the animals they cherish face imminent extinction and do not perceive their urgent need for conservation. By freely using the image of rare and threatened species in their product marketing, many companies may participate in creating this biased perception, with unintended detrimental effects on conservation efforts, which should be compensated by channeling part of the associated profits to conservation. According to our hypothesis, this biased perception would be likely to last as long as the massive cultural and commercial presence of charismatic species is not accompanied by adequate information campaigns about the imminent threats they face.
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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.
Chapter
Most primate habitats are undergoing intense and rapid changes due to anthropogenic influences resulting in many primate populations being threatened. Habitat loss and fragmentation are already extensive; thus dispersal to unoccupied habitats is an unlikely adaptive response to these changes. Furthermore, most primates have slow life histories and long generation times, and because environmental change is occurring at an unprecedented rate, gene-based adaptations are also unlikely to evolve fast enough to offer successful responses to these changes. However, long primate life histories are linked to well-developed brains, which may allow primates to respond to environmental change through behavioural flexibility. Here we ask: What are the most common challenges of changing environments for primates and what do we know about their behavioural abilities to respond to such changes? To answer this question, we first review the most common types of habitat/landscape alterations, the extent of human-primate interactions, and the impact of climate change. Next, we evaluate how primates respond to these changes via behavioural flexibility, and using different approaches and datasets, we discuss how to investigate if these responses are beneficial with regard to population persistence. Finally, we discuss how comparisons across species, space, and time can be used to draw generalizations about primate responses to environmental change while considering their behavioural flexibility and the data derived from case studies. We demonstrate how understanding behavioural flexibility as a response to environmental change will be crucial to optimize conservation efforts by constructing informed management plans.
Article
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.
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.
Article
The live capture of primates is occurring throughout the tropics and can be a threat to their conservation. Primates are owned as pets for a variety of reasons. Studies of the motivations for primate ownership have been conducted in several countries where they are endemic, but no study has examined this issue in Madagascar. Madagascar is home to the highest number of threatened primate taxa in any one country, and an estimated 28,000 lemurs were kept in illegal captivity from 2010 to mid-2013. We aimed to expand knowledge about the motivations of lemur ownership in Madagascar. Data were collected via a web-based survey (n = 229 respondents) and from the websites and social media pages of 25 hotels. We found that many lemurs (45%) were seen on the premises of a business or in a private home (27%). Many lemurs were perceived to be kept as personal pets (37%) or for money-making or tourism purposes (20%). When lemurs were used for money-making, owners could receive indirect (72% of the time) and direct benefits (28%). Hotels showing photographs of captive lemurs on their websites and social media sites charged USD 25.69 more per night for a standard room than hotels that did not show such photographs. We found little evidence that captive lemurs are kept as a social status symbol, for captive breeding, or as a fallback food. These findings provide evidence that the motivations for the ownership of, usually illegal, captive lemurs is typically linked with money-making or with the desire to have a lemur as a pet. These data can help target new outreach programs.