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Illegal lemur trade grows in Madagascar

  • January 2017
  • Nature 541(7636):157
DOI:10.1038/541157d
Authors:
Kim Reuter at Franklin Scholars
Kim Reuter
  • Franklin Scholars
Marni LaFleur at University of San Diego
Marni LaFleur
Tara A Clarke at North Carolina State University
Tara A Clarke
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Abstract

Correspondence: We call for urgent action to increase government effectiveness in fighting Madagascar’s illegal trade in live lemurs (see go.nature. com/2i6hvor). More funding is needed to investigate the issue, its extent and the factors behind it. Facilities to rehabilitate confiscated lemurs must be improved, and more international non-governmental organizations should contribute. Exploitation is pushing species such as the ring-tailed lemur (Lemur catta) towards extinction in the wild. Thousands of lemurs are kept openly as illegal pets. Touching and feeding the animals is common to encourage tourists, even in protected areas — despite a law forbidding human contact with lemurs in those areas. Environmental degradation is costing Madagascar up to 10% of its gross domestic product. A sapphire rush last year resulted in 45,000 miners digging in its protected areas. Organized poaching is decimating its sea-turtle populations, and the illegal pet trade is set to wipe out the last 100 wild ploughshare tortoises (Astrochelys yniphora). The country’s weak opposition to the illegal export of rosewood may cause it to face new sanctions under the Convention on International Trade in Endangered Species of Wild Fauna and Flora. It is time for the government to enforce its own laws and put Madagascar’s unique heritage above short-term financial gains.
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Correspondence
Scale up elephant
anti-poaching funds
Many populations of Asian
elephants (Elephas maximus)
have enjoyed 15years of
protection against poachers.
We s u gg e s t t ha t i n cr e a si n g
investment in anti-poaching
measures and law enforcement
in Africa could help to stem
the escalating crisis for African
elephants (Loxodonta africana).
Since 2010, Africa has
received some US$500million
of international donor funding
to increase law enforcement
in protected areas (go.nature.
com/2h76smi). However,
poaching is still rife, particularly
where rangers are sparse. Even
well-resourced parks in southern
Africa are not immune.
Poaching of Asian elephants
was stopped across Cambodia’s
Cardamom Rainforest Landscape
in 2001, and has been kept at
bay at an annual cost of $200
per square kilometre. Assuming
similar factors operate in Africa,
and given that the estimated
range of the African elephant is
3million km2, on-the-ground
action at poaching sites would
need some $600million annually.
Although daunting, this sum
is less than $1,500 a year for each
live African elephant — much
lower than even conservative
estimates of its value to ecosystem
services and ecotourism. The
global community must help to
raise these funds.
Thomas N. E. Gray, Suwanna
Gauntlett Wildlife Alliance,
Phnom Penh, Cambodia.
gray@wildlifealliance.org
Funds to help Eastern
Europe close the gap
The incentive for investigators
in Eastern Europe to apply for
Horizon 2020 funding from the
European Union is undermined
by the grant model defining how
researchers should be paid (go.
nature.com/2hqxgxi). It requires
that research stipends conform
to national basic salaries, which
are much lower in Eastern than
in Western Europe. This weakens
the motivation of researchers in
the eastern EU to put in the extra
effort required to catch up and
gain international standing.
Compared with Western
European centres, systems
for grant writing, funding
management and research
publication in Eastern Europe
are less developed. After years
of underfunding, the scientific
community there lacks the
necessary competitive edge. For
researchers who trained abroad,
the cushion of having research
Save last cloud forests
in western Andes
Wildfires in November 2016
consumed much of the last relic
cloud forests on the western
slopes of the Andes in northern
Peru, a well-known biodiversity
hotspot. Normally protected
against fire by mist throughout
the year, these forests were
suffering from severe drought.
Climate change and local human
intervention seem to have led
to a rapid and massive loss of
biodiversity, affecting hundreds of
species in a short space of time.
According to the International
Union for Conservation of
Nature’s Red List, several globally
threatened animal species, such
as the spectacled bear (Tremarctos
ornatus), live here. The area is a
discrete biogeographic region
(the Amotape–Huancabamba
zone; M.Weigend Bot. Rev.
68, 38–54; 2002) that has an
extraordinary concentration of
micro-endemic plant species,
most of which are restricted to
individual cloud-forest remnants
of just a few hectares (J.Mutke
etal. Front. Genet. 5, 351; 2 014) .
We c a l l o n t h e s c i en t i f i c
community to step up
biodiversity monitoring and to
devise programmes that will
protect these forests in the future.
Jens Mutke, Tim Böhnert,
Maximilian Weigend University
of Bonn, Germany.
jens.mutke@uni-bonn.de
Illegal lemur trade
grows in Madagascar
We call for urgent action to
increase government effectiveness
in fighting Madagascar’s illegal
trade in live lemurs (see go.nature.
com/2i6hvor). More funding
is needed to investigate the
issue, its extent and the factors
behind it. Facilities to rehabilitate
confiscated lemurs must be
improved, and more international
non-governmental organizations
should contribute.
Exploitation is pushing species
such as the ring-tailed lemur
(Lemur catta) towards extinction
in the wild. Thousands of lemurs
are kept openly as illegal pets.
Touching and feeding the animals
is common to encourage tourists,
even in protected areas — despite
a law forbidding human contact
with lemurs in those areas.
Environmental degradation is
costing Madagascar up to 10%
of its gross domestic product. A
sapphire rush last year resulted
in 45,000miners digging in
its protected areas. Organized
poaching is decimating its
sea-turtle populations, and the
illegal pet trade is set to wipe out
the last 100wild ploughshare
tortoises (Astrochelys yniphora).
Step on the natural
gas for German cars
The decision by Germany’s
Federal Council to phase out
petrol and diesel vehicles by 2030
is at odds with the government’s
investment in renewable energy,
which is not enough to produce
the extra power that electric cars
will need. We show how natural
gas could plug the gap.
Replacing internal-combustion
vehicles with electric cars would
reduce Germany’s primary
energy needs by 60%, from
about 570 terawatt-hours
(TWh) to about 230TWh
(detailed calculations available
from the authors). However,
the government’s brake on
renewables, mainly to protect
stability of the electricity grid,
means that only 63TWh will
come online by 2030 (see also
Nature 534, 152; 2016) . Mak ing
up the deficit with electricity
generated by burning natural gas
would create 131million tonnes
of carbon dioxide, which would
still save 30million tonnes on
2014 road-transport emissions.
To d e c a rb o n i z e i t s t r an s p o r t
sector entirely — and to meet the
shortfall under its plan to phase
out nuclear energy by 2030 —
Germany will need to step up
production of renewable energy
and develop smart storage grids.
Dénes Csala, Harry Hoster
Lancaster University, UK.
d.csala@lancaster.ac.uk
and living expenses provided by
their principal investigators is no
longer available when they return
home (Nature 538, 444 ; 2016 ).
As young investigators who
trained as postdocs in the
United States, we are finding it
increasingly hard to close the
research and salary gap with
Western European universities
because of the funding challenges
in Romania. It is essential for the
EU to instigate special funding
arrangements for Eastern
European countries in the current
calls if progress is to be made.
Cristian Berce, Ciprian
Tomuleasa Iuliu Hatieganu
University of Medicine and
Pharmacy, Cluj-Napoca, Romania.
Radu Meza Babes-Bolyai
University, Cluj-Napoca, Romania.
ciprian.tomuleasa@umfcluj.ro
The country’s weak opposition
to the illegal export of rosewood
may cause it to face new
sanctions under the Convention
on International Trade in
Endangered Species of Wild
Fauna and Flora.
It is time for the government
to enforce its own laws and put
Madagascar’s unique heritage
above short-term financial gains.
Kim E. Reuter Conservation
Internatio nal, Nairob i, Kenya.
Marni LaFleur, Tara A.
Clarke Lemur Love, San Diego,
California, USA.
kimeleanorreuter@gmail.com
12 JANUARY 2017 | VOL 541 | NATURE | 157
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... The Malagasy populations dependence on subsistence agriculture, fuelwood cutting (85% of the Malagasy population rely on charcoal for cooking) and the widespread use of slash and burn practices (known as 'tavy') lead to soil erosion, deforestation, overgrazing, desertification, and water pollution (Harper et al. 2007, Nellemann et al. 2014, Máiz-Tomé et al. 2018. Illegal logging and timber trade (e.g. of rosewood, Dalbergia spp.), wildlife trafficking (e.g. trade of the ploughshare tortoises, Astrochelys yniphora, and live capturing of lemurs to sell them as pets) and mining (e. g sapphire, ilmenite and nickel-cobalt mining) play also a significant role in species decline and environmental degradation (Duffy 2005, Schwitzer et al. 2014, Virah-Sawmy et al. 2014, Borgerson et al. 2016, Gore et al. 2016, Reuter et al. 2017, Zhu 2017. ...
Conservation perspectives at Lake Alaotra, Madagascar – ecological state, nature protection and resource use
Thesis
Full-text available
  • Jan 2020
Tropical wetlands maintain a high biodiversity and provide ecological services which are basis for millions of livelihoods. However, freshwater ecosystems are largely neglected in research and environmental policy. Today they are among the most threatened habitat types throughout the world with highest loss rates for natural inland wetlands in the tropics. The high dependency of local communities upon natural resources makes conservation management for wetlands in developing countries to a particular challenge. This study investigated the different perspectives of conservation planning at Lake Alaotra, the largest wetland complex of Madagascar. First, the ecological state of Lake Alaotra was assessed to close knowledge gaps and to provide an adequate basis for ecosystem-based conservation measures. Second, I evaluated the community-led management of a small protected area in order to determine its potentials and weaknesses. Third, the local fishery, as the largest lake resource user group, was investigated to understand the drivers of overfishing. By interlinking the results of the three perspectives of conservation planning – ecology, management and resource user – interrelations and trade-offs between the three dimensions were identified. The current ecological state of Lake Alaotra reveals that the anthropogenic disturbance is favoring the proliferation of invasive plant species and leading to the alteration of the water quality (e. g. hypoxia). Insights into the local management show that the community-based management contributes to the conservation of the natural flora and fauna. However, the small-scale conservation area suffers from isolation and illegal activities, while its management lacks recognition at community level. The fishery sector has grown dramatically although fish catches have fallen sharply. Species composition changes and low reproduction rates are reflecting the fishing pressure. A high population growth and lacking agricultural land force people to enter fishery and increases the human pressure on the lake. Overall this study shows that the conservation of multiple-value ecosystems, such as tropical wetlands in developing countries, require site-specific multidimensional approaches that interlink ecological demands, resource user needs and the local sociocultural setting. This research demonstrates that: ongoing livelihood dynamics linked to the socio-economic conditions have to be considered to create more realistic management policies; strengthening resource users’ assets will help to decrease the human pressure on the already considerably altered ecosystem; capacity building for local management associations and the adoption of local ideas and management concepts is needed to enable the evolvement of an locally legitimated and tailored wetland conservation management.
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... High polymorphism levels of MHC II genes are considered critical to the long-term survival of animal populations (Edwards and Potts 1996;Grogan et al. 2017), although species with low diversity could also be viable (Sommer et al. 2002). Like all lemurs, true lemurs face significant anthropogenic threats, including disease pressures, changing climatic conditions, and habitat loss and fragmentation (Schwitzer et al. 2013;Reuter et al. 2017). Many populations have become isolated (Irwin et al. 2010), and we indicate that an isolated population in our study shows a loss of genetic diversity. ...
Determining Mhc-DRB profiles in wild populations of three congeneric true lemur species by noninvasive methods
Article
Full-text available
  • Oct 2018
The major histocompatibility complex (MHC) is a highly polymorphic and polygenic genomic region that plays a crucial role in immune-related diseases. Given the need for comparative studies on the variability of immunologically important genes among wild populations and species, we investigated the allelic variation of MHC class II DRB among three congeneric true lemur species: the red-fronted lemur (Eulemur rufifrons), red-bellied lemur (Eulemur rubriventer), and black lemur (Eulemur macaco). We noninvasively collected hair and faecal samples from these species across different regions in Madagascar.We assessed DRB exon 2 polymorphism with a newly developed primer set, amplifying nearly all non-synonymous codons of the antigen-binding sites.We defined 26 DRB alleles from 45 individuals (17 alleles from E. rufifrons (N = 18); 5 from E. rubriventer (N = 7); and 4 from E. macaco (N = 20). All detected alleles are novel and show high levels of nucleotide (26.8%) and non-synonymous codon polymorphism (39.4%). In these lemur species, we found neither evidence of a duplication of DRB genes nor a sharing of alleles among sympatric groups or allopatric populations of the same species. The non-sharing of alleles may be the result of a geographical separation over a long time span and/or different pathogen selection pressures. We found dN/dS rates > 1 in the functionally important antigen recognition sites, providing evidence for balancing selection. Especially for small and isolated populations, quantifying and monitoring DRB variation are recommended to establish successful conservation plans that mitigate the possible loss of immunogenetic diversity in lemurs.
View
... High polymorphism levels of MHC II genes are considered critical to the long-term survival of animal populations (Edwards and Potts 1996;Grogan et al. 2017), although species with low diversity could also be viable (Sommer et al. 2002). Like all lemurs, true lemurs face significant anthropogenic threats, including disease pressures, changing climatic conditions, and habitat loss and fragmentation (Schwitzer et al. 2013;Reuter et al. 2017). Many populations have become isolated (Irwin et al. 2010), and we indicate that an isolated population in our study shows a loss of genetic diversity. ...
Determining Mhc-DRB profiles in wild populations of three congeneric true lemur species by noninvasive methods
Article
Full-text available
The major histocompatibility complex (MHC) is a highly polymorphic and polygenic genomic region that plays a crucial role in immune-related diseases. Given the need for comparative studies on the variability of immunologically important genes among wild populations and species, we investigated the allelic variation of MHC class II DRB among three congeneric true lemur species: the red-fronted lemur (Eulemur rufifrons), red-bellied lemur (Eulemur rubriventer), and black lemur (Eulemur macaco). We noninvasively collected hair and faecal samples from these species across different regions in Madagascar. We assessed DRB exon 2 polymorphism with a newly developed primer set, amplifying nearly all non-synonymous codons of the antigen-binding sites. We defined 26 DRB alleles from 45 individuals (17 alleles from E. rufifrons (N = 18); 5 from E. rubriventer (N = 7); and 4 from E. macaco (N = 20). All detected alleles are novel and show high levels of nucleotide (26.8%) and non-synonymous codon polymorphism (39.4%). In these lemur species, we found neither evidence of a duplication of DRB genes nor a sharing of alleles among sympatric groups or allopatric populations of the same species. The non-sharing of alleles may be the result of a geographical separation over a long time span and/or different pathogen selection pressures. We found dN/dS rates > 1 in the functionally important antigen recognition sites, providing evidence for balancing selection. Especially for small and isolated populations, quantifying and monitoring DRB variation are recommended to establish successful conservation plans that mitigate the possible loss of immunogenetic diversity in lemurs. Electronic supplementary material The online version of this article (10.1007/s00251-018-1085-z) contains supplementary material, which is available to authorized users.
View
... As an endangered strepsirrhine endemic to Madagascar, the ringtailed lemur is both a flagship conservation species for one of the world's top biodiversity hot spots and a prime example of a species in peril (Gould & Sauther, 2016;LaFleur et al. 2016). Like all nonhuman primates, ring-tailed lemurs face significant anthropogenic threats (Reuter et al. 2017;Schwitzer et al., 2013) and are increasingly susceptible to environmental change through loss of genetic diversity (Frankham, 2005a(Frankham, , 2005bCharpentier et al., 2008;Spielman et al., 2004). Studies such as this one are key for assessing a species' ability to respond to these threats, including novel pathogens, as well as to adapt to changing climatic conditions. ...
Genetic wealth, population health: Major histocompatibility complex variation in captive and wild ring‐tailed lemurs (Lemur catta)
Article
Full-text available
  • Aug 2017
Across species, diversity at the major histocompatibility complex (MHC) is critical to individual disease resistance and, hence, to population health; however, MHC diversity can be reduced in small, fragmented, or isolated populations. Given the need for comparative studies of functional genetic diversity, we investigated whether MHC diversity differs between populations which are open, that is experiencing gene flow, versus populations which are closed, that is isolated from other populations. Using the endangered ring-tailed lemur (Lemur catta) as a model, we compared two populations under long-term study: a relatively “open,” wild population (n = 180) derived from Bezà Mahafaly Special Reserve, Madagascar (2003–2013) and a “closed,” captive population (n = 121) derived from the Duke Lemur Center (DLC, 1980–2013) and from the Indianapolis and Cincinnati Zoos (2012). For all animals, we assessed MHC-DRB diversity and, across populations, we compared the number of unique MHC-DRB alleles and their distributions. Wild individuals possessed more MHC-DRB alleles than did captive individuals, and overall, the wild population had more unique MHC-DRB alleles that were more evenly distributed than did the captive population. Despite management efforts to maintain or increase genetic diversity in the DLC population, MHC diversity remained static from 1980 to 2010. Since 2010, however, captive-breeding efforts resulted in the MHC diversity of offspring increasing to a level commensurate with that found in wild individuals. Therefore, loss of genetic diversity in lemurs, owing to small founder populations or reduced gene flow, can be mitigated by managed breeding efforts. Quantifying MHC diversity within individuals and between populations is the necessary first step to identifying potential improvements to captive management and conservation plans.
View
... Lemurs in particular are among the most endangered species. Exploitation is pushing the ring-tailed lemur toward extinction in its natural environment, and a large number of lemurs are also kept illegally as pets (Reuter, LaFleur & Clarke, 2017). Increasing our knowledge on lemurs' perceptual skills may help us develop proper enrichment programs for lemurs confined in natural parks. ...
Preliminary Study to Investigate the Delboeuf Illusion in Ring-tailed Lemurs (Lemur catta): Methodological Challenges
Article
Full-text available
  • Aug 2017
Visual illusions are commonly used in animal cognition studies to compare visual perception among vertebrates. To date, researchers have focused their attention mainly on birds and mammals, especially apes and monkeys, but no study has investigated sensitivity to visual illusions in prosimians. Here we investigated whether lemurs (Lemur catta) perceive the Delboeuf illusion, a well-known illusion that occurs when subjects misperceive the relative size of an item because of its surrounding context. In particular, we adopted the spontaneous preference paradigm used in chimpanzees and observed lemurs’ ability to select the larger amount of food. In control trials, we presented two different amounts of food on two identical plates. In test trials, we presented equal food portion sizes on two plates differing in size: If lemurs were sensitive to the illusion, they were expected to select the food portion presented on the smaller plate. In control trials, they exhibited poor performance compared to other mammals previously observed, being able to discriminate between the two quantities only in the presence of a 0.47 ratio. This result prevented us from drawing any conclusion regarding the subjects’ susceptibility to the Delboeuf illusion. In test trials with the illusory pattern, however, the subjects’ choices did not differ from chance. Our data suggest that the present paradigm is not optimal for testing the perception of the Delboeuf illusion in lemurs and highlight the importance of using different methodological approaches to assess the perceptual mechanisms underlying size discrimination among vertebrates.
View
Primate Portrayals: Narratives and Perceptions of Primates in Entertainment
Chapter
  • Jan 2023
Across the globe and across time, primates have been used in live performances and depicted through imagery to entertain audiences and tell stories. Technological advances have led to a proliferation of ways in which we consume media and with that, audiences for primates in entertainment have flourished. Here we review some of the ways primates are used as entertainers and examine representations of primates in contemporary media. We provide an overview of the role of primates in the entertainment industry and discuss issues of animal welfare and conservation. An understanding of the history primates in media and entertainment is critical to regulating these practices and ensuring the health and welfare of both humans and animals.
View
The Past, Present, and Future of the Primate Pet Trade
Chapter
  • Jan 2023
Pet primates are those kept typically for companionship, enjoyment, and status, although their uses as pets may extend beyond these parameters. The trade in pet primates is historically rooted, with many primates playing important roles in human cultures and religions. Thus, it is not surprising that current sociocultural trends reveal an ongoing fascination with primates and their purchase as status pets. Recent reports from various regions are presented in this chapter, demonstrating the need for drastic interventions to avoid further losses. Capture of animals for the pet trade may be intentional or opportunistic and is often exacerbated by internet trade and social media. This situation is complicated by the difficulty of obtaining accurate numbers of primates bought and sold illegally. The health and welfare of primates captured or kept as pets is another area of great concern. Long-term solutions will require attention from governmental, professional, and public actors on local and international levels.
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Illegal Trade of Wild-Captured Lemur catta within Madagascar
Article
Full-text available
  • May 2019
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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https://doi.org/10.1016/j.biocon.2018.03.021
Thesis
  • Jun 2018
Tropical forests are facing an unprecedented number of threats worldwide and many species are in decline. The survival of lemurs, a diverse group of primates in Madagascar, is highly threatened by human disturbances. I examined the responses of these endemic primates to forest logging. Although anthropogenic disturbances have long-lasting effects on forest structure and composition, regenerating forests have considerable conservation potential as lemur habitat and facilitate coexistence of closely-related lemur species. However, disturbances may exert stress on lemurs and influence the presence of nematodes and microbiota composition and can affect the animals’ resistance against diseases. Some lemur species only appear to survive in undisturbed forests, others prefer selectively-logged forests. But very few can live without forests. Proper conservation actions, based on the results of this thesis, can help to ensure the long-term viability of lemurs, keeping the raft called Madagascar, including its unique flora and fauna, afloat.
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