The effects of habitat fragmentation and

degradation on wildlife: the case of the

lion tamarins (Leontopithecus spp.) in the
Brazilian Atlantic Forest

Guillermo Uceda Gómez (5581664)

Writing assignment
Environmental Biology Master Program
Utrecht University
2016-2017
Abstract: The Atlantic Forest of Brazil is the second largest rainforest of south America and
one the World´s biodiversity hotspots. However, it is highly fragmented and deteriorated due
to intense deforestation that started around the time of colonization, and continued during the
industrialization and urban development that followed. It is home to many plant and animal
species among which we find the lion tamarins (Leontopithecus spp.). The lion tamarins are a
genus of “New World Primates” which comprises four species: the golden lion tamarin (L.
rosalia), the golden-headed lion tamarin (L. chrysomelas), the black lion tamarin (L.
chrysopygus) and, the black-faced lion tamarin (L. caissara). The former three species are listed
as Endangered by the IUCN, meanwhile L. caissara is listed as Critically endangered. Thus, all
four species are subject to conservation projects to increase their numbers in the wild and to
mitigate the effects of habitat fragmentation on them. Moreover, a “Population and Habitat
Viability Assessment” (PHVA) has been organized three times, with the aim of proposing new
conservation actions to preserve these species. Thus, the aim of this paper is to review which
actions have been implemented since the last PHVA (2005) and what is still needed to be done
to preserve the four species. I conclude that despite all the efforts, the species are still in risk
and is still necessary to actively work in-situ improving their habitats. Furthermore, it is also of
great importance to keep on conducting basic research to better understand which are the
requirements of all four species. Finally, it is necessary to engage local communities in hands-
on conservation, as well as, applying a multidisciplinary approach that encompasses knowledge
from the social sciences and the scientific community.

Key words: lion tamarins, conservation programmes, PHVA, review.

Table of contents
1. Introduction 3
2. Habitat, ecology and threats to the conservation of the four species of lion tamarins 5
A. Golden lion tamarin.
B. Golden-headed lion tamarin
C. Black lion tamarin.
D. Black-faced lion tamarin
3. Genetic consequences of small population size 10
4. Fundamental and applied research that have been carried out, since the PHVA (2005), with the
purpose of generating information instrumental for outlining management plans to mitigate the
effect of fragmentation on these four species 12
A. Golden lion tamarin.
B. Golden-headed lion tamarin
C. Black lion tamarin.
D. Black-faced lion tamarin
5. Management programs: What has been implemented, and what still needed to be done? 20
6. Discussion and conclusions 23
7. References 24
1. Introduction

Habitat loss, fragmentation and degradation are among the major drivers of biodiversity
loss and species extinction (Schipper et al., 2008), turning available habitat into small isolated
patches. Animal populations living in these fragmented environments can experience various
consequences, such as a decline in gene flow, altered population dynamics, and resource
scarcity (Zeigler, 2011). As a result, populations decrease steadily, leading them into an
extinction vortex, eventually becoming extinct.

A good example of how habitat loss and fragmentation can affect biodiversity is the
Atlantic Forest of Brazil (Mata Atlantica). The Atlantic Forest is the second largest rainforest
of South America. Originally it covered 1.5 million Km2, mostly along the Brazilian west coast
with small areas in Paraguay and Argentina (Ribeiro et al., 2009). It stretches along vast
latitudinal (3º S to 30º S), longitudinal (35º W to 60º W) and altitudinal (0-2900 m.a.s.l.) areas.
Moreover, it covers a wide array of soil and climatic conditions. Thus, it represents an extremely
heterogeneous biome. It encompasses several types of ecosystems such as: evergreen forests,
semi-deciduous forests, deciduous forests, mangroves, swamps, and high-land grasslands
among others. As a consequence, it is home to a large variety of plant and animal species,
having a high rate of endemism, harbouring more than 20,000 plant species, 261 mammal
species, 688 species of birds, 200 species of reptiles and 280 species of amphibians (Silva &
Casteleti, 2003). In total, its flora and fauna represent 1-8 % of the World´s total species (Silva
& Casteleti, 2003).

Despite being one of the World´s biodiversity hotspots, it is highly affected by habitat
fragmentation and degradation as a result of intense deforestation. Due to a massive agricultural
expansion, starting around the time of colonization, and the industrialization and urban
development that followed, the Atlantic forest currently maintains only 11.7 % of its original
size in Brazil (Ribeiro et al., 2009), 24.9% in Paraguay (Huang et al., 2009), and 38.7 % in
Argentina (De Angelo, 2009) .These figures only represent a 12.59% of its total original size.
Nowadays, the Atlantic Forest has been transformed into a human-modified landscape: a
mosaic of old grown forest, secondary forest, grasslands and agroforestry exploitations,
embedded within a matrix of agricultural lands. In this sense, most of the remaining Atlantic
Forest is present in isolated forest fragments which are smaller of 100 ha (Zeigler, 2011). This
transformation process has put a lot of pressure onto many animal and plant species.

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 Endemic to the Atlantic forest is the callitrichine genus of New World Primates,
Leontopithecus. This genus comprises four species: golden lion tamarin (L. rosalia), golden-
headed lion tamarin (L. chrysomelas), black lion tamarin (L. chrysopygus) and black-faced
lion tamarin (L. caissara). During the last half of the 20th century all these four species have
been close to extinction. Deforestation, hunting and trade are the major causes of their decline.

L. rosalia is currently listed as endangered by the International Union for the

Conservation of Nature (IUCN) in 2008. An estimated number of 1.000 mature individuals
exist today in 104.5 Km2 of forest (Zeigler, 2011). L. chrysomelas was also categorized as
endangered by the IUCN in 2008. According to a survey conducted by Pinto & Rylands (1997)
there are between 6,000 and 15,500 individuals in total, ranging in 14,962 Km2, although its
range has been reduced by 30 % since the last survey (Raboy et al., 2010). The black lion
tamarin was downgraded to endangered by the IUCN in 2008. It is calculated that there are
1,000 mature individuals distributed in 11 isolated groups, ten of which are not considered
viable in the long term ( Kierulff, Mendes, & Oliveira, 2008) . At last, L. caissara is listed as
critically endangered (Kierulff, Mendes, & Oliveira, 2008) , since there are only 400 individuals
located in three isolated subpopulations.

All four species are the object of conservation programs. The characteristics of these
management programs depend on the specific threats causing the decline of each species and
on the feasibility, effectiveness and efficiency of the actions implemented. In this regard, there
is a captive population of every species except for the black-faced lion tamarin (due to a lack
of information). However, the ecology of the four species is studied, as well as the behaviour
and the genetics of wild populations. On the other hand, there are only translocation of
individuals for L. rosalia and L. chrysopygus. Moreover, there are habitat restoration
programmes for L. rosalia, L. chrysomelas and, L. chrysopygus. Also, there is a reintroduction
programme outlined for the golden lion tamarin and the black lion tamarin. Finally, besides
generating instrumental information to develop management programmes, there are also
educational programmes focusing on the communities within the species’ distribution ranges.

In 2005, the third “Population and Habitat Viability Assessment” (PHVA) was organized.
The aim of this PHVA was to assess the actual status and threats on the species, implementation
status of the conservation action plans for the four species, and to set new priorities for
conservation strategies and to address new problems. A species group was set up for each of
the species with the aim of identifying topics of relevance for the conservation of each species.
A modelling group was also created to model the evolution of the populations over time.
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Additionally, a GIS group was set to develop maps for each of the species. Likewise, three
topic-based groups were formed to prioritize conservation issues specific to all species. The
topics were the following: 1) Interinstitutional Cooperation and Communication, 2) Regional
landscape planning, socioeconomic aspects and education, 3) Metapopulation Management.

The aim of this essay is: 1) to review which conservation actions have been implemented
to recover the four species and, 2) to review which of the actions that were proposed during the
PHVA still need to be implemented. First of all, I will briefly point out the habitat characteristics
and those ecological aspects that make each of the species vulnerable. Secondly I will shortly
review the threats that made the four species to decline, including the consequences of small
population numbers. I will also highlight which fundamental and applied research have been
conducted to study and quantify the effects of fragmentation on the four species. Furthermore,
I will address the results of the management plans and what actions still need to be implemented
of those that were planned.

2. Habitat, ecology and threats to the conservation of the four species of lion tamarins

A. Golden lion tamarin (L. rosalia)

The IUCN ( 2008) listed L. rosalia as endangered due to its decreasing home range as
well as its declining habitat quality. The habitat of this species consist on seasonal rainforests
along the Atlantic coast of Brazil (Jerusalinksy, Melo, & Talebi, 2011). In these regions the
mean precipitation is 1.500 mm. This species is highly adaptive, being able to live in secondary
or degraded forest. Their capability of adaption to different conditions depends on the
abundance of resources and sleeping sites (Coimbra & Filho, 1977).

L. rosalia lives in family groups of 3 to 11 individuals. The groups are territorial and
defend home ranges that vary from 21 to more than 200 ha (Dietz et al., 1997; Kierulff, 2000).
The golden lion tamarin distribution range is nowadays limited to the Brazilian municipalities
of Araruama, Silva Jardim, Saquarema, Rio Bonito, Cabo Frio, Buzios, Casimiro de Abreu and,
Rio das Ostras (Procópio-de-Oliveira et al., 2008).

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 They are predominantly a monogamous species and reproduction can take place once or
twice per year(Jerusalinksy, Melo, & Talebi, 2011). Groups are normally composed of a
breeding pair and their immature and mature offspring that can be up to three-year-old (Kierulff
et al., 2012).

Golden lion tamarins are a fauni-frugivore species with long slender hands to exploit
microhabitat searching for small prey items (Raboy et al., 2002). Their diet comprises a wide
variety of ripe fruits, nectar and animal prey. Melastomataceae is the botanical family that
provides the most ripe fruit for L.rosalia (Kierulff et al., 2012). When searching for small prey
items they use tree barks, wood crevices, bromeliads and palm leaves (Raboy et al., 2002).

Despite the intensive management plan that started in the 70s L. rosalia is still threatened
(Kierulff et al., 2012). Deforestation and degradation of its habitat continue to be the major
threats the species is facing, next to hunting and illegal trade (Jerusalinksy, Melo, & Talebi,
2011). Kierulff and Procópio-de-Olivera (1996) estimated that only 20% of its original area of
occupancy is still forested. Alongside with these threats, urban development and the duplication
of the highway BR-101 that crosses through the distribution range are also some of the extrinsic
menaces that are contributing to the small numbers of L. rosalia.

Additionally, the species is threated by the introduction of allochthone species (Kierulff

et al., 2012) namely the introduction of two other callitrichid species: Callithrix jacchus
(Common marmoset) and Callithrix penicillata (Black-tufted marmoset). These two species
compete for resources with L. rosalia and could be the vector of diseases (Holst et al., 2006).
Further, a population of the congeneric species L. chrysomelas has been introduced in the
species distribution range, presenting the threat of hybridization between the two species
(Jerusalinksy, Melo, & Talebi, 2011).

Finally, the species is also affected by its small population size which makes it vulnerable
to environmental and demographic stochasticity (Jerusalinksy, Melo, & Talebi, 2011). Dietz et
al. (2000) conducted a survey to study the impact of inbreeding depression in the species. This
authors concluded that the long- term survival of the species has been reduced in those small
populations (<50 individuals) by 30%.

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 B. Golden-headed lion tamarin (L. chrysomelas)

The golden-headed lion tamarin is listed as endangered on the IUCN Red list of
Threatened species (2008). These authors estimated that the entire metapopulation of L.
chrysomelas has gone through a 50 % reduction in number in the past 20 years. The main reason
of its decline has been high rates of forest loss. Moreover, the remaining populations are
severely fragmented which comprises the long-term survival of the species.

The habitat of the golden-headed lion tamarin comprises three types of forest: mature
lowland forest, secondary or regenerating forest and cabruca agroforest (Raboy & Dietz, 2004).
Cabruca agroforest is a human-modified vegetation type which favours the persistence of part
of local biodiversity (Cassano et al., 2009). This type of agroforestry is typical for the region of
Southern Bahia. Cabruca agrosystems consist of cacao trees (Theobroma cacao) which are
grown under the shade of native forest trees. L. chrysomelas presents a great tolerance to
fluctuations in the amount of precipitations (Jerusalinksy, Melo, & Talebi, 2011). Hence, it
occurs in regions next to the coast which have a mean precipitation of 2000 mm. On the other
hand, the species in its western distribution range limit occurs in regions which have a well-
defined dry season, with a mean precipitation of less than 1000 mm.

As well as L. rosalia, golden-headed lion tamarins live in family groups which on average
have seven or eight individuals ( Oliveira et al , 2011). These researchers estimated that the
species defend territories that vary from 22 to 200 ha (based from various study areas). In a
review written by Baker et al (2002) it was stated that in these groups there is only one
reproductive female. Reproduction normally takes place only once a year, although, sometimes
twice. The diet of Golden-headed lion tamarin consists on ripe fruits, flowers, nectars, insects,
small vertebrates, and gums (Kierulff et al., 2002).

L. chrysomelas has been reported to occur in the following Brazilian municipalities: Una,
Ilhéus, Camacã, Jussari, São José, Buerarema, Itabuna, Aurelino Leal, Arataca, Pau Brasil,
Canavieiras, Barro Preto, Itororó, Santa Luzia, Entre Rios, Itapetinga, Santa Cruz do Vitoria,
Itaju da Colonia, Nova Canaã Ibicuí, Gongoji, Floresta Azul, Mascote, Potiraguá and, Ibicaraí
(Jerusalinksy, Melo, & Talebi, 2011).

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 The populations of golden-headed lion tamarins are vulnerable to direct and indirect
threats (Zeigler, De Vleeschouwer, & Raboy, 2013). The direct threats are related to the habitat
loss due to deforestation. At the current rate of deforestation (0.65 % per year; Zeigler et al.,
2010) the species is in risk of extinction, especially in the western part of the range. In the
eastern part of the range, the conversion of the cabruca agroforest into other types of crops will
also negatively affect the species (Zeigler, De Vleeschouwer, & Raboy, 2013). This conversion
is due to the fall in the price of the cocoa, originated from the fungal epidemic that affects the
plantations (Jerusalinksy, Melo, & Talebi., 2011). Furthermore, in the western part of its range
the remaining forest is being converted into cattle pasture (Zeigler, De Vleeschouwer, & Raboy,
2013). Additionally, the commercial and urban development that is occurring in certain areas
of the species range are contributing to its decline.

The indirect threats are related to the small size of the existing populations. Small
population size makes the L. chrysomelas vulnerable to environmental and demographical
stochasticity. Finally, and based on its status in the wild, the golden-headed lion tamarin is
likely to be affected by inbreeding depression. This phenomenon is especially predominant in
the western part of the species range, where deforestation is more intense (Raboy et al., 2010).

C. Black lion tamarin (L. chrysopygus)

L. chrysopygus is listed as endangered (IUCN, 2008) because it only occurs in an area of

490 Km2 and the remaining populations are extremely isolated and their habitat is still suffering
a decline in its quality. They inhabit old grown forest between 470 metres above sea level
(Morro do Diablo) and 930 metres above sea level (Pilar do Sul) in the Brazilian state of Sao
Paulo (Valladares-Padua, 1997). As well as the other Leontopithecus species it also lives in
secondary and degraded forest. Moreover, it is the only species of lion tamarin whose habitat
is not restricted to a coastal rainforest (Rylands, 1993). Accordingly, its home range gets 500
Km inland into the state of Sao Paulo. This region present seasonal precipitation having a
distinct dry season.

The black lion tamarin lives in group of 3 to 7 individuals (Valladares-Padua, 1993). In

these groups there is also one reproductive female that becomes oestrous once or twice per year.
According to Jerusalinksy, Melo, & Talebi (2011), their home ranges always exceed 100 ha
(113-119 ha). In addition, L. chrysopygus presents a larger home range in comparison with
other lion tamarins (Keuroghlian & Passos, 2001), although their daily range is more or less the
same.

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 As the other species within the genus L. chrysopygus feeds on fruits, nectar, seeds, small
prey items and gum. Moreover, a study conducted by Keuroghlian & Passos (2001), indicated
that the prey foraging of L. chrysopygus is quite variable compared to that of other species in
the genus. L. chrysopygus uses a wide variety of microhabitats and forest types (Passos and
Keuroghlian, 1999), and their foraging habits appear to be adjusted to seasonal cycles of prey
availability.

The species is suffering from a high level of isolation and from a small population size
(Jerusalinksy, Melo, & Talebi., 2011). In the species distribution range there is a high level of
farming activity which threatens the continuity of L. chrysopygus habitat. Moreover, the area is
characterized by intensive logging causing high rates of deforestation. On the other hand, the
species is also threatened by high levels of inbreeding which deteriorates the species genetic
quality (Dietz et al., 2000). This is caused by the reduction of gene flow between the highly
fragmented subpopulations.

D. Black-faced lion tamarin (L. caissara)

The black-faced lion tamarin is categorized as critically endangered (IUCN, 2008) due to
its small population size. There are around 400 individuals in the wild which are located in three
subpopulations (Amaral,Nascimento & Schmidlin, 2011). One of these subpopulations is
located on the island of Superagüi, while the other two are on the mainland, in the Brazilian
states of Sao Paulo and Paraná. These subpopulations were once one continuous population.
However, a study conducted by Vivekananda (2001) reported that the populations were split
after the construction of the Varadouro canal. Its geographical range is less than 300 Km2
(Amaral et al., 2011) and it represents the southernmost of all callitrichids. This distribution is
the smallest of all tamarin species being concentrated at low altitudes (Amaral Nascimento &
Schmidlin, 2011).

L. caissara inhabits areas of mature forest, lowlands and slopes at low altitudes
(Nascimento & Schmidlin, 2011). However, the species also thrives in secondary forest and
human-modified areas ( Nascimento & Schmidlin, 2011). L. caissara lives in groups which can
have up to 11 individuals. The average group size is six individuals (Ludwig, 2011), although
Nascimento et al. (2011) gave a more conservative estimation (4.5 individuals). The home
ranges are different between insular and mainland groups (Jerusalinksy, Melo, & Talebi, 2011).
The home range of the insular groups was estimated to be 70 ha, meanwhile, that of the
mainland ones was 300 ha.

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 The black-faced lion tamarin is an omnivorous species (Nascimento and Schmidlin,
2011). Like the other lion tamarin species, it eats fruits, insects, small frogs, nectar, fungi and,
flowers. Nevertheless, its diet is dependent on the habitat type in which L. caissara lives
(Nascimento & Schmidlin, 2011). Moreover, the diet presents seasonal variation according to
the abundance of each food resource (Ludwig, 2011).

The main threats to the long-term survival of the species are the small population size and
its restricted home range (Rylands et al., 2002). Moreover, the genetic isolation suffered by the
population of Superagüi island eliminates gene flow between the three subpopulations (Martins
et al., 2012). Additionally, the species is threatened by the loss of habitat especially in the
mainland range of the species (Vivekenanda, 1994). Activities such as agriculture, hunting and
the extraction of certain commodities (palm hearts), severely contribute to the destruction of
their habitat. Moreover, other human disturbances, for instance, tourism and real estate
speculation are also contributing to the decline of the species (Jerusalinksy, Melo, & Talebi,
2011).

3. Genetic consequences of a small population size

In non-fragmented populations, genetic variation is maintained or increased by mutation

and dispersal, whereas genetic drift and selection decrease it (Willi, Buskirk and Hoffman,
2006). Thus, the adaptive potential of a population depends on which of these processes
predominates. Genetic drift is the process by which certain alleles within the genetic pool of
the species are lost (Frankham, Ballou, & Briscoe, 2010). It is caused by chance effect as parents
pass their genes to their offspring. On the other hand, natural selection makes that the frequency
of deleterious mutations remains low. Thus, this balance between deleterious mutations and
selection will determine which alleles become fixed in the population. Conversely, dispersal or
migration increases the genetic diversity of a population as well as reduces the genetic
differences among populations (Frankham, Ballou, & Briscoe, 2010). Mills & Allendorf
(1996), suggested that one migrant per generation is enough to sustain the genetic variation of
the population. However, these authors also address that a maximum of ten migrants per
generations would be a desirable number for certain wild populations.

Populations that have suffered a restriction in their size or that have been isolated for
many generations, face two genetic threats (Keller & Waller, 2002). As a result of the random
fixation and/or loss of certain alleles by genetic drift, the levels of genetic variation decrease.
Concurrently, deleterious mutations tend to accumulate because selection is weaker in smaller

10
populations (Lynch, Conery, & Burger, 2012). Eventually, this could lead to a phenomenon
termed as mutational meltdown which implies the loss of evolutionary potential of the
population, due to high frequencies of deleterious mutations. The mutational meltdown is the
outcome of a synergy between three factors: population decline, genetic drift and mutation
accumulation (genetic load). Both processes tend to be gradual, therefore they do not
compromise the short-term survival of the population (Keller & Waller, 2002).

Another outcome of a restricted population size is inbreeding. It occurs when two

genetically related (by descent) individuals breed to produce offspring (Frankham, Ballou, &
Briscoe, 2010). Inbreeding reduces the reproduction and survival of offspring. This
phenomenon is referred as inbreeding depression (Keller & Waller, 2002). These authors also
stated that inbreeding depression increases homozygosity in the population. In this regard,
deleterious recessive alleles will be expressed, affecting the fitness of the populations. As a
result, the populations will be more prone to extinction.

As many other fragmented and endangered animal populations the four species of lion
tamarins are suffering genetic detrimental effects from their small populations size. In this
regard, Grativol et al. (2003) conducted an analysis of the genetic diversity of the remnant
populations of L. rosalia. The author concluded that the golden lion tamarin has lost a 67% of
its mitochondrial DNA diversity. Also Dietz et al. (2000) proved inbreeding to occur in this
species. Likewise, it has been demonstrated that L. chrysomelas is suffering from inbreeding
depression (Jerusalinsky, Melo, & Talebi, 2011) Moreover, it was observed that the two
existing subpopulations are becoming genetically different due to their isolation. The black-
faced lion tamarin is not suffering apparent deleterious consequences from its small population
size, although, low levels of genetic diversity have been observed (Martins et al., 2012). Finally,
L. chrysopygus is also being affected by inbreeding depression in an analogous manner as L.
rosalia. The loss of genetic diversity suffered by the species is slowing down population growth
rate (Jerusalinksy, Melo, & Talebi, 2011).

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4. Fundamental and applied research that have been carried out, since the PHVA (2005),
with the purpose of generating information instrumental for outlining management
plans to mitigate the effect of fragmentation on these four species.

The aim of the PHVA was to assess the status of all four species within the genus
Leontopithecus. Accordingly, documenting the changes that occurred as a result of habitat
fragmentation was essential for understanding a species´ status and allowing conservation
actions that ensure the long-term survival of a species. In this regard, it was necessary to specify
which were the main factors that were negatively affecting lion tamarin populations. Thereby,
it was agreed upon that a multidisciplinary approach was needed to tackle down the main threats
that all four species were facing. Furthermore, it was necessary to collect information on the
landscape, habitat, genetics, health, population demographics, ecology, community
interactions, and general biology of all four species, as well as improving the cooperation
among the parties involved.

Since the aim of this section was to review all the fundamental and applied research
produced, since 2005, some selection criteria on the information to be included were
established. The Selection criteria were the ones proposed by the specialist groups during the
PHVA in 2005. Thus, studies conducted after 2005 on the biology, ecology, behaviour, genetics
and demographics of these species, were included in this review. Regarding the golden lion
tamarin and the golden-headed lion tamarin there was a vast body of knowledge on the matter.
Meanwhile, little has been done, since 2005, for the other two species.

A. Golden lion tamarins (L. rosalia)

The specialist group for L. rosalia set the goal of 25, 000 ha of protected forest to harbour
2,000 tamarins by the year 2025, thus 10,000-12,000 additional hectares are needed (Holst et
al., 2005). These regions are not defined and need to be identified in order to focus actions of
protection and management. In this regard, Burity et al. (2007) conducted a new survey in
“Tuquara Municipal Park” where the species was thought to be extinct in the last survey (1993).
These authors reported the presence of L. rosalia. Therefore, and according to these results, the
area should be properly managed and well protected. In despite of these results, the authors
could not assure how many individuals were living in the area. This is a crucial point to assess
the long-term survival of the species in the region.

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 Another important aspect that the golden lion tamarin specialist group addressed was the
lack of a comprehensive metapopulation management plan (Holst et al., 2005). The researchers
addressed that the lack of a clear management plan could affect the genetics of the species, the
vulnerability to disease, and the risk of predation suffered by the subpopulations. Monteiro et
al. (2007) found that infection by parasitic intestinal helminths can limit the population size of
their host. Golden lion tamarin populations that are highly fragmented are force to travel
through longer distances on the ground being more prone to infection by these parasitic
helminths. Another aspect that Monteiro et al. (2007) found, was that infection by parasitic
helminths was correlated with the age and sex of the individuals. Therefore, these host-parasite
dynamics are of crucial importance to define proper management of L. rosalia subpopulations.

In addition, a study conducted by Hankerson & Dietz (2014) showed that predation has
an influence on the home range size. Moreover, the differences in the home range size that these
authors found between golden lion tamarin groups of Poço das Antas Biological Reserve (Rio
de Janeiro State, Brazil) were explained by: 1) group size; 2) male mate-searching opportunities
and/or group defence; 3) the group´s future reproductive potential; and 4) population density.

In their study, group size may only affect ranging in the largest groups. In this sense, very
large groups of golden lion tamarins (8+ individuals) had larger home ranges. Furthermore,
those groups that contained one or more adult natal males had significantly greater home ranges.
Home ranges were also found to be significantly greater in those groups in which there were
several potential breeding males. Hankerson & Dietz (2014) also found that groups with several
breeding females had bigger home ranges. As a result, these groups also had higher reproductive
potential. They hypothesize that groups with higher reproductive potential increase their home
range in order to cover future resource needs. Finally, they also showed that predation rate
affected home range size. Those groups that subject to intense predation suffered a decrease in
their home range due their lower population density.

Behaviour is also of great importance when trying to mitigate the effects of forest
fragmentation in wild animals. Thus, Sabatini & Ruiz-Miranda (2010) conducted a study on the
long distance communication among golden lion tamarins in União Biological Reserve. In their
study, they demonstrated that golden lion tamarins prefer to emit long calls from higher
branches. However, the golden lion tamarins they studied the União Biological Reserve used
all strata when not vocalizing long calls. This behaviour improves sound transmission, sound
perception and visual contact between individuals of different groups. Sabatini & Ruiz-Miranda
(2010) also demonstrated that golden lion tamarins prefer height between 1 m above ground up
13
to 1 m below the canopy of the forest. This understanding on the calling behaviour of species,
will help us to understand which are the habitat requirements of the species, and therefore, to
mitigate the effects of forest fragmentation.

B. Golden-headed lion tamarins

Guy et al. (2016) conducted a study to evaluate suitable areas for golden-headed lion
tamarins and Wied´s marmoset (Callithrix kuhlii), two species that normally live in sympatry.
These authors constructed “Ecological Niche Models” (ENMS) to identify regions of high
quality habitat for these two species. The models were used to: 1) identify areas suitable for
both species; 2) identify the overlapping areas which are suitable for the two species and; 3)
determine the amount of suitable areas within protected areas. The study was focused on the
southern Bahia region in the Brazilian Atlantic Forest. The EMS use both environmental data
and species occurrence data to create probability surface maps that depict the likelihood of
occurrence of a certain species in a given area. These maps take into account the suitable
conditions for the species as well as the probability of finding the species in the area. Guy et al.
(2016) concluded that only 36 % of the study area was suitable for L. chrysomelas. This
percentage amounts for a total of 10,659 Km2. Moreover, they found that 33% of the studied
area can harbour suitable conditions for both species. In addition, their results showed that only
6% of the study areas identified as suitable areas were currently within a protected area. This
study shows the great importance of enlarging the body of protected areas in order to preserve
the species in the long term.

In this respect, Zeigler (2011) conducted landscape analyses to determine the minimum
area requirements for a self-sustainable golden-headed lion tamarin population. Zeigler (2011)
stated that at least 60 individuals are needed for a population to have a 98% probability of
persisting over 100 years, if no catastrophes were considered. However, taking into account the
occurrence of catastrophes like fire or disease or the interaction of both, populations of 90, 170
and 250 individuals are needed. Based on these figures, the minimum patch size would be 700
ha (no catastrophes considered and high population density) or 4717 ha (catastrophes
considered and low population density). Nevertheless, these group sizes are not yet good to
maintain 98 % of genetic heterozygosity among golden-headed lion tamarin populations. Thus,
the author proposes that populations sizes would have to be: 780 (no catastrophes), 810
(disease), 920 (fire) and 960 individuals (interaction between fire and disease). Considering
these values, the minimum habitat requirements would be 7,800 ha and 18,113 ha, respectively

14
for the no catastrophes and high population density scenario and for the most extreme scenario
with low population density.

Furthermore, Zeigler et al. (2013) conducted another study to assess the risk of extirpation
of small metapopulations of L. chrysomelas in Bahia state, Brazil. They concluded that given
the current rate of deforestation all metapopulations are at risk of extinction particularly in the
western portion of their distribution range.

Oliveira et al. (2010) studied which tree species were of key value for the golden-headed
lion tamarins, both as food and sleeping sites in southern Bahia, Brazil. They concluded that
most of the species that L. chrysomelas uses belong to the families Sapotaceae and Myrtaceae.
Cabruca forest was also found to be a keystone habitat as well. Not only for feeding but also
for sleeping. Additionally, they found that single trees within the Cabruca agroforest resulted
to be of great importance for L. chrysomelas as sleeping sites. Oliveira et al. (2010) suggested
that to preserve the species in the long term, it is necessary to plant tree species belonging to
these two families which are extremely valuable for golden-headed tamarins. In this regard (
see Oliveira et al. (2011) as well), they also suggest that trees species belonging to these two
families should be retained in the Cabruca agroforest due to the fact that they least common in
this environment. Secondly, they also suggest that the number of trees in the Cabruca agroforest
should be augmented for the golden-headed lion tamarins to use them, both as food and sleeping
dens.

Additionally, Catenacci et al. (2016) conducted a study to determine the diet composition
and feeding behaviour of L. chrysomelas in degraded areas. Their study area was in southern
Bahia, Brazil. They studied the diet composition and feeding behaviour of two golden-headed
lion tamarin species throughout a period of 12 months. 81 out of 114 plant species were first
reported to be used by the species, thus indicating a greater dietary diversity than previously
known. Furthermore, these results indicate that the species is able of exploiting the resources
present in degraded areas. Moreover, individual trees of the family Melostomataceae were fund
to be used the most. Regarding the species´ time budget, Catenacci et al. (2016) found that the
species spends between 21 and 30% of its time in relation to feeding activity. Searching for
prey items accounted for the major part of time spent in foraging behaviours. During this
activity bromeliads were the preferred substrate. Fruit acquisition was the second most frequent
activity, followed by nectar drinking, exudate feeding and soil eating. These results, highlight
the importance of maintaining a forest mosaic that encompasses large patches of advance forest.

15
 As in the case of L. rosalia studying the behaviour of the species is of great importance
to truly understand how the species interacts with its environment. In this respect, Pessoa et al.
(2005) conducted a study to investigate whether or not L. chrysomelas is able of colour vision.
The authors highlight the importance of understanding if the species is able of colour
perception, to better understand its habitat requirements. They tested this via a behavioural
paradigm of discrimination learning, using stimuli of wide light spectral compositions. The
experiment comprised 3 males and 3 females. The results indicated that the males and one
female showed random responses to stimuli mimicking the conditions under which L.
chrysomelas forages in the wild. However, the remaining two females presented discrimination
ascertaining colour vision in the species. Colour vision might be useful when discriminating
between ripe over not ripe fruits or edible young leaves. On the other hand, these authors
suggest that more experiments need to be conducted on the topic to ensure this condition in the
species.

Galbusera & Gillemot (2008) conducted a study on the genetics of golden-headed

tamarins. Due to the fact that a captive breeding has been set up, these authors conducted an
experiment with polymorphic microsatellite markers which are useful when analysing
relatedness among individuals. They constructed the microsatellite primers making a screening
of a library of short fragments of genomic DNA which previously existed. In their study, the
polymorphic markers resulted to be useful for studying the relatedness between founders of the
captive populations. Moreover, the markers were useful to calculate the genetic variability
among individuals of the captive population.

Another important aspect that has been studied about L. chrysomelas, is its role as seed
disperser. Thus, Catenacci et al. (2009) conducted a study to further investigate this. They
collected feces of two groups of golden-headed lion tamarins ranging in deteriorated areas of
the Una Biological Reserve, Bahia, Brazil. The followed these groups from February 2006 to
January 2007. The obtained 524 samples containing seeds from 24 plant species which
belonged to 13 plant families. These authors also conducted a germination experiment to test
whether or not, the passage of the seed through the animal´s digestive tract improved the
germination of the seeds. Catenacci et al. (2009) concluded that the passage of the seed through
the animal´s digestive tract did not affect seed germination nor germination delay (only for
Aechmea spp.). However, golden-headed lion tamarin´ movement pattern contributed to the
dispersal of some fruit plant and epiphyte species. Thus, the movement of the individuals
observed in these two groups promoted the dispersal of seed towards areas of secondary

16
vegetation. The sites of faecal deposit were similar to the sites where the parent plants were
found. Nevertheless, pioneer species, such as M. mirabilis and M. hypoleuca were found in all
vegetation types. On the other hand, climax plant species, such as trees from the Myrtaceae
family were found in advanced forest. These three pattern found by Catenacci et al. (2009) are
very important for the survival of the dispersed plant species and, the distribution of new
seedlings.

In this regard, Cardoso et al. (2011) identified the fruit species eaten by L. chrysomelas
and related them to seed dispersal. In their study, Cardoso et al. (2011) monitored to golden-
headed lion tamarin groups between September 2006 and August 2007. They conducted their
study a Una Biological Reserve, Bahia, Brazil. These authors found that golden-headed lion
tamarin´s diet comprised fruit from 71 species and that most of the seeds dispersed were far
from the parental trees (> 20m). They also stated that the defecation pattern found in their study
could help to diminish competition between seedlings and could help the establishment of them.
Moreover, they found that the dispersion of the seeds took place within the plant´s habitat.

The studies by Cardoso et al. (2011) and Catenacci et al. (2009) highlight the importance
of L. chrysomelas as seed disperser. Thus, they play a keystone role in the maintenance of the
endangered Atlantic Forest in the region of southern Bahia. Moreover, small frugivores, such
as golden-headed lion tamarins are of great importance in the maintenance of the plant diversity
and composition. This seed dispersal observed in these two studies might be useful in
generating conservation strategies for L. chrysomelas. In this sense, if the plant species observed
to be dispersed in these two studies are included in reforestation and/or corridor programs, this
will enhance the likelihood of movement between forest patches. As a result of the increased
movement between patches, degraded areas would be regenerated by the animals themselves
via seed dispersal.

C. Black lion tamarins (L. chrysopygus)

Due to the fact that, the species occurs in really fragmented and isolated areas Carvalho
et al. (2014) carried out a study that would improve the success of the reintroductions and
translocations. These two practises normally suppose a stress for the animals that are being
handled. Consequently, the animals become immune compromised being more prone to
infection by opportunistic pathogens. Thus, Carvalho et al. (2014) studied ten free-ranging and
ten captive black lion tamarins. They collected nasal, oral, and rectal swaps and then cultured
to investigate the bacterial and fungal microbiota assemblage present in these three corporal

17
regions. In general, the most frequent organisms were Staphylococcus spp., Bacillus spp.,
Candida spp., and Aspergillus spp.

Moreover, Carvalho et al. (2014) concluded that nasal, oral, and rectal swaps of both
study groups (captive VS free ranging) were similar in the relative proportions of the major
bacterial and fungal strains and had similar compositions with respect to the most common
genera. However, organisms that are known to be pathogenic such as Aeromonas,
Pseudomonas, or Klebsiella were either only found in captive animals or were more frequent
in those individuals. The study conducted by these authors, highlight the importance or
minimizing the stress suffered by endangered species during translocations and reintroductions.
In this way, disease´s outbreaks will be avoided, aspect that is of crucial importance when
dealing with endangered species.

In order to properly preserve the species, it is of great relevance a thorough knowledge of

it. Thus, Garbino, Rezende, & Valladares-Padua (2016) conducted a basic research study on
the pelage colour of the species. Historically, there has been a lot of controversy about the
variation in colour of L. chrysopygus´ pelage. Hence, these authors examined museum
specimens and wild animals to investigate the nature of this variance. Garbino, Rezende, &
Valladares-Padua (2016) concluded that there is not a geographical cline that explains the
variation in the pelage´s hue, however, the variation is due to individual and ontogenetically
variation. Garbino and his research team also concluded that the pelage of L. chrysopygus
becomes darker over the time, and after several moults. Moreover, this study confirmed the
specific status of the black lion tamarin.

D. Black-faced lion tamarin (L. caissara)

Martins et al. (2012) conducted a genetic analysis of two different black-faced lion
tamarin populations. The study groups were located in the island of Superagüi and in Airiri
region, both in the southwest of Brazil. These authors analysed the genotype of 52 individuals
belonging from both subpopulations. They used 9 polymorphic markers to determine if these
two subpopulation were suffering from a bottleneck and to what extent both populations were
genetically different. Martins et al. (2012) concluded that both population experienced a sharp
population size reduction and genetic bottleneck. Despite of the genetic bottleneck, the authors
stated that these two subpopulations do not present any detrimental effect.

Martins et al. (2012) concluded that the mean number of alleles per locus (indicator of
the genetic diversity) was 2,56-2,67, figures which are comparable to those in another species

18
within the genus. Therefore, the authors stated that the genetic diversity of the species was
already low before the bottleneck and is not a consequence of anthropogenic destruction of its
habitat. Moreover, and contrary to the expectations, these two populations are not inbred.
Hence, these results are quite promising since population fitness and growth rate are not being
affected, meaning that the risk of extinction is attenuated.

With regard to gene flow both populations only presented a 13% of molecular variance
(Martins et al., 2012). Notwithstanding the presence of a barrier between the two populations,
it seems that there was already a genetic divergence between them two before the opening of
the Varadouro channel. Additionally, these authors concluded that there is a 6% within group
genetic divergence.

With the aim of enlarging the body of knowledge about the species distribution and
habitat requirements, Nascimento & Schmidlin (2011) conducted a study on the habitat
selection and frequency of use by the species. In this regard, they compared two insular groups
with two mainland groups. In their study, the authors concluded that inland groups preferred
swamps and inundated areas, as well as, secondary forest. On the other hand, island animals
preferred lowland forest and arboreal restinga (forest on a sandy substratum). Nascimento &
Schmidlin (2011) also discovered that the species avoids mountainous forest and that is why
the species is restricted to coastal areas. These authors also calculated the carrying capacity, K,
of the studied areas (region of Airiri and south of Superagüi island). Accordingly, the
estimations of K showed that the population can be increased up to 1500 individuals by means
of reintroductions. This study will set light to the habitat selection which could later be taken
into when planning conservation actions.

Nascimento et al. (2011) also carried out another study to better understand the different
habitat requirement from the two subpopulations in which the species still exists. They studied
two black-faced lion tamarin groups in São Paulo state and compared the results with data from
island groups. The authors analysed geospatial data using three range indicators: minimum
convex polygon (MCP), Kernel and the dissolve monthly polygon technique (DMP). They
concluded that the home ranges of the mainland groups were 345, 297, and 282 ha, respectively
for the three estimators used. Nascimento et al. (2011) also concluded that there was spatial
overlap between the mainland groups, although their home ranges did not overlap in time,
revealing the dynamic use of the habitat exhibited by the species.

19
 Despite the fact that, mainland home ranges are larger island groups displayed longer day
ranges, moving over greater distances (Alexandre T Amaral Nascimento et al., 2011). These
authors stated that a plausible explanation to these ranging patterns is that the resources are
more spread and scarce on Superagüi island than in the mainland. Moreover, L. caissara
individuals in the island subpopulation used more daily routes as opposed to the mainland
subpopulation. This also suggests that the resources in the mainland are more clustered. In
addition, Nascimento et al. (2011) showed that mainland groups use more core areas within
their range, rarely engaging in border patrolling and territorial defence. On the other hand, the
island groups presented the opposite pattern. They display more territorial behaviour which is
associated to their home range configuration and daily covered distance.

One of the main problems that the species is suffering is the isolation and the restricted
gene flow due to high levels of fragmentation of their habitat (Nascimento & Schmidlin, 2011).
Thus, Nascimento, Nali, & Da Fonseca (2014) conducted a study on the dispersal patterns of
the species, group formation and kinship in the species. These authors demonstrated that both
sexes disperse. Furthermore, they found that dispersal, especially in the case of males, seems to
be related to the existence of breeding possibilities in an existing group. In their study, the age
of the disperser varied between 8 months and 4 years old. Female migration might be also an
incentive for males to disperse and stablish new breeding groups. However, when this happened
all emigrants stablished their home ranges nearby their former groups (Nascimento, Nali, & Da
Fonseca, 2014). Remainning in a family group is adaptive due to familiarity with travel routes,
sleeping sites, food resources and potential predators.

5. Management programs: What has been implemented, and what still needed to be
done?

With respect to L. rosalia the first conservation actions were taken at the of 1960s with
field studies on the reproduction of the species (Coimbra-Filho, 1976). At the beginning of the
1970s the captive breeding program was set up, together with a studbook of the captive
individuals (Jerusalinksy, Melo, & Talebi, 2011). These two actions were the kick off for the
Golden Lion Tamarin Conservation Programme in 1983. Thus, in 1992 the first PHVA was
organized and following its recommendations the Associaçao Mico-Leão-Dourado (AMLD)
was created to coordinate all the efforts to preserve the species. Based in the basin of the river
São João ( in Poço das Antas biological reserve) the AMLD supports field studies,
reintroduction and translocation actions and educational programmes (Jerusalinksy, Melo, &

20
Talebi, 2011). Furthermore, AMLD puts forward the creation and implementation of protected
areas both in public and private properties.

The in-situ management of the species consist of a active management of the species
habitat (Jerusalinksy, Melo, & Talebi, 2011). Currently, the main focus is to augment the
number of protected areas, as well as establishing ecological corridors to improve the ecological
connectivity of the remaining forest patches. Finally, the conservation efforts are trying to
establish new subpopulations by means of reintroductions. With regard to the ex-situ
management the main goal has been always the proper management of the captive population
(c. 490 individuals) (Jerusalinksy, Melo, & Talebi, 2011). About a third of the individuals that
are currently living in the wild are descendants of animals reintroduced from captivity, and thus
originating from the ex-situ breeding programme.

Thanks to the efforts of the international community, and the intensive management the
species was downgraded from Critically Endangered to Endangered (IUCN, 2008). To improve
its conservation status further, actions such reforestation, across its distribution range, are still
ongoing. Moreover, the establishment of ecological corridors is still ongoing since its start in
1996 ( Kierulff & Procopio de Olivera, 1996) in Poço das Antas biological reserve. Finally, the
programme has also set up an environment friendly educational programme, in order to engage
local communities in its conservation (Matsuo et al., 2008).

As in the case of L.rosalia, the conservation programme of L. chrysomelas has followed

the recommendations of the three PHVA organized so far. With respect to the in-situ
conservation actions the focus has been the creation of protected areas in those regions in which
the species occurs (Jerusalinksy, Melo, & Talebi, 2011). Additionally, another important action
has been the protection of forest patches adjacent to those conservational units. In relationship
to the Cabruca agroforest which serves as habitat for the species (Oliveira, 2010), the
programme has stressed the importance of creating a certficate for those cocoa plantations
which are ecofriendly (Jerusalinksy, Melo, & Talebi, 2011). The ex-situ conservation
programme counts with a good number of founder individuals, and a healthy stable captive
population. Currently, reintroductions are not recommended for this species, so the captive
population serves as a genetic reservoire (Jerusalinksy, Melo, & Talebi, 2011).

The black lion tamarin conservation programme is mainly focused on: the creation of
protected aread within the species distribution range, reintroduction and translocation of
individuals, creation of ecological corridors to increase the gene flow of the species, and the

21
implementation of good agricultural practices together with educational programmes
(Jerusalinksy, Melo, & Talebi, 2011). The in-situ conservation actions are being directed by the
NGO IPÊ (by its acronym in Brazilian; Institute of Ecological Research), with the main goal to
improve the genetic quality of the wild populations. This goal is being achieved via the
translocation and reintroduction of individuals into the wild (Jerusalinksy, Melo, & Talebi,
2011). Moreover, a special effort is being put on educational programmes focusing on the
communities within the species’ distribution ranges. In addition, the programme is trying to
increase the amount of forest as well as improve the ecological conectivity of the remaining
forest patches (Valladares-Padua et al., 2002).

With respect to the ex-situ conservation programme there is a captive breeding

programme (Jerusalinksy, Melo, & Talebi, 2011), which in the past obtained really good results.
However, the captive population is suffering from health problems.

The black-faced lion tamarin was first described by Lorini & Persson (1994) thus the first
conservation actions aimed to gather information about the biology (Jerusalinksy, Melo, &
Talebi, 2011). In 1995, the IPÊ describes for the first time the feeding ecology of the species,
as well as, its behavioural repertoire. In 1999, the ecology and its habitat used was first
described from a group ranging in the island of Superagüi. Between 2000 and 2002, the IPÊ
monitored another two groups of L. caissara enlarging the body of knowledge on the species.
Also during those years, a new population estimate was made, accounting for a total of 183
(1,66 individuals/Km2) individuals in the island subpopulation (Jerusalinksy, Melo, & Talebi,
2011). These data were extrapolated to the mainland subpolations, therefore being able of
knowing the total population size (c. 400 individuals (Nascimento et al., 2011) In the following
years, the research was focused on caracterizing the habitat of the species in both parts of its
distribution range. Therefore, the behavioural patterns in both parts of its range were described
(Jerusalinksy, Melo, & Talebi, 2011).

The in-situ actions to preserve L. caissara involved the creation of a National Park that
enclosed the island of Superagüi and an adjacent one, in total 21,400 ha (Jerusalinksy, Melo, &
Talebi, 2011). The National part was afterwards enlarged, including part of the mainland
distribution range and encompassing c. 34,000 ha. With respect to the ex-situ conservation there
is no captive breeding programme, however, translocations of individuals might take place from
the island of Superagüi to the mainland (Jerusalinksy, Melo, & Talebi, 2011).

22
6. Discussion and conclusions
The four lion tamarin species are still endangered due to the continuous loss and
fragmentation of the Atlantic Forest of Brazil. However, their conservation status has improved
since the implementation of the conservation programs in the 1980s. Yet, it is still necessary to
actively work in-situ improving their habitats. This is the case, for example, of the golden lion
tamarin which almost went extinct in the 1980s and in 2003 the IUCN downgraded it to
endangered. Thus, the aim of this paper was to review which actions have been implemented
since the last PHVA (2005) and what is still needed to be done in the future to preserve the four
species.

During the PHVA the status of all four species was assessed. The different research
groups documented the changes that the four-species suffered because of habitat fragmentation
and degradation. In this regard, the researchers specified which were the main factors that were
negatively affecting the lion tamarin populations. Consequently, conservation actions were
proposed to ensure the long-term survival of the four species within the genus Leontopithecus.
Moreover, it was proposed that a multidisciplinary approach was needed to tackle down the
threats that the lion tamarins were facing. Hence, it was agreed upon to gather information on
the landscape, habitat, genetics, health, population demographics, ecology, community
interactions and general biology of all four species of lion tamarins.

Despite of what was agreed upon during the last PHVA there is still a great lack of
information on some of the research areas proposed (see Table 1). In this regard, more
information is needed on the landscape in which the four species still thrive. The major cause
of the deforestation has been the conversion to agriculture. This process would leave the lion
tamarin landscape lacking a continuous forest cover and will increase the vulnerability of the
populations to extinction (Zeigler et al., 2013).

Traditionally, studies on the consequences of habitat degradation on animal communities

have focused on reporting the biological richness of mature forests and how species richness is
affected by isolation, fragmentation, and edge effects (Chapman, Lawes, & Eeely, 2006).
Accordingly, the focus has been on the habitat but not in the matrix. The main goal of this
studies have been the creation of biological reserves to preserve the species living in those areas
(Chape et al., 2005). This has been also the case for the lion tamarins with the creation of the
Poço das Antas biological reserve in which the golden lion tamarin still thrives.

23
 However, these protected areas might be isolated, are relatively small and/or are poorly
managed to meet long-term conservation goals. Additionally, it has been reported that lion
tamarins sometimes occur outside these protected areas (i.e. Golden-headed lion tamarins in
Southern Bahia; Raboy & Dietz, (2004)). These occurrences are normally in agroforestry
systems as the shaded-cacao Cabruca. The agroforestry systems are suboptimal habitats for the
species although, they can mitigate the fragmentation and loss of natural habitat (Cassano et al.,
2009). This highlights the importance of preserving this management systems by means of
putting forward laws that encourage farmers to produce the cacao in such a way. Yet, these
systems have been only studied in the case of the golden-headed lion tamarin, thus it is
necessary to study them for the rest of the species. Farmers benefit from this agroforest and
natural vegetation by harvesting livelihoods from the forest (Vandermeer, 2003). On the other
hand, biodiversity is enhanced because of the more heterogeneous landscape composed of
patches of natural habitat and crops (Estrada, Raboy, & Oliveira, 2012). Thus, conservation in
the future, should combine the protection of more land and the preservation of these
management systems.

Table 1. Addressed research areas four each of the species since the last PHVA (2005). The
information of this table is based on the reviewed papers of the present work

Research areas L. rosalia L. chrysomelas L. chrysopygus L. caissara

Landscape X
Habitat X X X
Genetics X X
Health X
Pop. demographics X
Ecology X
Com. interactions X X
Biology X X X X

Additionally, more work is needed regarding the genetics of the four species. Since the
last PHVA only two studies have been conducted in two the four species (golden-headed lion
tamarin and black-faced lion tamarin; see Table 1). Because all lion tamarin species have
suffered a sharp reduction in their numbers, this might affect their ability to adapt to a changing
environment. Barriers to gene flow result in genetic structuring, as the divergence between
populations tends to broaden out. On the one hand, genetic studies are useful to assess the

24
current ability of wild populations to evolve and how diverse the different subpopulations have
got. On the other hand, they are good tool to design reintroduction and ex-situ breeding
programs. Furthermore, another aspect that might have been affected by a deteriorated genetic
diversity is the health of the lion tamarin species. A reduction in the genetic pool of the species
may make them more prone to infection, by opportunistic parasites, and to health problems.
This has been demonstrated in L. rosalia individuals infected by T. cuzi (Monteiro et al. 2006).
L. rosalia individuals presented cardiac abnormalities. Thus, conducting more genetic and
health studies is of crucial importance for the long-term preservation of the lion tamarin species.

Although many censuses have been conducted since the implementation of the
conservation programs none have been carried out since the last PHVA (see Table 1). Knowing
how many individuals still thrive in the wild is important to properly implement conservation
measures. An example of this, is the study conducted by Burity et al. (2007). They reported the
presence of L. rosalia in Tuquara National Park, however they could not ensure how many
individuals occurred in this area. Moreover, conducting more censuses will serve as a valuable
tool to assess the success of the conservation programs for the four species. Hence, in the future
in would recommendable to conduct regular censuses that will help to adjust the needs for each
of the species.

A thorough knowledge of the ecology of the four specie is also needed. Since 2005, this
aspect has been addressed in one of the four lion tamarins species (L. chrysomelas) (see Table
1). A series of studies broaden up the knowledge regarding the diet, key tree resources and the
role of L. chrysomelas as seed disperser. Thus, in the future in recommendable to conduct
similar studies regarding the other three species. Understanding which resources are keystone
for each of the species, as well as, knowing how do they interact with their environment will
help to the long-term survival of the lion tamarins.

Despite of the good results that the management programs are having, certain aspects can
be improved. In this regard, it is of great importance that the conservation actions consider the
findings of the basic research. Thus, it is recommendable that the programs should not only aim
to enlarge the amount of protected land, but also they should encourage farmers to implement
eco-friendly practices. Moreover, when trying to re-establish the ecological connectivity of the
forest patches, reforestation programs should consider the role as seed dispensers of these
species. Hence, reforestation programs should plant those trees that are key resources for the
lion tamarin species. In such a way, a positive feedback is created that would allow to preserve
both lion tamarins and the Atlantic Forest.
25
 In addition, a captive population should be created for L. caissara. Although
reintroductions might not be considered, the captive population can serve as a genetic reservoir
for the future. Thus, it is also recommendable the creation of a studbook. The creation of the
captive population should be thoroughly thought to minimize the damage to the wild
populations. Moreover, it is recommendable to conduct studies on the behaviour of the lion
tamarins species in captivity to improve their welfare.

In summary, some improvements have been achieved during the last few years as a
consequence of the works carried out by the management programs, but a continuous
intervention is still required. In addition, it is necessary to engage local communities in hands-
on conservation. In this regard, governmental policies that encourage local communities to live
in a more sustainable way should be put forward. Finally, it is of great importance that the
problems the four species are facing should be tackled through a multidisciplinary approach
engaging people from the social sciences and the scientific community. With respect to that, it
is necessary that all the parties involved actively cooperate to preserve the Atlantic Forest of
Brazil, and therefore the lion tamarins which are of unique ecological value.

26
7. References

Baker A. J., Bales K. M., & Dietz J. M. 2002. Mating system and group dynamics in lion
tamar- ins. In: Kleiman D. G., Rylands A. B., editors. Lion tamarins: biology and
conservation. Washington, D.C.: Smithsonian Institution Press. p 188–212.

Cardoso, N. A., Le Pendu, Y., Lapenta, M. J., & Raboy, B. E. 2011. Frugivory patterns
and seed dispersal by golden-headed lion tamarins (Leontopithecus chrysomelas) in
Una Biological Reserve, Bahia, Brazil. Mammalia, 75(4), 327–337.

Carvalho, V. M., Vanstreels, R. E. T., Paula, C. D., Kolesnikovas, C. K. M., Ramos, M.

C. C., Coutinho, S. D., & Cato-Dias, J. L. 2014. Nasal, oral and rectal microbiota of
Black lion tamarins (Leontopithecus chrysopygus). Brazilian Journal of
Microbiology, 45(4), 1531–1539.

Cassano, C. R., Schroth, G., Faria, D., Delabie, J. H. C., & Bede, L. 2009. Landscape and
farm scale management to enhance biodiversity conservation in the cocoa producing
region of southern Bahia, Brazil. Biodiversity and Conservation, 18(3), 577–603.

Catenacci, L. S., De Vleeschouwer, K. M., Nogueira-Filho, S. L. G., Bahian, S., & Forest,
A. 2009. Seed Dispersal by Golden-headed Lion Tamarins Leontopithecus
chrysomelas in Bahian. Biotropica, 41(6), 1–7.

Catenacci, L. S., Pessoa, M. S., Nogueira-Filho, S. L. G., & De Vleeschouwer, K. M.

2016. Diet and Feeding Behavior of Leontopithecus chrysomelas (Callitrichidae) in
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