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Zoogeography, Genetic Variation and Conservation of the Callicebus

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 Part I Fossil History, Zoogeography and Taxonomy of the Pitheciids
Chapter
Zoogeography, genetic variation and conservation

5 of the Callicebus personatus group

Rodrigo C. Printes, Leandro Jerusalinsky, Marcelo C. Sousa, Luis Reginaldo
R. Rodrigues & André Hirsch

Introduction Miocene of Colombia, appears to be the oldest fossil with a

resemblance to modern Callicebus (see Kay et al., Chapter 1),
The genus Callicebus occurs in two disjunct areas in South
although the paucity of samples prohibits a more systematic
America: the tropical forests of the Amazon and Orinoco basins
analysis.
(extending southwards to the Paraguay and Paraná rivers), and
Hershkovitz (1963, 1977, 1988, 1990) believed that Callicebus
the Brazilian Atlantic Forest. These two areas are separated by
originated in the upper Amazon basin, subsequently dispersing
over 500 km of drier vegetation types (Hershkovitz 1988). The
to lowland areas along river systems during the climatic changes
geographical origin of the contemporary forms of Callicebus has
of the Quaternary. According to this author’s centripetal dis-
caused considerable controversy and is still unclear (Kinzey 1982;
persal theory, populations – including those of what is now the
Hershkovitz 1988).
personatus group – became isolated during further river forma-
Twenty-nine species of Callicebus are currently recognized
tion, which disrupted dispersal routes, resulting in patterns of
(van Roosmalen et al. 2002; Wallace et al. 2006), making this one
sympatry and gradual speciation.
of the most diverse of Neotropical primate genera, comparable
By contrast, Kinzey (1982) emphasized the central role of
to Saguinus (32 taxa) and Cebus, with 33 taxa (Rylands et al.
Pleistocene refugia in Callicebus speciation. These refugia were
1996–1997). Kobayashi & Langguth (1999) and van Roosmalen
relict tracts of forest isolated during periods of drier climate
et al. (2002) recognize five species groups – cupreus, donacophi-
(Ab’Saber 1977; Defler 2004). Kinzey (1997) affirmed that
lus, moloch, personatus and torquatus – of which only the perso-
Callicebus fossils found by Lund in 1939, at Lagoa Santa
natus group has an exclusively extra-Amazonian distribution.
(Minas Gerais), represent the western-most extreme of the
The personatus group currently has five recognized species:
distribution of Callicebus melanochir, dispersing from a forest
Callicebus barbarabrownae, Callicebus coimbrai, Callicebus
refuge in central Bahia.
melanochir, Callicebus nigrifrons and Callicebus personatus.
While the debate is ongoing, most authors prefer to view
Although distributed predominantly in the Atlantic Forest,
the formation of the Pleistocene refugia as the fundamental
some members of the personatus group also occur in other eco-
process underlying platyrrhine speciation (Futuyma 1996;
systems, including arboreal Caatinga and riparian forests within
Defler 2004). Wherever Callicebus originated, it persists in
the Cerrado (Hershkovitz 1988). Inhabiting the most developed
both the Atlantic Forest and Amazonia, and the understanding
and populous region of Brazil, all five species have suffered
of the historical factors that permitted its dispersal between the
extensive habitat loss and fragmentation over the past five centur-
two biomes will be important not only for the definition of
ies. Anthropogenic pressures of all kinds, combined with a lack of
zoogeographic processes, but also the systematic assessment of
basic biological information about the species, have resulted in the
the ecological and geographic determinants of present-day
entire personatus group being considered threatened with extinc-
ranges.
tion, with two species, C. barbarabrownae and C. coimbrai, classi-
fied as critically endangered and endangered, respectively
(Machado et al. 2005; Veiga et al., 2008a, 2008b), an extremely Present-day diversity and distribution of the
worrying situation. Callicebus melanochir and C. personatus are
considered vulnerable, although C. nigrifrons is currently classi- Callicebus personatus group
fied only as “near threatened”. The current distribution of the Callicebus personatus species
group extends across the Brazilian states of Bahia, Sergipe, Minas
Zoogeography of the genus Callicebus Gerais, Espírito Santo, Rio de Janeiro and São Paulo, predomin-
As for all Neotropical primates, the origin of Callicebus is hard to antly in the Atlantic Forest biome, but also in neighboring
elucidate, due primarily to the lack of an adequate fossil record. Caatinga and Cerrado ecosystems (van Roosmalen et al. 2002).
Miocallicebus villaviejai Takai et al. 2001, from the middle In central Brazil, the distribution of Callicebus is interrupted by

Evolutionary Biology and Conservation of Titis, Sakis and Uacaris, eds. Liza M. Veiga, Adrian A. Barnett, Stephen F. Ferrari and Marilyn A. Norconk.
Published by Cambridge University Press. © Cambridge University Press 2013.

43
 Zoogeography, genetic variation and conservation
the Cerrado, a drier more open habitat which extends from the
Araguaia–Tocantins and Paraguai–Taquari Novo river systems,
in the west, to the São Francisco and Paraná–Paraíba in the east
(see Hershkovitz 1988). Hershkovitz believed that, in the past,
riparian forest along Cerrado river systems would have provided
suitable habitats for Callicebus, facilitating dispersal between the
Amazonian and Atlantic Forest biomes. He proposed that these
Cerrado-dwelling titis disappeared during the climatic changes of
the Quaternary, which caused the biome to become even drier,
restricting riparian forests to small, isolated valleys. With this, the
Cerrado became an ecological barrier for the titis. Current distri-
butions reflect this, with members of the personatus group being
restricted to the right bank of São Francisco River, in north-
eastern Brazil, and to the right bank of Tietê River, in the
southeast.
Distribution of the personatus group species
Callicebus personatus (Geoffroy, 1812)
This species occurs in the state of Espírito Santo, northwestern
Minas Gerais and northern Rio de Janeiro (van Roosmalen et al.
2002). Oliver and Santos (1991) indicated that the region of the
Itaúnas and Mucuri rivers might be a zone of intergradation
between C. personatus and C. melanochir. Callicebus personatus
occurs on the right bank of the Jequitinhonha River, but it
remains unclear whether this species or another titi occurs to
the northwest of this river (van Roosmalen et al. 2002). The
range of this species extends westwards along the Rio Doce
valley into Minas Gerais as far as the Mantiqueira Mountains.
It is possible that the distribution of C. personatus is more
restricted than previously supposed, as C. nigrifrons and not
C. personatus was recorded at the frontier between Minas Gerais
and Espírito Santo, an area formerly considered to be within the
range of C. personatus.
Callicebus nigrifrons (Spix, 1823)
Callicebus nigrifrons is restricted to the states of São Paulo and
Minas Gerais. It has the most ample distribution of any perso-
natus group species (van Roosmalen et al. 2002), and occurs in
both mature rainforest and disturbed fragments. It is found
north of the Tietê and east of the Paraná and Paranaíba rivers,
and on both margins of the São Francisco. The species also
occurs east of the Mantiqueira and Espinhaço ranges, where it
meets C. personatus (see above).
Callicebus melanochir (Wied-Neuwied, 1820)
Hershkovitz (1990) placed the geographic distribution of
C. melanochir between the Mucuri River, in Espírito Santo
and the Paraguaçu, in Bahia. However, van Roosmalen et al.
(2002) considered the possibility of an overlap zone with
C. personatus in the valleys of the Itaúnas and Mucuri rivers,
in the north of Espírito Santo.
As noted above, the Cerrado proper acts as a barrier to the
distribution of modern-day titi taxa, and C. melanochir
44
probably ranges no further west into Minas Gerais than Mon-
tes Claros (Printes 2007). To the north, the main obstacle to
the dispersal of C. melanochir appears to be the Paraguaçu
River. It is likely that C. melanochir once occurred in the
Pardo–Jequitinhonha interfluvium, but the forests of this
region have now been replaced by cattle pasture and our
surveys found no Callicebus there. Callicebus melanochir does
occur in the Pau Brasil National Park, south of the Jequitin-
honha. More surveys are needed, but it is possible that the
species may reach the Rio Doce, some 300 km further south.
To the south of the Jequitinhonha, C. melanochir is restricted
to remnant coastal forests. To the west, it is replaced by
C. personatus.
Callicebus barbarabrownae (Hershkovitz, 1990)
Until the survey of Printes (2007), this species was known from
only four localities, but C. barbarabrownae has now been
confirmed at no less than 37 sites. The species appears to be
endemic to the state of Bahia, where it inhabits upland areas
between 241 and 908 m above sea level (Printes & Rylands
2008; Printes et al. 2011). Using the minimum polygon convex
approach (IUCN 1994), its total range is believed to cover an
area of some 252,546 km2, although actual occupancy is esti-
mated at 2636 km2 (Figure 5.1).
No titis were recorded in the region west of Araci and
Nova Soure (Figure 5.1), which is dominated by the Cerrado.
However, C. barbarabrownae was recorded in the Caatinga of
the moister uplands northeast of Araci (Mandacaru, Miran-
dela and Serra Branca). The species was also recorded in
Caatinga habitat further north as far as the Salitre River,
170 km from Juazeiro, but titis were not recorded west of
the Chapada Diamantina, which supports Hershkovitz’s
(1988, 1990) conclusion: that topographic relief, or the shifts
in vegetation associated with it, limit the dispersal of titis in
this region.
In eastern Bahia, the Agreste forests of the coastal range
probably supported large populations of C. barbarabrownae in
the past, although this type of vegetation is rare in the present
day. We nevertheless recorded populations in five municipal-
ities (Cícero Dantas, Antas, Sítio do Quinto, Jeremoabo and
Pedro Alexandre).
Callicebus coimbrai (Kobayashi and Langguth, 1999)
Kobayashi and Langguth (1999) originally restricted the distri-
bution of C. coimbrai to the coastal rainforests between the
mouths of the São Francisco River in Sergipe and the Itapicuru
in Bahia. Nevertheless, Printes (2007) recorded the species at
Lamarão do Passé (Figure 5.1), extending its range some 200
km further south. Kobayashi and Langguth (1999) also believed
that C. coimbrai was restricted to primary rainforest, although
more recent surveys have shown that the species also occurs in
fragments of seasonal forest and forests with a Caatinga influ-
ence, along the border between the states of Sergipe and Bahia
(Sousa 2003; Jerusalinsky et al. 2006). However, further west,
 Distributional limits in the Brazilian northeast

50°W 45°W 40°W

o S ã o Fr
Ri an PE
PA Legend:

ci s
MA PI co
Capital Cities
AL
10°S

10°S
PALMAS Brasil State Division
Hydrography - rivers
SE
TO Hydrography - water bodies
ARACAJU
R i o I t a p i cur u Species Records
Callicebus barbarabrownae
C. barbarabrownae
Callicebus coimbrai

cisco
C. coimbrai
guaçu Callicebus melanochir
MT BA ara
Ri o P Callicebus nigrifrons

an
SALVADOR Callicebus personatus

ã o Fr
Geographic Distribution
C. barbarabrownae

Rio S
C. coimbrai
15°S

15°S
C. melanochir
? C. melanochir C. nigrifrons
GO DF C. personatus
? ? qu
itinh
onha
GOIÂNIA Je
io
R Rio Mucuri
C. personatus
anaíba
Pa r R. Doce
Ri o MG R . i o
S . ntôn R. D
A oce Atlantic Ocean
ES
20°S

20°S
Study Area
MS C. nigrifrons VITÓRIA N
Rio
Tie Cartographic Base:
tê í ba d o S u
W E
BDGEOPRIM, 2002;
a ra
oP IBGE, 2003; ESRI, 2001
Ri S
R i o Pa
ra n a
p an e SP RJ 1:10,500,000 Geoprocessing:
ma
André Hirsch
SAO RAULO 0 100 200 400
RIO DE JANEIRO Department of Zoology / ICB
PR km Federal Univesity of Minas Gerais
Belo Horizonte, March 2007

50°W 45°W 40°W

Figure 5.1 Geographic distribution of personatus group of Callicebus.

the species is replaced by C. barbarabrownae in more typical The lower Paraguaçu forms the limit between the geo-
Caatinga ecosystems (Printes et al. 2011). The species distri- graphic ranges of C. coimbrai, restricted to the left or north
bution covers little less than 30,000 km2 (Jerusalinsky 2008), bank, and C. melanochir, found on the right bank. Further west,
and our surveys confirmed its presence in at least 35 forest in the region of Feira de Santana, C. barbarabrownae occurs on
remnants (Sousa 2000, 2003; Jerusalinsky et al. 2006; Printes both banks of the Paraguaçu. This suggests to us that C. barbar-
et al. 2011). The largest of these fragments is a 3000 ha tract in abrownae dispersed prior to the formation of the Paraguaçu
São Francisco do Paraguaçu, Bahia, whereas the smallest is a river system, and that the process was influenced by regional
3 ha fragment in Arauá, Sergipe (Jerusalinsky et al. 2006). phytogeography, rather than physical barriers. There does
not appear to be a physical barrier between the eastern limit
Distributional limits of Callicebus in the of the range of C. barbarabrownae and the western limit of
C. coimbrai, although there may be an association with altitude
Brazilian northeast and related humidity gradients, with the latter species typically
The recent surveys of C. barbarabrownae and C. coimbrai occurring at lower, and relatively more humid altitudes.
have provided a number of insights into the factors limiting We also recorded C. coimbrai in areas of Caatinga with a
the distribution of Callicebus species in northeastern Brazil. strong rainforest influence (e.g. Nossa Senhora da Glória,
For example, C. melanochir replaces C. barbarabrownae in Sergipe). Coimbra-Filho and Câmara (1996) suggested that
the region known as the “Recôncavo Baiano” (south of the anthropogenic disturbance over the past 450 years has favored
Paraguaçu River in the municipality of Igrapiuna). The indi- the expansion of the more xeric Caatinga vegetation into areas
viduals observed in this area presented the unmistakable once covered by Atlantic Forest. If this is true, C. barbara-
C. melanochir color pattern of uniform gray trunk with brownae may now occupy areas that were inhabited by
chestnut-brown tail. C. coimbrai in recent times.

45
 Zoogeography, genetic variation and conservation

Genetic diversity The impact of land-use patterns on Callicebus populations needs

to be analyzed as a global phenomenon with regional character-
Genetic studies of Callicebus have mainly involved cytogenetic
istics. Although strategies for the conservation of biodiversity are
analyses, with a few contributions from molecular biology
usually defined and implemented at national and international
(Schneider et al. 1993; Bonvicino et al. 2003). The results have
levels (e.g. ECO 92 and COP 8), the success of these strategies
revealed a high karyotypic diversity in the genus, with diploid
depends ultimately on the practices of local communities, and the
numbers ranging from 2n ¼ 16 in Callicebus lugens (the lowest
understanding of their exploitation of natural resources (Silvano
number found in any primate) to 2n ¼ 50 in Callicebus
& Begossi 2005).
donacophilus (De Boer 1974; Minezawa & Borda 1984),
The reduction of available habitat for the eastern Brazilian
Callicebus pallescens (Stanyon et al. 2000; Dumas et al. 2005)
titis is ongoing, mainly due to demands for land for cattle
and Callicebus hoffmannsi (Rodrigues et al. 2001). This diver-
ranching and agriculture. These economic activities, together
sity is the result of genomic reorganization involving centric
with urbanization, are driven by the developmental paradigms
fusion and fissions, based primarily on tandem fusions and
of local governments. In Bahia, for example, 115 new munici-
pericentric inversions.
palities were created between 1970 and 2000, while the urban
Before the current study, three species from the personatus
population increased from 41% to 67% of the total (IBGE
group had been karyotyped: C. nigrifrons, 2n ¼ 42 (Nagamachi
2005). Even the most remote localities in the Bahian Caatinga,
et al. 2003), and C. personatus and C. coimbrai, both with 2n ¼
considered to be demographic deserts a century ago (Cunha
44 (Rodrigues et al. 2004, 2006). These karyotypes are com-
1901), are now undergoing development, facilitated by an
pletely homologous in G banding patterns and in the number
extensive network of highways. The progressive expansion of
and position of NOR. The difference in diploid numbers is due
both minor and major urban centres, such as Porto Alegre, São
to a centric fusion/fission rearrangement that transformed two
Paulo, Salvador and Belo Horizonte, has occurred at the cost of
acrocentric pairs of C. personatus and C. coimbrai chromo-
natural habitats. It has also generated secondary impacts on
somes into a metacentric one in C. nigrifrons (Rodrigues et al.
primate populations, with potential dangers ranging from
2004). The C banding revealed a slight reduction in the
roads and powerlines to domestic pets as potential predators
amount of constitutive heterochromatin in the C. coimbrai
(Printes et al. 2010).
karyotype. Comparative genomic mapping (ZOO-FISH) of
The resulting small, isolated populations of titis are exposed
human and C. personatus chromosomes showed that the per-
to synergistic genetic and demographic risks (Lacy 1992),
sonatus group represents a distinct lineage supported by five
although hunting pressure is probably negligible to moderate
chromosomal synapomorphies (Rodrigues 2006).
in most cases, given their small body size (Jerusalinsky 2008).
The role of chromosomal rearrangements in the speciation
Titis are also rarely kept as pets, in comparison with the
process is controversial. Many neighboring pairs of species are
larger-bodied capuchins (Cebus spp.) and the much smaller
known to have different karyotypes, e.g. Callicebus moloch
marmosets (Callithrix spp.) from the same region. It remains
(2n ¼ 48) and Callicebus hoffmannsi (2n ¼ 50); Callicebus
unclear to what extent this reflects the relative abundance of
donacophilus (2n ¼ 50) and Callicebus brunneus (2n ¼ 48);
the different species – marmosets, in particular, are very
C. nigrifrons (2n ¼ 42) and C. personatus (2n ¼ 44). In all these
common in many urban areas – or the difficulty of keeping
cases, divergence is due to a centric fusion/fission rearrange-
titis in captivity. Certainly, these monkeys are as rare in
ment, which could result in unviable or unfertile hybrids
zoos as they are among pet keepers. During our extensive,
because of problems in meiotic division, i.e. the formation of
long-term surveys of Callicebus coimbrai, for example, we
misbalanced gametes. Such rearrangements may represent a
have only observed three individuals being kept as pets
post-zygotic reproductive barrier, which would effectively isol-
(in contrast with dozens of Callithrix jacchus), and all three
ate species (King 1995).
had been found wandering in open areas, dispersing between
The karyotypes of C. melanochir and C. barbarabrownae
fragments (Jerusalinsky et al. 2006; Jerusalinsky 2008).
are unknown. Additional genetic studies are necessary to
Similarly, we observed only two individuals of C. barbarab-
understand the evolutionary relationships of Callicebus
rownae being kept as pets.
species, and to clarify the role of chromosomal rearrangements
In the specific case of C. melanochir, populations in south-
in the speciation process. Molecular studies may also contrib-
ern Bahia had been afforded a degree of protection by the
ute to our understanding of the phylogenetic relationships
traditional cabruca agroforestry system based on the cultivation
between the species of personatus group, and of this group
of cocoa trees in the shade of remnants of native forest, which
with the rest of the genus.
provided habitable cover for the titis. However, following
widespread infestation by the fungal parasite Moniliophthora
Land-use patterns and conservation issues (Crinipellis) perniciosa at the end of the 1980s, cocoa cultiva-
The personatus species group occurs in the Brazilian region tion declined abruptly, and the cabrucas have largely been
with the longest history of European colonization, which has replaced by pastures and eucalyptus plantations, neither of
resulted in widespread deforestation and habitat fragmentation. which are titi-friendly.

46
 Acknowledgments

An additional current problem is the Agrarian Reform
Program, which has stimulated the growth of political organ-
izations such as the Movimento dos Sem Terra (Landless Agri-
cultural Workers’ Movement), which are able to exert
considerable pressure on governments for the occupation of
large rural properties throughout the Atlantic Forest. Some
settlements have resulted in effective and well-integrated pro-
grams of sustainable development, but more often than not,
the primary objective of these groups is the occupation of
forested areas. This is partly because these areas are considered
to have more productive soils, but also because landowners are
more likely to relinquish forested land than that already under
cultivation. Ultimately, government agencies will also often
prioritize the areas because they are considered to be “unpro-
ductive” and as such, less valuable for the assessment of com-
pensation due to the landowner on confiscation.
Despite increasing attempts in recent decades to integrate
conservation efforts with economic development, the protec-
tion of natural populations in conservation units, such as parks
and reserves, still seems to be the most effective approach. In
this light, the five species of personatus group face widely
differing scenarios. Considering only federal- and state-
protected areas, the three least-threatened species of the group
are represented by populations in relatively extensive areas of
forest: C. nigrifrons in seven reserves, totalling more than
100,000 ha, C. personatus at nine localities, with a combined
area of more than 100,000 ha, and C. melanochir in four areas
with more than 50,000 ha of forest.
At the opposite extreme, neither C. barbarabrownae nor
C. coimbrai – the two most endangered taxa of this group – are
known to occur in any kind of official reserve. Jerusalinsky
et al. (2006), for example, estimated that the total remnant
population of C. coimbrai comprises some 500–1000 individ-
uals, occupying a total area of 100–150 km2, pulverized into
numerous unprotected forest fragments, most of which cover
less than 100 ha. Surveys of the 100,000 ha Raso da Catarina
Ecological Station have failed to confirm the presence of
C. barbarabrownae in this potentially important federal reserve
(Printes 2007). These and other findings have led the Brazilian
Federal Environment Institute’s Centre for the Protection of
Brazilian Primates (ICMBIO/CPB) to create an interinstitu-
tional working group for the conservation of C. barbara-
brownae and C. coimbrai, and to coordinate proposals for
the creation of federal reserves aimed at the protection of
these species. These species, together with C. personatus and
C. melanochir (and Cebus xanthosternos and Cebus robustus)
have been included in the portfolio of the International
Committee for the Conservation and Management of Primates
of the Northern Atlantic Forest and Caatinga, established in
2006 with the objective of assisting the Federal Institute in
strategic decision-making for in situ and ex situ conservation
(MMA 2006).
In the specific case of C. coimbrai, privately owned reserves –
known as Reservas Particulares de Patrimônio Natural or
RPPNs – may play an especially important role in the conser-
vation of the species. While they may protect only relatively
small areas of forest, and proportionately small populations
of titis, such areas may nevertheless represent a substantial
contribution to the conservation of the species, especially for
the development of metapopulation management strategies,
in combination with an eventual network of public reserves.
A number of potential sites are currently under study in
Sergipe, and may also contribute to the conservation of other
endangered endemics, such as the yellow-breasted capuchin,
Cebus xanthosternos, and the maned sloth, Bradypus torquatus.
Acknowledgments
We would like to thank Drs. Anthony Rylands, Stephen Ferrari
and Júlio César Bicca-Marques. Roberto Groehs, Luisa
Lokschin and André Alonso assisted in the surveys of
C. barbarabrownae. Fieldwork was supported by Conservation
International, Critical Ecosystem Partnership Fund, Fundação
Biodiversitas, Margot Marsh Biodiversity Foundation, Insti-
tuto de Estudos Sócio-Ambientais do Sul da Bahia, CODE-
VASF, Universidade Federal de Sergipe, and Programa
Macacos Urbanos (UFRGS–INGA). We are also grateful to
André Hirsch for Figure 5.1.

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