Book Title: Phylogeny, Molecular Population Genetics, Evolutionary Biology and

Conservation of the Neotropical Primates. Edited by M. Ruiz-García and J. M.

Shostell (2016). Nova Science Publisher Inc., New York, USA. Book ID: -5975-
ISBN: Hardcover 978-1-63485-165-7; E-book 978-1-63485-204-3. Pp. 3-38.

Chapter 1

AN INTRODUCTION TO NEOTROPICAL PRIMATES

Joseph M. Shostell1 and Manuel Ruiz-Garcia2

1
Math, Science, and Technology Department,
University of Minnesota Crookston, Crookston, MN, US
2
Laboratorio de Genética de Poblaciones Molecular-Biologia Evolutiva),
Departamento de Biología, Facultad de Ciencias,
Pontificia Universidad Javeriana, Bogotá DC., Colombia

ABSTRACT
The Neotropics contains the greatest abundance and diversity of primate species of
any bio-region in the world. They make up an impressive and varied assemblage of species,
from the small pigmy marmoset weighing one hundred grams, to the woolly spider
monkeys (muriquis) tipping the scale at 10-14 kg. Some species in the group, such as the
bearded capuchin, show signs of high intelligence evidenced by their use of primitive tools
to open nuts and fruit, and many of these species are flagships whose very presence is
crucial for the dispersal of seeds and maintenance of primary forests.
Unfortunately, a large percentage of Neotropical primate species is threatened or
endangered due to various anthropogenic activities including deforestation, illegal hunting
and wildlife trade, mining, and road construction. Moreover, there is a general paucity of
data pertaining to this group because their habitats can be difficult to access and the sheer
expansiveness of the Neotropical area. Here, we present new research findings from thirty-
eight of the world’s leading Neotropical primate scientists in order to bridge this
informational gap. Specifically we provide up to date biological, molecular, conservation,
and phylogenic information on many of these poorly understood, yet amazing creatures. It
is our intention that this new information will be used as a resource by the novice and
professional alike in order to improve society’s understanding of Neotropical primates and
to help protect them long into the future.

Keywords: primates, Neotropics, phylogeny, population genetics, evolutionary biology and

conservation
2 Joseph M. Shostell and Manuel Ruiz-Garcia

GENERAL INTRODUCTION TO NEOTROPICAL PRIMATES

He looked down at the large seed and then reached for the stone next to the anvil. It
was a large stone, one he had selected for the larger seed. Using both hands he raised it
high up and then quickly slammed it down on the seed. The capuchin repeated the behavior
until the Attalea seed cracked opened...

This book discusses the group of primates referred to as Platyrrhini (flat nosed), also known
as Neotropical primates or new world monkeys. Besides having relatively large brains and
being quite clever, they have complex social systems, good grasping ability and many possess
prehensile tails that support their expert climbing ability. Some, as noted above, are known for
their use of tools. Their diversity in form and color is impressive and ranges for example from
a small brownish-gold pigmy marmoset of 100 grams to a woolly spider monkey (Brachyteles
arachnoides) in excess of 14 kg.
The Neotropics is the most taxonomic rich terrestrial system in the world and covers an
expansive area including Mexico, the Caribbean, Central America, and South America. Within
this area we find roughly 34% of Earth’s primate diversity and some areas of the Neotropics
such as the Western Amazon have up to 40% (Mittermeier and Richardson 2013) of its
mammalian biomass (save flying mammals) consisting of primates alone (Janson and Emmons
1990). Primate diversity, including richness and evenness, varies geographically with
precipitation, latitude, forest cover, and anthropogenic factors (Peres and Janson 1999, Redford
1992). They are mostly arboreal and, given their frugivorous diets, they are key dispersal agents
for the plant communities in which they live (Chapman 1989). Levey et al. (1994) suggested
that approximately 80% of Neotropical plants rely on primates and other frugivorous animals.
As a consequence of this diet and mobility, their presence affects forest regeneration and helps
forests to maintain a rich community structure (Nunez-Iturri and Howe 2007). Thus, primates
are inexplicably linked to forest ecosystem health and the ability of the forest to maintain
important ecosystem services such as carbon sequestration. At a time when atmospheric carbon
dioxide emissions are ever increasing and there is a concomitant rise in global temperatures,
the preservation of tropical rain forests is paramount. Similar to the canary in the coal mine, the
presence of primates indicates good ecosystem health. They are an important part of the food
chain as well as evidenced by them being targeted by many carnivores.
Moreover, primates have also been used as valued flagships for educational issues
regarding the Neotropics. The general public seems to respond more to primates than to a
general call for conserving tropical rain forests, perhaps because monkeys have many similar
features as to our own and are closely related to us genetically compared to non-primate taxa.
Similarities in physiology also make non-human primates ideal models for better understanding
human health and designing vaccinations for various tropical diseases such as malaria. Of
course this benefit to biomedical research is also a threat to non-human primate survival and
will be discussed in more detail later along with hunting, and live capture.
 An Introduction to Neotropical Primates 3

STATUS OF NEOTROPICAL PRIMATES

Neotropical primates are threatened by many factors, the main categories being habitat
loss/degradation, hunting, and live capture. Recent evidence presented by Kim et al. (2015)
claims that there is a rise in world deforestation rates, a contradiction to the United Nations
Food and Agriculture Organization’s most recent report. The losses of tropical rain forests,
where the world has its greatest terrestrial biodiversity and where Neotropical primates live, is
staggering with Brazil alone losing about 2.25 million hectares per year (Kim et al. 2015).
Both large-scale commercial logging and small-scale slash and burn techniques convert
healthy primary forests into agricultural and ranch areas (Mittermeier et al. 1989). Besides
denuding an area of trees and plummeting diversity in that area, a once continuous forest
becomes fragmented isolating species and disrupting their dispersal routes. Building of roads,
expanding of cities, development of mineral mines, construction of hydroelectric dams, are all
examples of anthropogenic activities that degrade primate habitat.
Hunting poses another major threat to primates. Primates are hunted for food, as
agricultural pests, or in some cases just for sport. More often, hunters prefer to target larger
species (>2 kg) (Bodmer et al. 1997) and also use the carcasses of primates as bait to lure in
and catch jaguars and other predators. Primates are also threatened by live capture. They are
kept alive to support biomedical research, such as for the development of new vaccines against
malaria and other tropical diseases. Constant demand also comes from zoos and the pet
industry. Legal and illegal trafficking occurs to support these demands.
Primates are subjected to a number of smaller threats which individually may seem to be
inconsequential, but collectively, are dangerous to their constitutions. For instance, disturbance
by domestic animals and introduction of invasive species can be detrimental. In the Caribbean
for example, the presence of invasive species is thought to have played a significant role in loss
of primates. Finally, there are also biological limitations of primates and natural environmental
variability. For example, reproduction rates tend to be low in larger species, thus making it
difficult for species to adapt to rapid environmental change. Interestingly, environmental
changes are hypothesized to be the cause of extinctions of platyrrhines that were in Patagonia
(Kay 2015). These threats, individually or synergistically, are real and have worsened the status
of many Neotropical primates as evidenced by 52% of all Neotropical primate species officially
recognized as threatened, endangered, or critically endangered on the IUCN Red List
(Mittermeier and Richardson 2013). The latter part of this book (Chap 13-19) discusses
conservation strategies to help protect Neotropical primates.

ORGANIZATION OF BOOK
Although there is some overlap, the topics of this book are divided into two general
sections. The first one includes chapters two through 13 and focuses on phylogeny, molecular
population genetics, and evolutionary biology. The second section includes chapters 14 through
19 addressing topics of conservation. Inclusive of both sections there are several different types
of studies. Some for example take a panoramic approach and cover topics linking together most
or all of the Platyrrhini. These include a comparison of extinct and extant communities (Chap
4 Joseph M. Shostell and Manuel Ruiz-Garcia

2), a description of sex chromosome systems (Chap 8), and estimations of temporal splits
supported be mitogenomic analyses (Chap 10). Other studies focus on an individual species
across one or multiple countries (Chap 3, 5, 15, and 16) or on multiple species within one or
more genera (Chap 4, 6, 7, 8, 11, 12, 13, and 14) or even on all taxa within a family (Chap 9).
Finally, the highest scale-level of study discusses all Neotropical primates within a significantly
large geographical area such as a preserve (Chap 18) or country (Chap 19). All 23 primates
distributed in Bolivia are mentioned in Chapter 19.

INTRODUCTION OF NEOTROPICAL PRIMATE FAMILIES

The systematics of Neotropical primates is complex and controversial among
primatologists and consequently there are continuous revisions of classifications in some
taxonomic groups. Certainly, the phenotypic similarity among howler monkey species
(Alouatta genus) or the high variability within species of capuchins, for instance can make
systematics very challenging. We have also seen a steady increase in the number of species
with the use of the phylogenic species concept (rather than the biological species concept) and
with the discovery of new taxa in museums and the wild (Groves 2001, Mittermeier 1982,
Rylands et al. 2012). Based on the work of Mittermeier and Richardson (2013) we currently
recognize five Neotropical primate families (Aotidae, Atelidae, Callitrichidae, Cebidae, and
Pitheciidae), 20 genera, and 204 species/subspecies (Mittermeier and Richardson 2013).
Therefore, this introduction acknowledges these taxa and the morphological criteria used to
validate them. However, molecular data are more consistent with the existence of only three
families (Atelidae, Cebidae and Pitheciidae; see chapter 10 of this volume and Schneider and
Sampaio 2015).
With the collaborative help of many primatologists, native peoples, and universities, this
book covers approximately 60% of Platyrrhini taxa and discusses each of the families and many
of their genera in detail. We hope the newly gathered data presented here, including
microsatellite and mitochondrial DNA data, will help resolve some of the taxonomic issues
regarding Neotropical primates. The application of molecular techniques has greatly enhanced
our knowledge of primate systematics and evolution over the last two decades. Today, different
than thirty years ago, we can rely on taking small, non-invasive tissue samples from specimens,
and more rapidly and less ambiguously compare multiple taxa. Also, the availability of high
throughput next generation sequencing has made it easier to process samples, obtain results,
and consequently, increase the number of genetic studies focusing on Neotropical primates
(Lynch Alfaro, 2015). The next section gives an overview of each of the five Neotropical
primate families.

Callitrichidae
The Callitrichidae (Chapters 3, 8, 18, and 19) is one of five Platyrrhine families and
contains 7 genera, 43 species and 62 taxa. Four of the genera (Callithrix, Cebuella, Callibella,
and Mico) represent the marmosets (Figure 1) and the remaining three genera (Saguinus,
Leontopithecus, and Callimico) represent the tamarins (Figure 2).
 An Introduction to Neotropical Primates 5

Figure 1. Marmosets photographed by M. R-G: A) Cebuella pygmaea sampled near Nuevo Rocafuerte
at the Napo River in the Ecuadorian Amazon in 2013. B) Cebuella pygmaea in the Quistococha Zoo in
Iquitos (Peru) in 2010. C) Mico chrysoleuca sampled at the Aripuana River (Brazil) in 2012. D) A Mico
argentata that lightly nibbled the neck of M. R-G near the Tapajos River (Brazil) in 2005. E) Mico
melanura in Chuchini near the Ibare River (Bolivia) in 2003.

Figure 2. Tamarins photographed by M. R-M: A) An indigenous girl with her pet Saguinus mystax in
Contamaná near the Ucayali River in the middle of the Peruvian Amazon in 2010., B) Saguinus
fuscicollis weddelli in Santa Cruz de la Sierra (Bolivia) in 2010. C) Saguinus tripartitus sampled near
6 Joseph M. Shostell and Manuel Ruiz-Garcia

the Napo River in Ecuador in 2013. D) A couple of Saguinus fuscicollis lagonotus at the Belem market
in Iquitos in 2002.

Nevertheless, the genus Callibella seems to not be supported as a full genus by molecular
analysis (Schneider et al., 2012). Marmosets and tamarins are much smaller than other
Platyrrhines, ranging from approximately 110 to 700 g, even smaller than the squirrel monkey
(Cebidae family). Different from other Platyrrhines, they have claws instead of nails at the ends
of all their digits save the distal phalanx of the big toe in each foot. The claws are useful for
accessing sap, a staple of their diet. Another distinct difference is the number of molars.
Callitrichidae have two rather than three molars on each side of the mandibular bones and in
the maxillae. Similar to other primates they have longer hind limbs than forelimbs, and unlike
many other primates that have non-prehensile tails. The overall distribution range of
Callitrichidae extends from Costa Rica, through Bolivia, and into Southern Brazil, but the
distributions of marmosets and tamarins rarely overlap. Callitrichidae primates are principally
arboreal, diurnal, and omnivorous, subsisting on sap, small animals (frogs, spiders, and lizards),
flowers, and fruit. Due to their light weight they can utilize the top layers of the forest canopy
staying clear of large predators. Socially this family is complex. They have a flexible mating
system exhibiting monogamy, polygyny and polyandry and they engage in cooperative
breeding (Rylands 1996). Most species in this family have twins and gestation is roughly 140-
145 days. Their small size, quickness, and presence in the upper canopy make them challenging
to study. A total of 14 species are either critically endangered, endangered, or vulnerable. Their
threats, are common to those of other Neotropical primates and include deforestation, general
habitat degradation, and live collection for biomedical research. In Chapter 3, Ruiz-Garcia et
al., discusses the endemic Colombian Saguinus leucopus (Günther, 1877) and provides
population genetics findings from blood and hair sampled from 47 individuals. This particular
taxon has the smallest distribution range of any known Saguinus species and there is scarcely
any molecular data published for it (Ruiz-Garcia et al., 2014). Currently, Saguinus leucopus is
classified as endangered by IUCN and is in appendix 1 of CITES. There are no protected areas
for this species except for one small preserve. However it is interesting to note that this endemic
Colombian species is one of the Neotropical primate species which has managed to adapt and
live within the cities. The same has been observed for Aotus lemurinus in Manizales
(Colombia), Saguinus bicolor and Saimiri spp in Manaus (Brazil), different species of
Callithrix in diverse Atlantic Brazilian cities (such as Vitoria or Rio de Janeiro) and the brown
howler monkey (Alouatta clamitans) in the Brazilian city of Porto Alegre.

Taxonomy of species in Callitrichidae family (marmosets and tamarins)

Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primate
Family: Callitrichidae
Genera: Callithrix, Cebuella, Callibella, Mico, Saguinus,
Leontopithecus, and Callimico
Species: Callibella humilis (Van Roosmalen et al., 1998), Callithrix aurita (Geoffroy,
1812), Callithrix flaviceps (Thomas, 1903), Callithrix geoffroyi (Geoffroy,
 An Introduction to Neotropical Primates 7

1812), Callithrix jacchus (Linnaeus, 1758), Callithrix kuhlii (Coimbra-Filho,

1985), Callithrix penicillata (Geoffroy, 1812), Cebuella pygmaea (Spix,
1823), Leontopithecus caissara (Lorini and Persson, 1990), Leontopithecus
chrysomelas (Kuhl, 1820), Leontopithecus chrysopygus (Mikan, 1823),
Leontopithecus rosalia (Linnaeus, 1766), Mico acariensis (Van Roosmalen et
al., 2000), Mico argentatus (Linnaeus, 1771), Mico chrysoleucus (Wagner,
1842), Mico emiliae (Thomas, 1920), Mico humeralifera (Geoffroy, 1812),
Mico intermedius (Hershkovitz, 1977), Mico mauesi (Mittermeier, et al,
1992), Mico leucippe (Thomas, 1922), Mico manicorensis (Van Roosmalen
et al., 2000) Mico marcai (Alperin, 1993), Mico melanurus (Geoffroy, 1812),
Mico nigriceps (Ferrari and Lopes, 1992), Mico rondoni (Ferrari et al., 2010),
Mico saterei (Silva Jr. and Noronha, 1998), Saguinus bicolor (Spix, 1823),
Saguinus fuscicollis (1823), Saguinus geoffroyi (Pucheran, 1845), Saguinus
imperator (Lönnberg, 1940), Saguinus inustus (Schwarz, 1951), Saguinus
labiatus (Geoffroy, 1812), Saguinus leucopus (Güunther, 1877), Saguinus
martinsi (Thomas, 1912), Saguinus mystax (Spix, 1823), Saguinus
melanoleucus (Ribeiro, 1912), Saguinus midas (Linnaeus, 1758), Saguinus
niger (Geoffroy, 1803), Saguinus nigricollis (Spix, 1823), Saguinus oedipus
(Linnaeus, 1758), Saguinus tripartitus (Milne-Edwards, 1878).

Cebidae
The Cebidae family (capuchins and squirrel monkeys) contains 2 genera (Cebus and
Saimiri), 21 species, and 35 taxa (chapters 4-7, 10, 14, 15, 18, 19). This is a diverse and complex
family that has the distinction of having a rather confusing and somewhat controversial
taxonomy. New mitochondrial data collected from over 450 capuchin monkeys (Ruiz-García
al., Chap 7) supports the removal of Sapajus as a genus and thus, as noted above, recommends
the existence of two rather than three genera, in disagreement with early studies (Silva 2001 &
2002, Lynch Alfaro et al., 2012). At the taxonomic level of species, the authors recognize the
value of the phylogenetic species concept, but also caution against its indiscriminate use leading
down the path of taxonomic inflation (Zachos et al., 2013). Together, chapters 4, 5, 6, and 7
offer genetic data on 944 capuchin monkeys.
The Cebidae are divided unequally into two groups, capuchins (Cebus) (Figure 3) and the
smaller squirrel monkeys (Saimiri) (Figure 4). It is not our intention to discuss nor describe all
species in this family in detail, rather here we provide an overview of each group beginning
with the capuchins. Capuchins have a wide variety of names tied to their outward appearance
or to their behavior. Take for example, the bearded capuchin (Cebus apella libidinosus), the
white fronted capuchin (Cebus albifrons), or the large headed capuchin (Cebus apella
macrocephalus) which reflect their appearance. Some capuchins have alternative common
names that reflect their behavior and food preference.
For example, the large headed capuchin is also referred to as maicero or corn eater in
Colombia. Species in the genus Cebus are considered medium-sized primates and range in size
from approximately 2.5 to 5 kg (Fragaszy et al., 2004). For the tufted capuchin Cebus apella,
8 Joseph M. Shostell and Manuel Ruiz-Garcia

Leigh (1994) reported males weighing as much as 6.1 kg compared to females of 3.2 kg, a clear
sign of sexual dimorphism.

Figure 3. Capuchins photographed by M. R-G: A) A Cebus albifrons and his friend: a dog. Photo taken
near from Puyo in the Ecuadorian Amazon in 2011. B) A Cebus apella macrocephalus sampled in the
Napo River (Peru) in 2003. C) A Cebus albifrons sampled in the Ucayali River (Peru) in 2002. D) A
pair of Cebus capucinus sampled in Honduras in 2015. E) A Cebus apella cay (= libidinosus) sampled
in Puerto Suárez (Santa Cruz Department; Bolivia) near to the frontier with Brazil in 2010.

Figure 4. Squirrel monkeys: A) A little Saimiri boliviensis peruvensis lost by its mother and adopted in
an Indigene community (Bretaña; Puhinauva Channel; Ucayali River; Peru) in 2003. This specimen
showed a coat pattern typical of S. boliviensis peruvensis but its mitochondrial DNA was typical of S.
sciureus macrodon. B) An adult specimen of Saimiri boliviensis peruvensis at the Centro de
 An Introduction to Neotropical Primates 9

Primatologia in Iquitos (Peru) in 2002. C) A mother and her baby (Saimiri sciureus macrodon) below
to be sampled in the Ecuadorian city of Coca very near to the Napo River in 2013.

As an example of size, Cebus apella reach on average a height of approximately 440 mm

for males and 390 mm for females (Hakeem et al., 1996). Sexual maturity is reached between
5.5-8 years and 6-10 years in males and females respectively and they tend to be long lived
(Hakeem et al., 1996). Capuchins have prehensile tails but their grasping ability is not as
developed as the tails of spider monkeys and other atelids. Their thick molars assist them in the
mastication of their food, which for Cebus apella in a semideciduous forest of Brazil, may
consist of fruit pulp (53.9%), seeds (16%), flowers (11.1%), leaves and new shoots (6.3%),
roots (1.5%), and corn (13.9%) (Galetti and Pedroni, 1994).
Capuchins, widely distributed in the Neotropics, and given their diet, are key seed dispersal
agents for the forest communities they inhabit (Wehncke et al., 1994; Wehncke and Domíguez,
2007). They are one of the most common primates of the Neotropics capable of adapting to
multiple forest types (Mittermeier and Roosmalen, 1981). Cebus apella, for example, has a
distribution that extends from the Eastern Andes Cordillera of Colombia to approximately 27
degrees south in Brazil, a distribution larger than any other Neotropical primate species (Chap
6).
Capuchin group size, density, and home range size vary with habitat. White-throated
capuchins (Cebus capucinus) which have the most northern distribution of all capuchin species,
live in groups of 10-20 (Chap 5) and have densities of 18-30 individuals per kilometer. Home
ranges for Cebus apella vary from less than 0.2 km2 to up to 9 km2 (Spironello 2001; Terborgh
and Janson, 1983). Their group dynamics are sophisticated with evidence of coordinated group
movement (Boinski 1995) and mobbing behavior against some predators (Chapman 1986).
Perry’s work (2011) suggests capuchins also have social traditions and engage in social
learning. Furthermore, there are many studies that document their use of tools which is a clear
sign of their intelligence. We observed their intelligence in our own study as well. While Dr.
Manuel Ruiz-Garcia (M.R) was trying to take a hair sample from a capuchin (Cebus albifrons)
with a pair of tweezers the monkey snatched the tool and began to pluck at the hairs of M.R.
The roles had suddenly reversed and the capuchin had become the researcher!
Threats to capuchins includes biomedical research, deforestation, and being targeted as
agricultural pests. In support of conservation measures, Rodrigues dos Santos et al., (Chap 14)
evaluates the use of mangrove areas in Northeastern Brazil as refuge sites for capuchins
undergoing threats of habitat loss and subjected to hunting (Figure 5).
Saimiri (squirrel monkeys) are much lighter and smaller than capuchins with heights about
300 mm and weights roughly 0.90 to 1.0 kg with males slightly heavier than females (Defler
2010). They have a golden-orange color on their back, and distal parts of arms and legs whereas
the rest of their body is mostly grey, brown, or black. One of their distinguishing features is the
white mask around their eyes (Figure 6). They are distributed across Central America and parts
of South America (Groves 2004) and can reach some of the highest densities for Neotropical
primates. The Pacaya National Reserve can have squirrel monkey densities up to almost 73
ind/km2, significantly higher than any other primate.
Squirrel monkeys are shorter lived than capuchins and typically have a life span of 20 years
and live in large groups (Boinski 1987). As Boinski (2005) highlights, squirrel monkeys have
a variety of species dispersal patterns, probably greater than found in any other primate species.
10 Joseph M. Shostell and Manuel Ruiz-Garcia

For example, S. sciureus males spend most of their life alone as peripheral individuals whereas
S. oerstedii males of the same cohort tend stay together (Boinski et al., 2005).

Figure 5. Many medium and large size Neotropical primates are hunted for food by native communities.
A smoked Cebus apella to be consumed in Rivera Alta (Beni River; Bolivia) in 2003. The smoking
helps the meat to be preserved for many days in the warm climate of the jungle.

Figure 6. Squirrel monkeys: A) A Saimiri sciureus macrodon sampled in an Indigene community in the
Napo River (Peru) in 2003. B) A Saimiri sciureus macrodon sampled in the Amazon River, Colombia
in 2002. C) A Saimiri boliviensis boliviensis in the Santa Cruz Department (Bolivia) in 2010.
 An Introduction to Neotropical Primates 11

Their smaller size are both a benefit and detriment in regards to predation. Bird predators
are a particular risk for them (Boinski, 1987), but the success of avian predators is a function
of forest cover (Boinski et al., 2003). Also, given their diminutive size humans rarely hunt them
for food. What is considered as an anti-predatory strategy, all pregnant squirrel monkeys within
a group birth within a single week (Boinski 1987). Similar to other Neotropical primates,
squirrel monkeys are threatened by habitat loss and fragmentation, but they seem to be habitat
generalists and have been observed in both disturbed and undisturbed sites. Within Chapter 15,
Carretero-Pinzón discusses how the Colombian squirrel monkey copes with habitat
fragmentation.
In the last years, with the indiscriminate application of the Phylogenetic species concept,
many “supposed” species of Saimiri have been defined (from 5 to 12 different taxa).
Nevertheless, Ruiz-García et al., (2015) showed that the molecular data only detected 1 to 3
full species. This is one of the Neotropical primate taxa easily sampled from a genetics point
of view due to their large groups and because they are easily attracted to human food. For
example, in Manuel Antonio National Park (Costa Rica), many groups of Saimiri oerstedii
citrinellus daily move to the hotels around five in the afternoon to receive fruit from tourists.
This tolerance to humans allowed M.R. to quietly approach two squirrel monkeys and capture
them while they ate. He gently held them with bare hands by the nape of their necks to avoid
being bitten. Hairs were quickly sampled and the animals were liberated without any problems.
There was no need for traps, anesthetics or even tweezers.

Taxonomy of species in Cebidae family

Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primate
Family: Cebidae
Subfamilies: Cebinae, Saimiriinae
Genera: Cebus, Saimiri (squirrel monkey)
Species: Cebus apella (with a large variety of subspecies, although for some authors
are different species), C. albifrons, C. capucinus, C. flavius, C. kaapori, C.
nigritus, C. olivaceus, C. robustus, C. xantosthernos, Saimiri boliviensis (with
different subspecies), S. cassiquiarensis (with different subspecies), S.
oerstedii (with different subspecies), S. vanzolinii, S. sciureus (with different
subspecies), S. ustus. This last species is dubious with molecular analyses.

Atelidae
The Atelidae family (chapters 8, 10, 11, 12, 13, 18, 19) consists of four genera (Ateles,
Brachyteles, Alouatta, and Lagothrix) 28 species and 42 taxa (Mittermeier and Richardson,
2013). These are the largest primates of the Neotropics and some are the most threatened. Here
we provide an overview of each genus considering its morphology, distribution, threats, and
conservation.
12 Joseph M. Shostell and Manuel Ruiz-Garcia

Ateles (Spider Monkeys)

Similar to the other Atelidae genera, Ateles or spider monkeys are large bodied and mostly
arboreal (Figure 7). Primatologists studying this genus commonly disagree about the
classification of its species in part due to the intraspecific and interspecific variation in pelage
color (Hines 2005). Their colors range from red to dark gray in Mesoamerica to black in South
America. Spider monkeys have long, thin limbs giving credit to their name. They also have
prehensile tails but lack thumbs. As an example of weight, studies of Ateles geoffroyi (Figure
8) have provided a range of 3.2 to 9.0 kg (Ford and Davis 1992, Emmons and Feer 1997). As
Hines (2005) points out in his doctoral thesis, this relatively large range of weights may be due
to including immature adults. Head and body lengths for this species are 305-630 mm plus a
tail length of 520-855 mm (Emmons and Feer 1997, Reid 1997). To support their primarily
frugivorous diet (Van Roosmalen 1980) spider monkeys have a fairly large territory size. The
distribution range of spider monkeys includes Southern Mexico and extends through the
Amazon of Brazil. All of the species of the Ateles genus are endangered or critically endangered
except for Ateles paniscus (Linnaeus 1758; Red faced spider monkey) that is listed as
vulnerable (Figure 9). However, its current listing is more serious than its former listing as a
species of least concern. Their plight along with the other species within the Ateles genus has
worsened due to hunting, live capture for zoos and pets, and habitat loss. Spider monkeys also
have low reproductive rates and are very sensitive to environmental disturbances (Rosenberger
and Strier 1989). In Chapter 13, Ruiz-Garcia et al. discuss data collected from 283 spider
monkeys, the largest molecular genetics sample set of Ateles ever analyzed.

Figure 7. Photographs of spider monkeys taken by authors: A) Some individuals of Ateles belzebuth in
the Quistococha zoo near to Iquitos (Peruvian Amazon) in 2010. B) An Ateles chamek sampled in the
Yavarí River in the Brazilian Amazon near the border of Peru. C) M. R-G (second author) sampling an
 An Introduction to Neotropical Primates 13

Ateles fusciceps fusciceps near Santo Domingo de Tsáchila (Ecuador) in 2013. D) An Ateles chamek
sampled in the Santa Cruz Department (Bolivia) in 2010.

Figure 8. Photographs of spider monkeys taken by M.R-G: A) An Ateles geoffroyi yucatanensis

sampled in the Mexican Quintana Roo state in 2015. Note the blue eyes. Traditionally, only individuals
of A. hybridus were considered to have blue eyes. B) An Ateles geoffroyi yucatenensis sampled in
Belize in 2016.

Figure 9. An Ateles paniscus at the Manaus Zoo (Brazilian Amazon) in 2011.

Brachyteles

Brachyteles (muriquis) contains the largest individuals of the Atelidae family (Fonseca et
al., 1994). The southern woolly spider monkey (Brachyteles arachnoides) males can reach up
to 15 kg in weight with lengths (head plus body) of 595 mm (Aguire 1971). The pelage of
Brachyteles is gray to yellow-brown and the two species within the genus vary in face color
(complete black or with mottled pink) and presence of opposable thumbs (Rosenberger and
Strier 1989). They subsist on a diet of fruit, leaves, flowers, and to a less extent on twigs, stem,
and bark (de Carvalho et al., 2004). Data from Aguirre (1971) suggest that Brachyteles reside
14 Joseph M. Shostell and Manuel Ruiz-Garcia

in groups of 7 to 8 although Melo et al., (2005) reported group sizes of up to 18. Both have
prehensile tails and spend time social grooming (Strier 1992).
The distribution of the endemic Brackyteles in Brazil is very limited due to habitat
destruction through deforestation (Bergallo et al., 2000), hunting (Talebi and Soares 2005), and
other anthopogenic pressures. Strier (2000) estimates that there are less than 1,200 Brachyteles
individuals left within the Atlantic forest of Southeastern Brazil. Much of the southern species
(B. arachnoides) is protected within undisturbed forests of Sāo Paulo State Park whereas a large
percentage of the northern species (B. hypoxanthos) inhabits private lands (Strier and Fonseca
1996). The combined total of northern and southern populations of muriquis today (<2,200) is
far below its former estimated population size of 400,000 (Melo and Dias 2005). However,
there is good news here, the establishment of the protected reserve RPPN Feliciano Miguel
Abdala has helped one sub-population of the northern species (considered one of the most
critically endangered primates) to continually increase in size (Strier et al., 2006). Much
conservation work needs to occur to ensure and widen this progress.

Alouatta (Howler Monkeys)

Howler monkeys (Alouatta) are known for and are named after their piercing cry made
possible by their tubular shaped hyoid bone, very different from the horseshoe structure of a
human’s. There are other common characteristics among the different species of howlers (i.e.,
prehensile tail), but a similarity of phenotypes has complicated its systematics (Figures 10 &
11). To help overcome this challenge Ruiz-Garcia et al., (Chap 12) offers new mitochondrial
data and new insights about systematics in Alouatta. Colors of bodies vary from entirely black
(i.e., male black howlers, Alouatta caraya) to black with red hands (Alouatta belzebel) to
complete red (Alouatta juara, red howler). Sexual dimorphism exists with males larger than
females. For example Estrada (1982) noted the average weight of Alouatta palliata males and
females to be 7.75 kg and 6.5 kg respectively. Their densities are dependent on a number of
factors across the large distribution range of this genus. For example, densities of Alouatta
palliata in a 1500 ha reserve in Northern Costa Rica ranged from 7-15 ind/km2 (Stoner 1994)
whereas for Alouatta pigra in the Lamanai Archaeological Reserve in Belize the density
averaged 35 ind/km2 (Gavazzi et al., 2008). Group sizes and home ranges also vary across
geographical location, study, and species. As one of many examples, Carpenter (1934, 1962)
showed an average group size of Alouatta palliata of 18. Howler monkeys are generalists and
enjoy a wide distribution from Southern Veracruz, Mexico to Northern Argentina as well as a
range of elevations from 0 to 3,000 masl. And, similar to other Neotropical primates all howler
monkeys are considered important dispersal agents for forests, yet data suggests they are of
poorer quality agents compared to Ateles species. Unlike Ateles species, Alouatta tend to
defecate in piles creating dense aggregations of seeds (Andresen 2002). Of the 12 species listed
here, two are listed by IUCN as endangered with most of the remaining considered of least
concern. Compared to spider monkeys and other Atelidae, howler monkeys have some
competitive advantages including a large distribution range, being generalists, having shorter
interbirth intervals (Fedigan and Rose 1995), and being able to supplement their diets by
accessing live fences in fragmented habitats (Asensio et al. 2009). Although, howler monkeys
can live in very disturbed forests we remember one particular incident in Costa Rica when a
troop of howler monkeys (Allouata palliata) confronted an excavator that was clearing the trees
 An Introduction to Neotropical Primates 15

near them. For all of their fortitude they are surprisingly very delicate as offspring and difficult
to feed. They also easily die from rickets. We observed many young howler monkeys
succumbed to this disease in Colombia, Peru and Brazil. However, the howler monkeys from
Trinidad and Tobago seemed relatively easy to rear (by locals) from babies to adults without
providing any special food.

Figure 10. Photographs of howler monkeys taken by authors: A) A skull of a male of Alouatta seniculus
from the Antioquia Department (Colombia). B) A young exemplar of Alouatta coibensis trabeatta from
the Azuero Peninsula (Panama) in 2013. C) M. R-G sampling some red howler monkeys (Alouatta spp)
in Trinidad and Tobago in 2014. D) Two Alouatta pigra sampled in the Community Baboon Sanctuary
Visitor Center in Bermundian Landing (Belize) in 2016.

Figure 11. Photographs of howler monkeys taken by authors: A) A young Alouatta pigra female around
two years old sampled in the Community Baboon Sanctuary Visitor Center in Bermundian Landing
16 Joseph M. Shostell and Manuel Ruiz-Garcia

(Belize) in 2016. B) An Alouatta palliata sampled in Manta (Ecuador) in 2013. C) A female of

Alouatta caraya sampled in Santa Ana de Yacumo in the Mamoré River (Beni Department, Bolivia) in
2003. D) An Alouatta seniculus sampled near Genaro Herrera in the Ucayali River (Peruvian Amazon)
in 2002.

Lagothrix (Woolly Monkeys)

The Lagothrix genus (woolly monkeys) is comprised of two arboreal species, one having
four molecularly confirmed morphological subspecies (Ruiz-Garcia et al., 2014). Each species
has thick woolly hair, a prehensile tail, and pseudo opposable thumbs (Figure 12) (Ramirez
1989). They are one of the larger primates with males of L. lagotricha cana weighing an
average of 9.49 kg. Other Lagothrix taxa such as L. lagotricha lagotricha are lighter, with males
and females weighing of 7.28 kg and 7.02 kg respectively (Smith and Jungers 1997). In regards
to size, Lagothrix lagotricha cana has a length (body + head) of approximately 495 mm for
males and only slightly smaller for females. Woolly monkeys feed on fruit, leaves, flowers, and
buds and have an important niche as seed dispersal agents because their feeding behavior
positively affects tree recruitment (Levi and Peres 2013, Peres et al., 2016). They are distributed
in the Amazon of Brazil, Peru, Ecuador, and Colombia with highest densities of over 30
ind/km2 (Fooden 1963, Peres 1988). Lopez-Strauss et al., (Chap 19) discusses the distribution
records of Lagothrix lagotricha in Bolivia and Puertas et al., (Chap 18) provides an analysis of
this species’ population trends between 2006 and 2014. The average group size of Lagothrix
lagotrica in Northern Colombia is roughly 11 but has been known to range from 1 to 18
(Kavanagh and Dresdale 1975). Peres (1996) noted group sizes of up to 49 for this species
within the Northwestern Amazon. The main threats to Woolly monkeys are subsistence and
market hunting (Peres 1990), and habitat loss (Figure 13). Three of the woolly monkey species
are listed as either critically endangered or endangered and all five species are experiencing a
decrease in their population size. One of the critically endangered species, formerly considered
to be in a separate genus, is discussed more in detail below.

Figure 12. Photographs of woolly monkeys: A) A Lagothrix lagotricha poeppigii sampled in the San
Martín Department, Huallaga River, Peru in 2008. B) A Lagothrix lagotricha lagotricha (gray) in the
 An Introduction to Neotropical Primates 17

forefront and a Lagothrix lagotricha poeppigii in the background (reddish-brown). Both taxa live in
Ecuador. C) A female of the endemic Colombian Lagothrix lagotricha lugens in 2002. D) M. R-G with
a female Lagothrix lagotricha in 2013.

The yellow tailed woolly monkey (Lagothrix flavicauda) Humboldt 1812 has also been
referred to as Oreonax flavicauda (Figure 14). Its common name matches its prehensile tail,
which is indeed partly yellow. We have limited information on this species, relying on very
few and infrequent studies. After the discovery of this species by Humbold in 1802 it was not
mentioned again until 1926, and then there was another gap until 1976 (Graves and O’Neill
1980). The authors described a dead specimen of 400 mm long (head + body) that possessed a
tail 575 mm long. One of the few more recent studies by Deluycker (2007) reported group sizes
of up to 20.

Figure 13. Skin of a Lagothrix lagotricha cana (tschudii) from Northern Bolivia. This population of
Lagothrix was discovered in Bolivia in 1999. This photo was taken in the Colección Boliviana de
Fauna in 2010.

Figure 14. The skin of the endemic Peruvian and very rare Lagothrix flavicauda. Some authors claimed
that this taxon should be classified as a different genus, Oreonax flavicauda. However, these claims
were based on a small amount of morphological data. Molecular genetics analyses clearly show that
this taxon belongs to the genus Lagothrix. A) A Lagothrix flavicauda specimen from the mastozoology
18 Joseph M. Shostell and Manuel Ruiz-Garcia

collection of the San Marcos University in Lima (Peru) in 2009. Note the yellow coloration in the
scrotal and ventral tail areas. B) A stuffed exemplar of Lagothrix flavicauda in the Natural History
Museum of San Marcos University in Lima (Peru) in 2009.

This lack of data is due to the yellow-tailed woolly monkey living in a difficult to access
terrain at a higher elevation (1,500-2,700 masl) on the eastern side of the Peruvian Andes
(Buckingham and Shanee 2009). Deforestation, not responding well to disturbance (Leo Luna
1987), and only having a very limited habitat, help to explain why this species is critically
endangered (Figure 15). Clearly there is great need to obtain a current population size estimate
of this species. To assist in taxonomic and conservation efforts, Ruiz-Garcia et al., recently
published the first molecular analysis of Lagothrix flavicauda (Ruiz-Garcia et al., 2014).

Figure 15. A live individual of Lagothrix flavicauda sampled in the Upper Mayo River (San Martín
Department, Peru) in 2010. This is one of the most critically endangered primates in the world. There
are no more than 250 individuals estimated to be living in wild. Indeed, it was re-discovered in 1974
after it was considered extinct. No public zoo in the world has a live individual of this species.
However, M.R-G was able to observe this captive individual within a private Ecuadorian zoo. To our
knowledge this is the only example of a live captive individual of this species.

As we note here, everyone has a role to play in conservation efforts. In an expedition to the
Peruvian Neotropical rain forest, M. R-G and his team saved a young female of Lagothrix
lagotricha poeppiggii (named Inia) in a market from Iquitos (Figure 16). The animal was for
sale to be eaten. In the Peruvian Amazon forests, people eat woolly monkey’s tail soup (sopa
de cola de Choro). The researchers bought the animal for 40 soles (around 10-12 US dollars)
and carried it on their scientific boat for two months. This young female was very intelligent.
She seemed to delight in stealing human food, wetting human clothing and bedding, and eating
toothpaste.
Taxonomy of species in Atelidae family

Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
 An Introduction to Neotropical Primates 19

Order: Primate
Family: Atelidae
Genera: Alouatta, Ateles, Brachyteles, Lagothrix.
Species: Alouatta arctoidea (Cabrera, 1940), A. belzebul (Linnaeus 1766), A. caraya
(Humboldt 1812), A. juara (Elliot 1910), A. discolor (Spix 1823), A. guariba
(Humboldt 1812), A. macconnelli (Elliot 1910), A. nigerrima (Lönnberg
1941), A. palliata (Gray 1849), A. pigra (Lawrence 1933), A. puruensis
(Lönnberg 1941), A. sara (Elliot 1910), A. ululata (Elliot 1912), Ateles
belzebuth (Geoffroy 1806), A. chamek (Humbodt 1812), A. geoffroyi (Kuhl
1820), A. fusciceps (Gray 1812), A. hybridus (Geoffroy 1829), A. marginatus
(Geoffroy 1809), A. paniscus (Linnaeus 1758), Brachyteles arachnoides
(Geoffroy 1806), B. hypoxanthus (Kuhl 1820), Lagothrix lagotricha cana
(Geoffroy 1812), L. lagotricha lagotricha (Humboldt 1812), L. lagotricha
lugens (Elliot 1907), L. lagotricha poeppigii (Schinz 1844), Lagotricha
flavicauda (Humboldt 1812). The molecular results could show a lower
number of species in Ateles.

Pitheciidae
The pitheciidae family (chapters 8, 10, 16, 17, 18, 19) contains the uakari (Cacajao), titi
monkeys (Callicebus), bearded saki (Chiropotes), and saki monkeys (Pithecia). In this section
we discuss each of these genera.

Cacajao (Uakari)

The origination of the Cacajao name may be from the ‘kah kah’ calling sound it makes.
20 Joseph M. Shostell and Manuel Ruiz-Garcia

Figure 16. A young female (named Inia) of Lagothrix lagotricha poeppigii after stealing food from
humans in Iquitos (Peru) in 2003.

All three Cacajao species have no opposable thumbs nor a prehensile tail, but there are
some defining characteristics for each species (Figure 17). For instance, Cacajao calvus has a
hairless red head, a result of a thin epidermal layer and presence of vascular capillaries (Majory
et al., 2015). On the other hand, C. melanocephalus has a full head of hair. Finally, Cacajao
ouakary is the largest of the three species and has a pale orange/white pelage. Adults weigh
approximately 2.7 to 3.45 kg (Ayres 1986) and their lengths are 360-570 mm (body + head)
(Ayres 1989). Tail length is minimal at only about 137-185 mm. They are frugivorous but also
consume great quantities of unripe seeds from trees (Ayres 1989, Boubli 1999, Kinzey 1992).
Cacajao are distributed in Brazil, Colombia, Peru and Venezuela (Hershkovitz 1987, Boubli
1997) and can reach densities of 10-17 ind/km2 (Ayres 1986, Bowler
et al., 2013, Paim 2005). Deforestation and hunting are the main threats to this genus and they
are considered one of the rarer primates in the lowland area of the Amazon. They are also
natural prey of Harpy Eagles (Harpya harpya) (Leonard and Bennett 1996). Good news, the
genus is found within the Pico dal Neblina National Park of Brazil and the Venezuelan Serrania
de la Neblina National park which together make up the largest protected area of tropical
rainforests in the world (Boubli 2002). However, these “protected” areas are not entirely safe
since gold mining can occur within. Currently Cacajao calvus is listed as threatened by IUCN
(2008).

Figure 17. Photos of uakari monkeys: A) A pair of Cacajao calvus living in the house of a human
family in Iquitos (Peru) in 2002. The children of the family said that their mother loved the uakaris
more than themselves. B) A Cacajao calvus in Iquitos (Peruvian Amazon) in 2002. C) A Cacajao
calvus at the Nanay River, near Iquitos (Peru) in 2010. D & E) An adult male of Cacajao calvus in the
Huachipa zoo (Lima, Peru) in 2009.
 An Introduction to Neotropical Primates 21

The uakaris are extremely jealous and very dangerous because they have large canines.
The eminent North-American primatologist, Thomas Defler who has lived in Colombia for the
last 30 years, commented that at the Caparú Station near the Apaporis River (Colombian
Amazon), he cares for a uakari male which was in love with one of his female students. Once,
when Thomas approached the student, the uakari furiously rushed in and tried to bite his jugular
vein. He thought that it was his time to die.

Callicebus

The Callicebus genus contains one of the most diverse assemblages of species. These are
the highly arboreal, small to medium-sized titi monkeys (Figure 18). They have no opposable
digits and possess thick, long hair (Hershkovitz (1990) and a pelage color that varies across
species. For example C. pallescens has a pale buff agouti whereas C. cupreus has a buff brown
agouti interspersed with reddish areas (sideburns, underparts of body, inner surface of limbs),
and C. moloch has a pelage that is grey, reddish, or brown (Jones and Anderson 1978).
Depending on the species, titi monkeys weigh between approximately 0.5 to 2 kg (Jones and
Anderson 1978, Hershkovitz 1988, Smith and Jungers 1997) and have a body- head length of
270-450 mm (Hershkovitz 1990) in addition to a long non-prehensile tail. They inhabit tropical
rain forests of the Oronoco and Amazon basins as well Brazil’s Atlantic Forest Region and
drier forests of Bolivia and Paraguay (Van Roosmalen et al., 2002, Wallace et al., 2006).
Studies document varying densities across location and species. For instance Chiarello (2000)
noted titi monkey (Callicebus personatus) densities from 0.28 to 10.2 ind/km2. Other authors
(Freese 1975, Jones and Anderson 1978) showed a greater range and upper density value (2.1-
24 ind/km2).
22 Joseph M. Shostell and Manuel Ruiz-Garcia

Figure 18. Photographs of titi monkeys: A) Callicebus moloch sampled near the Tapajos River (Brazil)
in 2005. B) Callicebus cupreus sampled near Indiana, Amazon River in Peru in 2003. C) Callicebus
cupreus in Atalaia do Norte (Yavarí River, Brazil) in 2003 D) Callicebus donacophilus sampled at
Puerto Suárez (Santa Cruz Department, Bolivia) in 2010. E) Callicebus discolor at the Napo River
(Peru) in 2010. F) Callicebus lugens sampled in the Guainia Department (Colombia) in 2011.

Titi monkeys are very vocal, live in a network of groups (Wright 1989), and demonstrate
a parental division of labor (Menzoza 1986). Their diets consist of fruit (mostly), leaves, and
insects (Kinzey et al., 1977). Titi monkeys do have threats, but they seem to thrive in disturbed
forest areas. In antithesis of many other Neotropical primates, titi monkey densities are highest
in disturbed areas (Van Roosmalen et al., 2002). This is probably the Neotropical primate genus
that requires the greatest amount of karyological and molecular analyses to appropriately
understand the evolutionary and phylogenetic relationships among the possible species
contained in this genus.
These monkeys are monogamous and they are extremely loving and faithful with the
person which raises them. They consider their human owner to be their mate. Indeed, each
night, they sleep in the bed with their human owner.

Chiropotes (Bearded Sakis)

There are five generally accepted species in Chiropotes (the bearded sakis). They are
recognized by their conspicuous beards, temporal swellings, and bushy non-prehensile tails
(Van Roosmalen et al., 1981). They are much larger than sakis (Pithecia), yet smaller than
 An Introduction to Neotropical Primates 23

uakaris. Bearded sakis have average weights of 3.1 kg and 2.6 kg for males and females
respectively (Ford 1994) and their bodies (up to a little over 400 mm in males) and tails are
comparable in length (up to about approximately 385 mm in females) (Hershkovitz 1985).
There is little sexual dimorphism in bearded sakis, but unlike titis and sakis, bearded saki males
have extremely large and conspicuously colored scrota. For example, they can even be bright
pink. Another difference is that bearded sakis and uakaris have long, curved penile spines
(Hershkovitz 1993, Dixson 1998). Similar to uakaris, bearded sakis form groups as large as 56
that have multiple subgroups (Ayres 1981, Ayres 1986). These larger groups, also referred to
as troops, break up at feeding sites. Norconk and Kinzey (1994) suggest this as a strategy to
reduce competition. Neither titi monkeys nor sakis have this type of group structure. Bearded
sakis are mostly frugivores eating fruit pulp and seeds, but also eat flowers and to a lesser extent
insects (Santos 2002). The genus is found in Brazil, French Guiana, Guyana, Suriname,
Venezuela, and Columbia. General threats to bearded sakis are habitat loss, habitat
fragmentation, and hunting. The distribution of the species within this genus are not equal nor
are the severity of threats. For example, Chiropotes satanas (black bearded saki), endemic to
the Eastern Amazonia within Brazil, is listed as critically endangered by IUCN and is projected
to decline by 80% in the next thirty years. Also, both Chiropotes albinasus (red nosed bearded
saki) and Chiropotes utahicae (Uta Hick’s bearded saki) are listed as endangered and are
threatened by the trans Amazon highway as well as farming and ranching. Recommended
conservation strategies for Chiropotes spp. include carefully monitoring their international
trade as well as creating additional protected reserves and captive breeding programs.

Pithecia (Sakis) (Chapters 10, 17)

According to Hershkovitz (1987) the Pithecia genus (Sakis) consists of five species.
However, Marsh (2014) used a morphological point of view and named 16 species of Pithecia.
It’s very likely that when molecular analyses of all the Pithecia taxa are carried out, the number
of real species will be considerably less.
Sakis have long bushy tails, and a pelage ranging from reddish brown to black (Figure 19).
Males and females have weights of 1.8-3 kg and 1.51- 2.70 kg respectively (Ayres and Clutton-
Brock 1992). Thus, they are considered medium sized primates and are smaller than their
uacaris cousins. Their size makes them vulnerable to a series of natural predators including
mammals, raptors (Luna et al. 2010), and snakes. With low reproduction rates, even a
successful catch of one saki per year per predator could disrupt a population (Struhsaker and
Leakey 1990, Janson 1992). Sakis live in small (2-4, upper range of 7) (Buchanan et al. 1981,
Oliveirar et al. 1985) social monogamous groups (Di Fore et al. 2007) and each group has one
sexually mature male and one sexually mature female. Going from individual group sizes to
calculating density of individuals per area it is clear that we are missing much information
regarding this genus. In fact, Vié et al. (2001) is one of the few studies that provides density
data (0.64 ind/km2). Two of the five species (Pithecia monachus) and Pithecia irrorata) of the
genus are listed as being data deficient by IUCN. Moreover, our knowledge of the distribution
of Pithecia aequatorialis is also incomplete. Insufficient data on these species makes it very
challenging to create helpful conservation plans to protect them. Further complicating the
collection of data are the behavior characteristics of these species. They tend to be shy, move
very silently, and are difficult to capture (Vié et al. 2001). Parts of chapters 10 (phylogenetics),
24 Joseph M. Shostell and Manuel Ruiz-Garcia

17 (biogeography and conservation), 18 (Pithecia in national reserve) and 19 (distribution and

conservation in Bolivia) provide new data and analyses of this genus.

Figure 19. Photos of Pithecia: A) Pithecia aequatorialis sampled at the Napo River in Peru in 2003. B)
A Pithecia aequatorialis (left) and a Pithecia monachus (right) at the Isla de Los Monos in the Amazon
River (Peru) in 2010. C) A family of Pithecia inusta in Las Leyendas Zoo in Lima (Peru, 2010). D) A
female Pithecia chrysocephala in Manaus (Brazil, 2012).

During the 1990’s it was relatively easy to find skulls, skins and young animals of the
larger Neotropical primates (Lagothrix and Alouatta, and to a lesser extent Ateles) in many
indigenous communities of the Colombian and Peruvian Amazon. At that time the indigenous
people intensely hunted these large primates and relied on them as a significant source of meat.
However, it has been considerably more difficult to obtain samples from large Neotropical
primates in these communities from 2005 through today. In contrast, it is easier to obtain skulls
and tissues from Pithecia today than during the 1990s. This could mean that genera such as
Lagothrix and Alouatta have been extirpated by hunting in many areas near indigenous
communities in the last few decades and that Pithecia monkeys are currently heavily hunted.
Unfortunately, these monkeys are also hunted for their furry tails to be used as dusters.

Taxonomy of species in Pitheciidae family

Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primate
Family: Atelidae
Genera: Cacajao, Callicebus, Chiropotes, Pithecia
 An Introduction to Neotropical Primates 25

Species: Cacajao calvus (Geoffroy 1847), C. melanocephalus (Humboldt 1811), C.

ouakary (Spix 1823), Callicebus modestus (Lönnberg 1939), C. donacophilus
(D’Orbigny 1836), C. pallescens (Thomas 1907), C. olallae (Lönnberg 1939),
C. oenanthe (Thomas 1924), C. cupreus (Spix 1823), C. discolor (Geoffroy
and Deville 1848), C. ornatus (Gray 1886), C. caligatus (Wagner 1842), C.
dubius (Hershkovitz 1990), C. stephennashi (Van Roosmalen, Van
Roosmalen and Mittermeier 2002), C. cinerascens (Spix 1823), C. hoffmannsi
(Thomas 1908), C. baptista (Lönnberg 1939), C. moloch (Hoffmannsegg
1807), C. brunneus (Wagner 1842), C. bernhardi (Van Roosmalen, Van
Roosmalen, and Mittermeier 2002), C. aureipalatii (Wallace et al., 2006), C.
medemi (Hershkovitz 1963), C. torquatus (Hoffmannsegg 1807), C. lugens
(Humbodt 1811), C. lucifer (Thomas 1914), C. purines (Thomas 1914), C.
regulus (Thomas 1927), C. personatus (Geoffroy 1812), C. nigrifrons (Spix
1823), C. melanochir (Wied-Neuwied 1820), C. barbarabrownae
(Hershkovitz 1990), C. coimbrai (Kobayashi and Langguth 1999), Chiropotes
albinasus (Geoffroy and Deville 1848), C. satanas (Hoffmannsegg 1807), C.
chiropotes (Humboldt 1811), C. utahickae (Hershkovitz 1987), C. israelita
(Spix 1823), Pithecia pithecia (Linnaeus 1758), P. monachus (Geoffroy
1812), P. irrorata (Gray 1842), P. albicans (Gray 1860), P. aequatorialis
(Hershkovitz 1987).
Aotidae
The Aotus genus (night monkeys) (Chapters 8, 9, 19) contains a growing list of species. Up
until 1983 there was only one recognized Aotus species (Aotus trivirgatus) and an assemblage
of diverse subspecies (Hershkovitz 1949, Hernnández-Camacho and Cooper 1976). A series of
publications presenting new biogeographical, karyotypical and morphological data about
Aotidae helped to persuade primatologists to increase the number of Aotus species (Ma 1981,
Ma et al., 1976a, 1976b, 1980, and Hershkoitz 1983) as well as place them in their own family.
Chapter 9 lists all 13 Aotus species and provides new insights about their systematics and
phylogenetic relationships.
26 Joseph M. Shostell and Manuel Ruiz-Garcia

Figure 20. Photographs of night monkeys: A) This Aotus spp. was sampled in the Southern Andes of
Ecuador in 2011. Its phenotype resembles that of Aotus nancymaae, although this species is not yet
reported for Ecuador. B) This is probably an Aotus lemurinus. It was sampled near Macas (Ecuadorian
Amazon) in 2011. However, this taxon is reported for mountain habits and this specimen was obtained
in the Amazon. The taxonomic situation of Aotus in Ecuador must be clarified. C) A young individual
of Aotus nigriceps sampled in Novo Aripuana (Madeira River, Brazil) in 2012.

Night monkeys have several unique characteristics (Figure 20). Perhaps the most obvious
is the masking of their external ears in their fur making it seem that they have no earlobes;
hence their name (a = without, otis = ear). They lack a prehensile tail, have a dense pelage and
large eyes. Their common name, night monkeys, is due to their nocturnal habits and they seem
to be most active at dawn and dusk. However, one species, Aotus azarai is cathemeral and is
active during the day and night (Erkert et al., 2012). Weights of adults (males and females)
range from roughly 0.57 to 1.6 kg (Hernández-Camacho and Defler 1985, Hernandez-Duque
2004). Densities of night monkeys vary greatly with study and geographic location. For
example Green (1978) reported densities of Aotus griseimembra in the Bolivar Department in
Colombia to be 1.5 ind/km2. In contrast, Fernandez-Duque et al., (2001) recorded densities of
Aotus azarai azarai at over 60 ind/km2 in Argentina. There was even a higher density of 150
ind/km2 of A. a. boliviensis (Garcia and Braza 1989) in a forest remnant that may have served
as a refuge. The accuracy of distribution studies will be influenced by the time of day they were
conducted since night monkeys are nocturnal. Fairly unique among primates, night monkeys
form monogamous groups comprised of a pair of sexually mature adults (male and female)
along with an infant, juvenile or sub-adult. Males share parenting of infants taking up the brunt
of this responsibility (carrying, sharing food, and playing) in the third week (Juárez et al., 2003,
Rotundo et al., 2002).
Night monkeys have a diet of fruit nectar, flowers, leaves, and for some (Aotus brumbacki
and Aotus zonalis) insects as well (Hladik et al., 1971, Solano 1995). These arboreal primates
inhabit multiple forest types including primary and secondary forests as well as tropical and
 An Introduction to Neotropical Primates 27

dry forests at a range of elevations (Hermández-Camacho and Cooper 1976, Brooks 1996,
Defler 2003). Four of the Aotus species are listed as vulnerable by IUCN and they do face
multiple threats. Some Aotus species have been heavily sought after since the early 1970s as
models in biomedical research (Hernández-Camacho and Cooper 1976, Maldonado et al.,
2009). Consequently, thousands of night monkeys are removed annually to further the
development of vaccinations against malaria and other tropical diseases (Gozalo et al., 1996,
Spirig et al., 2005, Daubenberger et al., 2007). Their benefits to research have spurred on legal
and unfortunately, illegal trades (Figure 21). In Colombia for example, the illegal trade of Aotus
nancymaae has been an absolute national scandal and it has been reflected in all communication
media (see Ruiz-García et al., 2013). Night monkeys are also affected by illegal trafficking to
support the pet industry. To offset the biomedical demand, centers have developed, such as the
Reproduction and Conservation of Non-Human Primates at Iquitos in Peru. Careful
management of these centers is important as is the enforcement of governmental regulations of
animal trafficking. Conservation of Aotus azarae and Aotus nigriceps is further discussed in
chapter 19.

Figure 21. The illegal trade of Aotus due to laboratories working with malaria vaccines has been a
serious problem in Colombia. To counter this activity researchers are helping to determine the origin of
these animals and if permissions have been granted. This was an Aotus vociferans sampled for blood in
a laboratory from Leticia (Colombian Amazon).

The face of the night monkeys seems gentle and huggable but this species can be very
aggressive and can provide very serious bites. We experienced these attacks first hand in
Argentina and Ecuador.

Taxonomy of species in Aotidae family

28 Joseph M. Shostell and Manuel Ruiz-Garcia

Kingdom: Animalia
Phylum: Chordata
Class: Mammalia
Order: Primate
Family: Aotidae
Genus: Aotus
Species: Aotus azarae (Humboldt 1811), A. boliviensis (Elliot 1907), A. brumbacki
(Hershkovitz 1983), A. griseimembra (Elliot 1912), A. infulatus (Kuhl 1820),
A. jorgehernandezi (Defler and Bueno 2007), A. lemurinus (I. Geoffroy 1843),
A. miconax (Thomas 1927), A. nancymaae (Hershkovitz 1983), A. nigriceps
(Dollman 1909, A. trivirgatus (Humboldt 1811), A. vociferans (Spix 1823),
A. zonalis (Goldman 1914).

ACKNOWLEDGMENTS
Special thanks to Sophia Shostell and Joelle Shostell for their continued support. Also,
special thanks to Mark Katsohs for his enthusiasm to see this project succeed. Thanks also to
Penn State University Fayette—The Eberly Campus and the University of Minnesota
Crookston for their support and for recognizing the significance of research in a changing
world. Also, thanks to the many collaborators who helped to obtain Neotropical primate
samples over the last 20 years. Those who should be especially mentioned are Pablo Escobar-
Armel (Colombia), Diana Alvarez (Colombia), Nicolás Lichilín (Colombia), Kelly Luengas
(Colombia), Luisa Castellanos (Colombia), Myreya Pinedo (Colombia), Lina Argüello
(Colombia), Hugo Gálvez (Peru), Alan Velarde (Peru), Armando Castellanos (Ecuador),
Andrés Laguna (Ecuador), Bob Wallace (Bolivia), Julieta Vargas (Bolivia), Gustavo Gutierrez-
Espeleta (Costa Rica) and Andrés Eloy Bracho (Venezuela). Finally, we thank the many
indigenous communities in Mexico, Guatemala, Belize, Honduras, Costa Rica, Panama,
Colombia, Venezuela, Trinidad and Tobago, French Guiana, Ecuador, Peru, Bolivia, Brazil,
Paraguay and Argentina for their assistance in obtaining samples of Neotropical primates to
enhance our population genetics, phylogeography, phylogenetic, systematic and evolutionary
biology knowledge of these amazing creatures.

REFERENCES
Aguirre, A. C. (1971). O mono Brachyteles arachnoides (E. Geoffroy). Situaçáo actuala da
espécie no Brasil. Academia Brasiliera de Ciencias. 53 pp.
Andresen, E. (2002) Primary seed dispersal by red howler monkeys and the effect of defecation
patterns on the fate of dispersed seeds. Biotropica, 34 (2): 261-272.
Asensio, N., Arroyo-Rodriguez, V., Dunn, J. C., and Cristóbal-Azkarate. (2009). Conservation
value of landscape supplementation for howler monkeys living in forest patches.
Biotropica, 41(6): 768-773.
 An Introduction to Neotropical Primates 29

Aulu, J. (1976) Seasonal sex skin colouration and hormonal fluctuations in free-ranging and
captive monkeys. Hormones and Behavior 7: 481–494.
Ayres, J. M. (1981). Observações sobre a ecologia e o comportamento dos cuxiús (Chiropotes
albinasus e Chiropotes satanas, Cebidae: Primates) Master’s Thesis. Manaus: Instituto
Nacional de Pesquisas da Amazônia e Fundação Universidade do Amazonas.
Ayres, J. M. (1989). Comparative feeding ecology of the uakari and bearded saki, Cacajao and
Chiropotes. Journal of Human Evolution 18: 697-716.
Ayres, J. M., and Clutton-Brock, T. H. (1992). River boundaries and species range size in
Amazonian primates. The American Naturalist 140 (3): 531-537.
Ayres. J. M. (1986). The white uakaris and the Amazonian flooded forests. PhD thesis.
Cambridge University, Cambridge, UK.
Bergallo, H. G., Geise, L. Bonvicino, C. R., Cerqueira, R., D’Andrea, P., Esberard, C. E. et al.,
(2000). Memíferos. In: A Fauna Ameaçada de Extinçāo do Estado do Rio de Janeiro (Eds.)
Bergallo, H. G., Rocha, C. F D., Alves, M. A. S., and Sluys, M. C. pp. 125-135. Editora da
Universidade do Estado do Reo de Janeiro Rio de Janeiro, Brazil.
Bodmer, R. E., Eisenbergy, J. F., Redford, K. H. (1997). Hunting and the likelihood of
extinction of Amazonian mammals. Conservation Biology 11 (2): 460-466.
Boinski, S. (1987). Birth synchrony in squirrel monkeys (Saimiri oerstedi): a strategy to reduce
neonatal predation. Behavioral Ecology and Sociobiology 21 (6): 393-400.
Boinski, S. and Campbell, A. F. (1995). Use of trill vocalizations to coordinate troop movement
among white-faced capuchins: a second field test. Behavior 132 (11/12): 875-901.
Boinski, S., Kauffman, L., Westoll, A., Stickler, C., M., Cropp S., and Ehmke, E. (2003). Are
vigilance, risk from avian predators and group size consequences of habitat structure? A
comparison of three species of squirrel monkey (Saimiri oerstedii, S. Boliviensis, and S.
sciureus. Behaviour 140 (11/12): 1421-1467.
Boinski, S., Kauffmann, L, Schet, and S., Vreedzaam, A. (2005). Dispersal patterns among
three species of squirrel monkeys (Saimiri oerstedii, S. boliviensis, and S. sciureus): II
within-species and local variation. Behaviour 142 (5): 633-677.
Boubli, J. P. (1997). A study the lack uakari, Cacajao melanocephalus, in the Pica de Neblina
National Park, Brazil. Neotropical Primates 5: 113-115.
Boubli, J. P. (1999). Feeding ecology of black-headed uacaris (Cacajao melanocephalus
melanocephalus) in the Pico de Neblina National park, Brazil. International Journal of
Primatology 20: 719-749.
Boubli, J. P. (2002). Lowland floristic assessment of Pico da Neblina National Park, Brazil.
Plant Ecology 160: 149-167.
Bowler, M., Vasecchi, J. Queiroz, H. L., Bodmer, R., and Puertas, P. (2013). Conservation of
the Pitheciids, Communities and uacaris: conservation initiatives in Brazil and Peru. In
Veiga, L. M., Barnett, A. A., Ferrari, S. F., and Norconk, M. A. (Eds.). Evolutionary
Biology and Conservation of Titis Sakis, and Uacaris, Cambridge University Press 2013.
Brooks, D. M. (1996). Some observations of primates in Paraguay. Neotropical Primates 4:
15-19.
Buchanan, D. B., Mittermeier, R. A., and Van Roosmalen, M. G. M. (1981). The saki monkeys,
genus Pithecia. In Coimbra-Filho, A. F., and Mittermeier, R. A. (Eds.). Ecology and
Behavior of Neotropical Primates. Pp. 391-417. Academia Brasileira de Ciências, Rio de
Janeiro.
30 Joseph M. Shostell and Manuel Ruiz-Garcia

Buckingham, F., and Shanee, S. (2009). Conservation priorities for the Peruvian yellow-tailed
woolly monkey (Oreonax flavicauda): a GIS risk assessment and gap analysis. Primate
Carpenter, C. R. (1934). A field study of the behavior and social relations of howling monkeys.
Comparative Psychology Monographs 10: 1-168.
Carpenter, C. R. (1962). Field studies of a primate population. In Bliss, E. L. (Ed.). Roots of
Behavior. Pp. 286-294. Harper, New York New York, USA.
Chapman, C.A. (1986). Boa constrictor predation and group response in white-faced Cebus
monkeys. Biotropica 18 (2): 171-172.
Chiarello, A. G. (2000). Density and population size of mammals in remnants of Brazilian
Atlantic forest. Conservation Biology 14 (6): 1649-1657.
Daubenberger C.A., Spirig R., Patarroyo M.E., and Pluschke G. (2007). Flow cytometric
analysis on cross-reactivity of human-specific CD monoclonal antibodies with splenocytes
of Aotus nancymaae, a non-human primate model for biomedical research. Veterinary
Immunology and Immunopathology 119(1-2), 14-20.
De Carvalho, O. Jr., Ferrari S. F., and Strier, K. B. (2004). Diet of a muriqui group (Brachyteles
arachnolides) in continuous primary forest. Primates, 45 (3): 201-204.
Defler, T.R. (2010). Historia Natural de los Primates Colombianos. Universidad Nacional de
Colombia, Bogotá, Colombia. Pp. 612
Delfer, T. R. (2003). Primates de Colombia. Conservación Internacional, Bogotá.
Deluycker, A. M. (2007). Notes on the yellow tailed woolly monkey (Oreonax flavicauda) and
its status in the protected forest of Alto Mayo, Northern Peru. Primate Conservation 22:
41-47.
Di Fiore, A., Fernandez-Duque, and Hurst, D. (2007). Adult male replacement in socially
monogamous equatorial saki monkeys (Pitecia aequatorialis). Foliã Priatologica 78: 88-
98.
Dixson, A. F. (1998). Primate sexuality. Oxford: Oxford University Press.
Ekert, H. G., Fernandez-Duque, E., and Scheideler, A. (2012). Seasonal variation of temporal
niche in wild owl monkeys (Aotus azarai azarai) of the Argentinean Chaco: a matter of
making? Chronobiology International 29 (6): 702-714.
Emmons, L. H., and F. Feer. (1997). Neotropical Rainforest Mammals: A Field Guide, Second
Edition. The University of Chicago Press, Chicago & London.
Estrada, A. (1982). Survey and census of howler monkeys (Alouatta palliata) in the rain forest
of Los Tuxtlas, Veracruz, Mexico. American Journal of Primatology 2: 363-372.
Fedigan, L. M. and Rose, L. M. (1995). Interbirth interval variation in three sympatric species
of neotropical monkey. American Journal of Primatology 37: 9-24.
Fernandez-Duque, E. (2004). High levels of intrasexual competition in sexually monomorphic
owl monkeys. International Journal of Primatology 75(suppl. 1): 260.
Fernandez-Duque, E., Rotundo, M., and Sloan, C. (2001). Density and population structure of
owl monkeys (Aotus azarai) in the Argentinean Chaco. American Journal of Primatology
53: 99-108.
Fonseca, G. A. B., Rylands, A. B., Costa, C. M. R., Machado, R. B. and Leite, Y. L. R. (1994).
Livro Vermelho dos Mamíferos Brasileiros Ameaçados de Extinção. Fundação
Biodiversitas, Belo Horizonte.
Fooden, J. (1963). A revision of the woolly monkeys (Genus Lagothrix). Journal of
Mammalogy, 44: 213-247.
 An Introduction to Neotropical Primates 31

Ford, S. M. (1994). Evolution of sexual dimorphism in body weight in platyrrhines. American

Journal of Primatology 34: 221-244.
Ford, S. M., and L. C. Davis. (1992). Systematics and Body Size: Implications for Feeding
Adaptations in New World Monkeys. American Journal of Physical Anthropology
88(4):415-468.
Fragaszy, D. M., Visalberghi, E. and Fedigan, L. M., (2004) The Complete Capuchin the
Biology of the Genus Cebus. Cambridge University Press. Cambridge, United Kingdom.
Freese, C. (1975). Final report: A census of non-human primates in Peru. (PAHO Project
AMR-0719. Pan American Healt Organization, Washington, D. C.
Galetti, M. and Pedroni, F. (1994). Seasonal diet of capuchin monkeys (Cebus apella) in a
semideciduous forest in south-east Brazil. Journal of Tropical Ecology 10(1): 27-39.
García, J. E., and Braza, F. (1989). Density comparisons using different analytic-methods in
Aoutus azarae. Primate Report 25: 45-52.
Gavazzi, A. J., Cornick, L. A., Markowitz, T. M., Green, D. and Markowitz, H. (2008). Density,
distribution, and home range of the black howler monkey (Alouatta pigra) at Lamanai,
Belize. Journal of Mammalogy 89(5): 1112-1112.
Gozalo, A., Ballou, W. R., Lucas, C. M., Wellde, B., Hall, B. T., Kumar, S., Kaslow, D.,
Haynes, D., Lyon, J., Bell, B., Wood, J., and Watts, D. M. (1996). Efficacy of passively
transferred rabbit antibody to two different recombinant Plasmodium falciparum MSP-1
constructs in infected Aotus nancymai. 45th Annual Meeting of the American Society of
Tropical Medicine and Hygiene, Baltimore, Maryland, December 1-5. Supplement to
American Journal of Tropical Medicine and Hygiene 55 (2): 163.
Graves, G. R., and O’Neill, J. P. (1980). Notes on the yellow-tailed woolly monkey (Lagothrix
flavicauda) of Peru. Journal of Mammalogy, 62 (2): 345-347.
Green, K. M. (1978). Primate censusing in northern Columbia: a comparison of two techniques.
Primates 19: 537-550.
Groves, C. P. (2004). The what, why and how of primate taxonomy. International Journal of
Primatology 25: 1105-1126.
Hakeem, A. Sandoval, R. R., Jones, M., and Allman, J. (1996). Brain and life span in primates.
In Birren, J. E. and Schaie, K. W. (Eds.). Handbook of the Psychology of Aging, 4th Edition.
Sand Diego, CA. Academic Press. pp. 78-104.
Hakeem, A., Sandoval, R. G., Jones, M., and Allman, J. (1996) Brain and life span in primates.
In Steklis, H. D. and Erwin, J. (Eds.). Handbook of the Psychology of Aging (pp. 1-39).
New York, New York: Wiley-Liss.
Hernández-Camacho, J., and Cooper, R. W. (1976). The nonhuman primates of Colombia. In
Thorington Jr, R. W. and Heltne, P. G. (Eds.). Neotropical Primates: Field Studies and
Conservation (pp. 35-69). Washington D.C.: National Academy of Sciences.
Hershkovitz, P. (1949). Mammals of northern Colombia. Preliminary report n° 4: Monkeys
(Primates), with taxonomic revisions of some forms. Proceedings of the United States
National Museum 98: 323-427.
Hershkovitz, P. (1983). Two new species of night monkeys, genus Aotus (Cebidae, Platyrrhini):
A preliminary report on Aotus taxonomy. American Journal of Primatology 4: 209-243.
Hershkovitz, P. (1985). A preliminary taxonomic review of the South American bearded saki
monkeys genus Chiropotes (Cebidae, Platyrrhini) with the description of a new subspecies.
Fieldiana: Zoology 27 (1363): 1-46.
32 Joseph M. Shostell and Manuel Ruiz-Garcia

Hershkovitz, P. (1987). The taxonomy of South American sakis, genus Pithecia (Cebidae
Platyrrhini): a preliminary report and critical review with the description of a new species
and a new subspecies. American Journal of Primatology 12: 387-468.
Hershkovitz, P. (1987). Uacaris New World monkeys of the genus Cacajao: a preliminary
taxonomic review with a description of a new subspecies. American Journal of
Primatology 12: 1-53.
Hershkovitz, P. (1988). Origin, speciation, and distribution of South American titi monkeys,
genus Callicebus (Family Cebidae, Platyrrhini). Proceedings of the Academy of Natural
Sciences of Philadelphia 140 (1): 240-272.
Hershkovitz, P. (1990). Titis, new world monkeys of the genus Callicebus (Cebidae,
Platyrrhini): A preliminary taxonomic review. Fieldiana Zoology, New Series (55): 1-109.
Hershkovitz, P. (1993). Male external genitalia of non-prehensile tailed South American
monkeys. Part 1: Subfamily Pitheciinae, Family Cebidae. Fieldiana: Zoology New Series
73: 1-17.
Hines, J. J. H. (2005). Ecology and Taxonomy of Ateles geoffroyi in Parque Nacional Pico
Bonito, Atlántida, Honduras. Doctoral Thesis. The Australian National University.
Hladik, W. M., Hladik, A., Bousset, J., Valdegbouze, P., Viroben, G., and Delort’Laval, J.
(1971). Le régime alimentaire del primates de l’oele de Barro Colorado (Panamá): résultats
des analyses quantitatives. Folia Primatologica 16: 85-122.
Janson, C. H. (1992). Evolutionary ecology of primate social structure. In Smith, E. A. and
Winterhalder, B. (Eds.). Evolutionary Ecology and Human Behaviour. Aldine de Gruyter
New York, New York.
Janson, C. H., and Emmons, L. H. (1990). Ecological structure of the nonflying mammal
community at Cocha Cashu Biological Station, Manu National Park, Peru. In Gentry, A.
H. (Ed.), Four Neotropical Forests. (pp. 314-338). Yale University Press, New Haven.
Jones, C. and Anderson, S. (1978). Callicebus moloch. Mammalian Species 112: 1-5.
Jones, C., and Anderson, S. (1978). Callicebus moloch. Mammalian species 112: 1-5.
Juárez, C., Rotundo, M. and Fernanxez-Duque, E. (2003). Behavioral sex differences in the
socially monogamous night monkeys of the Argentinean Chaco. Revista de Etologia, 5
(suppl.): 174.
Kavanagh, M. and Dresdale, L. (1975). Observations on the woolly monkey (Lagothrix
lagothricha) in northern Columbia. 16(3): 285-294.
Kay, R. F. (2015). Biogeography in deep time – What do phylogenetics, geology and
paleoclimate tell us about early platyrrhine evolution? Molecular Phylogenetics and
Evolution 82: 358-374.
Kim, D., Sexton, J. O., and Townsend, J. R. 2015. Accelerated deforestation in the humid
tropics from the 1990s to the 2000s. Geophysical Research Letters, 3495-3501.
10.1002/2014GL062777.
Kinzey, W. G. (1992). Dietary and dental adaptations in the Pitheciinea. American Journal of
Physical Anthropology 88: 499-514.
Kinzey, W. G. Rosenberger, A. L., Heisler, P. S., Prowse, D. L. and Trilling, J. S. (1977). A
preliminary field investigation of the yellow handed titi monkey, Callicebus torquatus
torquatus, in Northern Peru. Primates 18 (1): 159-181.
Leigh, S. R. (1994). Relations between captive and noncaptive weights in anthropoid primates.
Zoo Biology 13 (1): 21-43.
 An Introduction to Neotropical Primates 33

Leo Luna. (1987). Primate conservation in Peru: a case study of the yellow-tailed woolly
monkey. Primate Conservation (8): 122-123.
Leonard S, Bennett C. (1996). Associative behavior of Cacajao calvus ucayalii with other
primate species in Amazonia Peru. Primates 37(2): 227-30.
Levey, D. J., Moermond, T. C., Denslow, J.S., (1994). In McDade, L.A., Bawa, K. S.,
Hespenheide, H. A., Hartshorn, G. S. (Eds.). La Selva: Ecology and Natural History of a
Neotropical Rain Forest. (pp. 282-294). University of Chicago Press, Chicago.
Levi, T. and Peres, C. A. (2013). Dispersal vacuum in the seedling recruitment of a primate-
dispersed Amazonian tree. Biological Conservation 163: 99-106.
Luna, A. G., Sanmiguel, R., Di Fiore, A., and Fernandez-Duque. (2010). Predation and
predation attempts on red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia
aequatorialis) in Amazonian Ecuador. Folio Primtologica 81: 86-95.
Lynch Alfaro, J. W. 2015. Special issue: phylogeny and biogeography of neotropical primates.
Molecular Phylogenetics and Evolution 82: 345-347.
Lynch Alfaro, J. W., Silva Jr., J. D. S., Rylands, A. B., 2012. How different are robust and
gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. American
Journal of Primatology 74 (4), 273-286.
Ma, N. S. F., Elliott, M. W., Morgan, L. M., Miller, A. C., and Jones, T. C. (1976a).
Translocation of Y chromosome to an autosome in the Bolivian owl monkey, Aotus.
American Journal of Physical Anthropology 45, 191-202.
Ma, N. S. F., Jones, T. C., Millar, A. G., Morgan, L. M., and Adams, E. A. (1976b).
Chromosome polymorphism and Bandung patterns in the owl monkey (Aotus). Laboratory
Animal Science, 26: 1022-1036.
Ma, N. S. F., Renquist, D. M., Hall, R., Sehgal, P. K., Simeone, T., and Jones, T. C. (1980).
XX/XO sex determination systems in a population of Peruvian owl monkeys, Aotus.
Journal of Heredity 71: 336-342.
Maldonado, A. M., Nijman, V., and Bearder, S. K. (2009). Trade in night monkeys Aotus spp.
In the Brazil-Colombia-Peru tri-border area: international wildlife trade regulations are
ineffectively enforced. Endangered Species Research 9: 143-149.
Marsh LK. (2014). A taxonomic revision of the Saki monkeys, Pithecia Desmaret, 1804.
Neotropical Primates 21: 1-163.
Mayor, P., Mamani, J. Montes, D. González-Crespo, C., Sebastián, M. A., and Wowler, M.
(2015). Proximate causes of the red face of the bald uakari monkey (Cacajao calvus). Royal
Society Open Science 2: 150145.
Melo, F. R. and Dias, L. G. (2005). Muriqui populations reported in the literature over the last
40 years. Neotropical Primates 13 (suppl.): 19-24.
Melo, F. R., Braz, A. P., Cosenza, D, S., Ferraz, S. L., Souza, F., Nery, M. S., and Rocha, M.
J. R. (2005). The near extinction of a population of northern muriquis (Brachyteles
hypoxanthus) in Minas Gerais, Brazil. Neotropical Primates 13 (1): 10-14.
Melo, F. R., Cosenza, B. A. P., Ferraz, D. S., Souza, S. L. F., Nery, M. S., and Rocha, M. J. R.
(2005) The near extinction of a population of northern muriquis (Brachyteles hypoxanthus)
in Minas Gerais, Brazil. Neotropical Primates, 13:10–14.
Menzoza, S. P. and Mason, W. A. (1986). Parental division of labour and differentiation of
attachments in a monogamous primate (Callicebus moloch). Animal Behavior 34: 1336-
1347.
Mittermeier, R. A. (1982). Introduction. International Zoo Yearbook 22: 1-2.
34 Joseph M. Shostell and Manuel Ruiz-Garcia

Mittermeier, R. A. and Richardson, M. (2013) Primate populations, conservation of.

Encyclopedia of Biodiversity 6: 250-260.
Mittermeier, R. A. and Roosmalen, M. G. M., (1981). Prelimniary observation on habitat
utilization and diet in eight Surinam monkeys. Folia Primatologica, 36: 1-39.
Mittermeier, R. A., Kinzey, W. H. and Mast, R. B. (1989). Neotropical primate conservation.
Journal of Human Evolution 18 (7): 597-610.
Norconk, M. A. and Kinzey, W. G. (1994). Challenge of neotropical frugivory: travel patterns
of spider monkeys and bearded sakis. American Journal of Primatology 34: 171-183.
Nunez-Iturri, G., and Howe, H. F. 2007. Bushmeat and the fate of trees with seeds dispersed
by large primates in a lowland rain forest in Western Amazonia. Biotropica 39, 348-354.
Oliveira, J. M. S., Lima, J. G., Bonvivino, C., Ayres, J. M., and Fleagle, J. G. (1985).
Preliminary notes of the ecology and behavior of the Guianan saki (Pithecia pithecia,
Linnaeus 1766; Cebidae, Primates). Acta Amazonica 15: 249-263.
Paim, F.P. (2005). Relatório Final – Monitoramento Ambiental de Vertebrados Arborícolas nas
Trilhas do Ecoturismo da RDSM. Unpublished manuscript, Instituto de Desenvolvimento
Sustentável Mamirauá.
Peres, C. A. (1988). Primate community structure in western Brazilian Amazonia. Primate
Conservation 9: 83-87.
Peres, C. A. (1990). Effects of hunting on western Amazonian primate communities. Biology
Conservation 54: 47-59.
Peres, C. A. (1996). Use of space, spatial group structure foraging group size of gray woolly
monkeys (Lagothrix lagotricha cana) at Uruca, Brazil. A review of the Atelinae. In
Norconk, M. A., Garber, P. A., and Rosemberger, A. F. (Eds.). Adaptive radiation of
neotropical primates. (pp. 467-488). Plenum Press, New York.
Peres, C. A. and Janson, C. H. (1999). Species coexistence, distribution, and environmental
determinants of neotropical primate richness: A community-level zoogeographic analysis.
In Fleagle, J. G., Janson, C. H. and Reed, K., (Eds.). Primate Communities. (pp. 55-74).
Cambridge University Press, Cambridge.
Peres, C. A., Emilio, T., Schietti, J., Desmoulière, S. J. M., and Levi, T. Dispersal limitation
induces long-term biomass collapse in overhunted Amazonian forests. (2016). Proceedings
of the National Academy of Sciences 113 (4), 892-897.
Perry, S. (2011). Social traditions and social learning in capuchin moneys (Cebus).
Philosophical Transactions of the Royal Society B 366: 988-996.
Ramirez, M. (1989). The woolly monkey, genus Lagothrix. In Mittermeier, R. A., Rylands, A.
B., Coimbra-Filho, A. F., and Fonseca G. A. B. (Eds.). Ecology and Behavior of
Neotropical Primates, Vol 2. (pp. 539-575). Academica Brasiliera de Ciencias, Rio de
Janeiro.
Reid, F. A. (1997). A Field Guide to the Mammals of Central America and Southeast Mexico.
Oxford University Press, New York and Oxford.
Rosenberger, A. L., and Strier, K. B., (1989). Adaptive radiation of the ateline primates.
Journal of Human Evolution 18: 717–750.
Rotundo, M., Fernandez-Duque, E., and Giménez, M. (2002). Cuidado beparental en el mono
de noche (Aotus azarai azarai) de Mormosa, Argentina. Neotropical Primates, 10: 70-72.
Ruiz-Garcia, M. Excobar-Armel, P. Leguizamon, N., Manzor, P., Pinedo-Castro, M., and
Shostell, J. M. (2014). Genetic characterization and structure of the endemic Colombian
 An Introduction to Neotropical Primates 35

silvery brown bare-face tamarin, Saguinus leucopus (Callitrichinae, Cebidae, Primates).

Primates 55 (3): 415-435.
Ruiz-García, M., Luengas, K., Leguizamón, N., Thoisy, B., Gálvez, H. (2015). Molecular
Phylogenetics and Phylogeography of all the Saimiri species (Cebidae, Primates) inferred
from mt COI and COII gene sequences. Primates 56: 145-161.
Ruiz-Garcia, M., Pinedo-Castro, M., and Shostell, J. M. (2014). How many genera and species
of woolly monkeys (Atelidae, platyrrhine, primates) are there? The first molecular analysis
of Lagrothrix flavicauda, an endemic Peruvian primate species. Molecular Phylogenetics
and Evolution 79: 179-198.
Ruiz-García, M., Vásquez, C., Camargo, E., Castellanos-Mora, L.F., Gálvez, H., et al., (2013).
Molecular genetics analysis of mtDNA COII gene sequences shows illegal traffic of night
monkeys (Aotus, Platyrrhini, Primates) in Colombia. Journal of Primatology 2: 107.
doi:10.4172/2167-6801.1000107.
Rylands, A. B. (1996). Habitat and the evolution of social and reproductive behavior in
Callitrichidae. American Journal of Primatology 38: 5-18.
Rylands, A. B. and Mittermeier, R. A. (2009) The diversity of the new world primates
(Platyrrhini): an annotated taxonomy. In Garber, P.A., Estrada, A., Bicca-Marques, J. C.,
Heymann, E. W., and Strier, K. B. (Eds.). South American Primates, Developments in
Primatology: Progress and Prospects. Springer.
Rylands, A. B. Mittermeier, R. A., and Silva Jr., J. S., (2012). Neotropical primates: taxonomy
and recently described species and subspecies. International Zoo Yearbook 46: 11-24.
Santos, R. (2002). Ecologia e comportamento de cuxiús (Chiropotes satanas) na Amazônia
Oriental: Perspectivas para a consevaçã de poplações fragementadas [Master’s thesis].
Belém: Museo Paraense Emílio Goéldi e Universidade Federal do Pará.
Schneider, H., and Sampaio, I. (2015). The systematics and evolution of New World primates
– A review. Molecular Phylogenetics and Evolution 82: 348–357.
Schneider, H., Bernardi, J.A.R., Da Cunha, D.B., Tagliaro, C.H., Vallinoto, M., Ferrari, S.F.
and Sampaio, I. (2012). A molecular analysis of the evolutionary relationships in the
Callitrichinae, with emphasis on the position of the dwarf marmoset. Zoologica Scripta 41:
1–10.
Silva Jr., J. de S. (2001). Especiação nos macacos-prego e caiararas, gênero Cebus Erxleben,
1777 (Primates, Cebidae). Doctoral Thesis, Universidade Federal do Rio de Janeiro.
Silva Jr., J. de S. (2002). Sistemática dos macacos –prego e caiararas, gênero Cebus Erxleben,
1777 (Primates, Cebidae). Livro de Resumos, X Congresso Brasieliero de Primatologia:
Amazônia – A Última Fronteira: 35. Bélém, Brazil.
Smith, R. J. and Jungers, W. L. (1997). Body mass in comparative primatology. Journal of
Human Evolution 32: 523-559.
Solano P. (1995). Patrón de actividad y área de acción del mico nocturno Aotus brumbacki
Hershkovitz, 1983 (Primates: Cebidae) Parque Nacional Natural Tinigua Meta, Colombia.
Doctoral dissertation. Pontificia Universidad Javeriana, Bogotá.
Spirig R, Peduzzi E, Patarroyo ME, Pluschke G, and Daubenberger CA. (2005). Structural and
functional characterization of the Toll like receptor 9 of Aotus nancymaae, a non-human
primate model for malaria vaccine development. Immunogenetics 57: 283–288.
Spironello, W. R. (2001). The brown capuchin monkey (Cebus apella): ecology and home
range requirements in Central America. In: Bierregaard, R. O. Jr., Gascon, C., Lovejoy, T.
36 Joseph M. Shostell and Manuel Ruiz-Garcia

E., Mesquita, R. (Eds.) Lessons from Amazonia: the Ecology and Conservation of a
Fragmented Forest. Yale University Press, New Haven, Connecticut, USA, pp 271-283.
Stoner, K. E. (1994). Population density of the mantled howler monkey (Alouatta palliate) at
La Selva Biological Reserve, Costa Rica: a new technique to analyze census data.
Biotropica 26 (3): 332-340.
Strier, K. B. (1992). Faces in the Forest: the Endangered Murique Monkeys of Brazil. Oxford
University Press.
Strier, K. B. (2000). Population viabilities and conservation implications for muriquis
(Brachyteles arachnoides) in Brazil’s Atlantic Forest. Biotropica 32 (4b): 903-913.
Strier, K. B. and Fonseca, G. A. B. (1996/1997). The endangered muriqui in Brazil’s Atlantic
Forest. Primate Conservation 17: 131-137.
Strier, K. B., Boubli, J. P., Possamai, C. B., and Mendes, S. L. (2006). Population demography
of northern muriquis (Brachyteles hypoxanthus) at the Esacao Biologica de Caratinga
Reserva Particular do Patrimonio Natural Feliciano Miguela Abdala, Minas Gerais, Brazil.
American Journal of Physical Anthroplogy 130: 227-237.
Struhsaker, T. T., and Leakey, M. (1990). Prey selectivity by crowned hawk-eagles on monkeys
in the kibale forest, Uganda. Behavioral Ecology and Sociobiology 26: 435-443.
Talebi, M. and Soares, P. (2005). Conservation research on the southern murique (Brachyteles
arachnoides) in Sāo Paulo state, Brazil. Neotropical primates, 13 (suppl.): 53-59.
Terborgh, J. W., and Janson, C. H. (1983). Ecology of primates in southeastern Peru, National
Geographic Research Reports 15: 655-662.
Van Roosmalen, M. G. M. (1980). Habitat Preferences, Diet, Feeding Strategy and Social
Organization of the Black Spider Monkey (Ateles paniscus Linnaeus 1758) in Suriname.
Doctoral thesis. Universities of Wageningen and Amsterdam.
Van Roosmalen, M. G. M., Mittermeier, R. A., and Milton, K. (1981). The bearded sakis, genus
Chiropotes. In Coimbra-Filho, A. F. and Mittermeier, R. A. (Eds.). Ecology and Behavior
of Neotropical Primates. (pp. 419-441). Rio de Janeiro, Brazil: Academia Brasileira de
Ciências.
Van Roosmalen, M. G. M., Van Roosmalen, T. and Mittermeier, R. A. (2002). A taxonomic
review of the titi monkeys, genus Callicebus Thomas, 1903, with the description of two
new species, Callicebus bernhardi and Callicebus stephennashi, from Brazilian Amazonia.
Neo-tropical Primates 10(suppl.): 1–52.
Vié, J., Richard-Hansen, C., and Fournier-Chambrillon, C. (2001). Abundance, use of space,
and activity patterns of white-faced sakis (Pithecia pithecia) in French Guiana. American
Journal of Primatology 55: 203-221.
Wallace, R. B., Gomez, H., Felton, A. and Felton, A. M. (2006). On a new species of titi
Monkey, genus Callicebus Thomas (Primates, Pitheciidae), from western Bolivia with
preliminary notes on distribution and abundance. Primate Conservation (20): 29–39.
Wehncke, E. V. and Domínguez, C. A. (2007). Seed dispersal ecology of non-restricted
frugivores, capuchin monkeys in three Neotropical forests. Journal of Tropical Ecology
23: 519-528.
Wehncke, E. V., Valdez, C. N., and Dominguez, C. A. (2004). Seed dispersal and defecation
patterns of Cebus capucinus and Alouatta palliata: consequences for seed dispersal
effectiveness. Journal of Tropical Ecology 20: 535-543.
An Introduction to Neotropical Primates 37