Overview

Brief Summary

Biology

The cotton-headed top tamarin is diurnal and arboreal, feeding on fruit, insects, tender vegetation, small vertebrates and bird eggs (6) (10). With the exception of smaller prey, animals are killed with a bite to the head (3). Cotton-headed tamarins obtain the water they need by licking leaves that are wet with rain or dew, rather than expose themselves to predation by venturing down onto the forest floor (5). When not feeding, much time is spent in social grooming. Like other tamarins, they run their clawed digits through each other's fur, examining it, and use their teeth, lips and tongue to pick off particles (8). These social monkeys live in groups of 3 – 13 individuals, with the average being around 7 (2). Their home ranges extend from 7-10 hectares and often overlap with those of other groups, with contact between groups being agonistic (5). These tamarins are territorial, scent marking their home ranges and defending them with showy confrontations, fluffing up their fur and making loud calls to scare away intruders and attract individuals from their own group (6). There can be more than one adult male and female in the group but only one female actually breeds (3) (5). Reproduction in other females is suppressed by the behavioural domination of the reproductive female, and by the effects of her pheromones and genital gland scent (6). Males and other group members play a major role in caring for the young (8). The co-operative breeding system of tamarins appears to be unique amongst primates, and serves to help the breeding female care for the offspring (7). Lactation and feeding the young demands a great deal of energy, and so males and other group members often carry the young, allowing the female more time to forage and feed, while other members of the group also help by surrendering food morsels to the young and the breeding female (7). This explains why the female is usually larger in size than the male. In fact, research suggests that smaller males are often preferred mating partners by the females as they are more nimble in the forest and therefore better food gatherers (6). Like other tamarins, the cotton-headed tamarin usually gives birth to twins (8) (9). The gestation period is around 140 days (2), and the offspring, born helpless (3), are carried everywhere rather than being left in nests (9). The co-operative care of the group is key to the infant's development, for they become independent after only two months. This unique breeding system is also essential as it enables tamarins to maintain a high reproductive rate (6). Once established as breeders in a group, a female can produce twins once a year, and sometimes twice (9).
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Description

The stunning cotton-headed tamarin is one of South America's most endangered primates (5). Its name describes the fantastic crest of long white hair flowing around the black face like a mane of white cotton (6). Its body is small and covered with thick fur, with a brown back and shoulders, and white to yellow chest and limbs (6). The fore and hind limbs are similar in size, allowing it to move quadrupedally through the forest, running along branches or jumping short distances between tree braches (7) (8). Like marmosets and other tamarins, the ancestral primate nails on their toes and fingers have evolved into claws on all but their big toes, allowing them to climb in a squirrel-like fashion in the trees (6) (9). This small monkey has a long tail, which assists in balance; it is reddish orange towards the base and black towards the tip (5). Males and females look the same in appearance, as do the young (7).
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Distribution

Range Description

Saguinus oedipus occurs in north-western Colombia between the Río Atrato and the lower Río Cauca (west of the Río Cauca and the Isla de Mompos) and Magdalena, in the Departments of Atlantico, Sucre, Cordoba, and western Bolivar, north-western Antiquoia (from the Uraba region, west of the Río Cauca) and north-eastern Choco, east of the Río Atrato, from sea level up to 1,500 m (Hernández-Camacho and Cooper 1976; Hershkovitz 1977; Hernández-Camacho and Defler 1989; Mast et al. 1993 ).

The south-western boundary of the cotton-top's range has not been clearly identified. Mast et al. (1983) suggested that it may extend to Villa Arteaga on the Río Sucio (Hershkovitz 1977), which included reports of Cotton-top Tamarins in Los Katios National Park. However, Barbosa et al. (1988) were unable to find any evidence of Cotton-top Tamarins in this area nor in Los Katios, where they observed only Saguinus geoffroyi.

Groups have been seen in the Islas del Rosario and Tayrona National Park in the Sierra Nevada de Santa Marta (Mast et al. 1993; A. Savage and L. H. Giraldo, pers. obs.). However, these populations were founded by captive animals that were released into the area (Mast et al. 1993) and these remnant populations are here considered as outside of the historic range of the species.
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Geographic Range

Northwest Colombia

Biogeographic Regions: neotropical (Native )

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Historic Range:
Costa Rica to Colombia

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Range

Confined to Colombia, but formerly much more widespread across the country (2).
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Physical Description

Morphology

Physical Description

Cotton-top tamarins are distinguished from other members of the genus Saguinus by possessing a crest of long whitish hair from the forehead to the nape flowing over the shoulders. Their back is brown and the underparts of the arms and legs are whitish to yellow. The rump and inner sides of thighs are reddish-orange. The base of the tail is also reddish-orange, while the tip is blackish.

Characteristics that distinguish callitrichids from other new world monkeys are modified claws instead of nails on all digits and the presence of two rather than three molars on each side of the jaw.

Range mass: 260 to 380 g.

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Ecology

Habitat

Habitat and Ecology

Habitat and Ecology
This species occurs in humid forest in the south to dry deciduous forest in the north; recorded from primary and secondary forests. Known at altitudes up to 400 m, but could occur in higher elevations in the upper valley of the Río Sinu (Defler 2004).

Marmosets and tamarins are distinguished from the other monkeys of the New World by their small size, modified claws rather than nails on all digits except the big toe, the presence of two as opposed to three molar teeth in either side of each jaw, and by the occurrence of twin births. They eat fruits, flowers, nectar, plant exudates (gums, saps, latex) and animal prey (including frogs, snails, lizards, spiders and insects). Marmosets have morphological and behavioural adaptations for gouging trees trunks, branches and vines of certain species to stimulate the flow of gum, which they eat, and in some species form a notable component of the diet. The dentition of the tamarins (Saguinus and Leontopithecus) does not provide for gouging and they eat gums only when readily available.

Tamarins live in extended family groups of between four and 15 individuals, but usually 2-8. Saguinus oedipus lives in groups of 2-9. Savage et al. (1996a,b) observed reproductively active groups that ranged in size from 3-6. Generally, only one female per group breeds during a particular breeding season. Lives in groups of 2-9 individuals.

Size:
Tamarins are monomorphic - exhibiting only minor differences in body and canine size.
Adults H&B 20.8-25.9 cm, TL 33.0-41.0 cm (Hershkovitz 1977)
Weight 416.5 g (n = 10) (Savage 1990).

Systems
  • Terrestrial
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Cotton-top tamarins inhabit tropical rainforests, open woodlands, and secondary growth. They are sensitive to any alteration in their habitat.

Terrestrial Biomes: forest ; rainforest ; scrub forest

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This species is found in tropical rainforest edges and secondary forests. It has been found in a variety of habitats from wetland tropical forest, to moist woodland forest and dry thorn forest savannah (5).
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Trophic Strategy

Food Habits

Cotton-top tamarins are primarily insectivorous; insects being 40% of their diet. They also eat a large amount of fruit which consists of 38.4% of their diet. Feeding on exudates, which is known as gum feeding, takes up 14.4% of their diet. Saguinus oedipus have an interesting characteristic which consists of food associated calls that are correlated with food preferences. Certain calls made by cotton-top tamarins were strictly associated with a feeding context and were not used in non-feeding contexts. However, it should be noted that there is a 3% error, when these specific calls are made in non-feeding contexts.

Animal Foods: insects

Plant Foods: fruit; sap or other plant fluids

Primary Diet: omnivore

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Life History and Behavior

Life Expectancy

Lifespan/Longevity

Average lifespan

Sex: male

Status: captivity:
23.1 years.

Average lifespan

Status: captivity:
23.0 years.

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Lifespan, longevity, and ageing

Maximum longevity: 26.2 years (captivity) Observations: One 26.2 year old animal was still alive in captivity (Richard Weigl 2005). Amyloid-beta protein plaque deposits typical of Alzheimer's disease, but not neurofibrillary tangles, were observed in the brains of animals over 12 years of age, suggesting these animals may develop early Alzheimer's disease pathology (Lemere et al. 2008).
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Reproduction

Saguinus oedipus has a monogamous breeding system. This species has a form of cooperative breeding, which isn't present in many other Primates. It consists of adult 'helpers' staying in the family and gaining breeding experience instead of breeding themselves. This may result in the highest reproductive potential of all primates.

Mating System: monogamous ; cooperative breeder

Cotton-top tamarins are reproductively active seasonally with females being seen pregnant or suckling young only from January to June. They have an estrous cycle of 15 days and gestation lasts approximately 140 days. Sexual maturity is reached at 18 months in females and 24 months in males. Saguinus oedipus gives birth to non-identical twins twice each year.

Breeding interval: Saguinus oedipus breeds twice each year

Average number of offspring: 2.

Average gestation period: 140 days.

Average age at sexual or reproductive maturity (female): 18 months.

Average age at sexual or reproductive maturity (male): 24 months.

Key Reproductive Features: iteroparous ; seasonal breeding ; gonochoric/gonochoristic/dioecious (sexes separate); viviparous

Average birth mass: 39.36 g.

Average gestation period: 178 days.

Average number of offspring: 1.9.

Average age at sexual or reproductive maturity (male)

Sex: male:
550 days.

Average age at sexual or reproductive maturity (female)

Sex: female:
548 days.

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Molecular Biology and Genetics

Molecular Biology

Barcode data: Saguinus oedipus

The following is a representative barcode sequence, the centroid of all available sequences for this species.


There is 1 barcode sequence available from BOLD and GenBank.

Below is the sequence of the barcode region Cytochrome oxidase subunit 1 (COI or COX1) from a member of the species.

See the BOLD taxonomy browser for more complete information about this specimen.

Other sequences that do not yet meet barcode criteria may also be available.

AATCGCTGATTATTTTCAACCAACCACAAAGACATCGGAACATTATACCTACTATTTGGCGCATGAGCGGGAGCTGTGGGAACAGCCCTA---AGTTTCCTTATCCGAGCAGAACTAGGCCAACCTGGGAGCTTGTTTGAGGAT---GATCATGTCTATAATGTTATCGTTACATCCCACGCATTTATTATAATTTTCTTCATAGTTATACCCATTATAATCGGGGGTTTTGGCAACTGACTAATCCCCCTAATA---ATTGGCGCCCCAGACATAGCATTCCCTCGAATAAATAATATAAGCTTCTGACTTCTACCCCCATCACTCCTCCTTCTACTTGCATCCTCAACCTTAGAGGCCGGCGCTGGAACTGGCTGAACAGTATACCCACCCCTAGCAGGAAACATATCACATCCAGGCGCCTCTGTAGACCTA---GTTATTTTCTCACTGCACCTGGCAGGTGTGTCTTCCATCTTAGGGGCTATCAACTTCATCACCACAATCATTAACATAAAACCCCCTGCCATAACCCAGTACCAAACCCCCTTATTCGTATGATCCGTTTTAATCACAGCAGTTCTTCTTCTACTCTCCCTGCCTGTCTTAGCTGCC---GGAATTACTATACTACTAACTGACCGAAATCTTAACACTACTTTCTTCGACCCTGCAGGCGGCGGTGATCCTATCCTGTACCAACACCTATTCTGATTCTTTGGTCATCCCGAAGTATATATTCTTATCCTACCAGGGTTCGGAATAATTTCACACATTGTAACATACTACTCTAATAAAAAA---GAGCCGTTTGGATACATAGGCATAGTTTGAGCTATAATATCTATCGGATTTTTAGGGTTTATCGTATGAGCTCATCACATATTTACAGTCGGAATGGATGTCGACACCCGCGCATACTTCACATCAGCCACTATAATCATCGCTATTCCTACTGGGGTGAAAGTATTTAGTTGACTA---GCCACCCTACACGGCGGC---AATATCAAATGATCCCCCGCAATACTATGGGCCCTAGGCTTCATCTTCCTCTTTACCGTAGGAGGGCTGACAGGAATCGTATTAGCTAACTCATCACTGGATATTGTACTACATGATACATACTATGTAGTAGCCCACTTCCACTATGTT---CTATCTATGGGGGCAGTATTTGCCATCATAGGGGGATTTATCCACTGATTCCCACTATTCTCAGGTTACACACTTGACCAAACCTATGCTAAAATTCACTTCACTATTATATTTGTAGGCGTAAACCTAACCTTTTTCCCACAACACTTCCTCGGATTATCAGGAATACCCCGA---CGATATTCAGACTACCCTGACGCCTATACT---ACATGAAATATCATCTCATCTGTAGGCTCATTAATCTCACTGACAGCAGTGATACTAATAATTTTTATAATCTGAGAAGCATTCTCTTCTAAGCGCAAAGTT---TCAACCATTGAACAACTATCAACTAAC
-- end --

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Statistics of barcoding coverage: Saguinus oedipus

Barcode of Life Data Systems (BOLDS) Stats
Public Records: 1
Specimens with Barcodes: 1
Species With Barcodes: 1
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Conservation

Conservation Status

IUCN Red List Assessment


Red List Category
CR
Critically Endangered

Red List Criteria
A2cd

Version
3.1

Year Assessed
2008

Assessor/s
Savage, A. & Causado, J.

Reviewer/s
Mittermeier, R.A. & Rylands, A.B. (Primate Red List Authority)

Contributor/s

Justification
This species is listed as Critically Endangered due to a severe reduction in population, estimated to be greater than 80% over the past 3 generations (18 years) due to destruction of habitat.

History
  • 2000
    Endangered
  • 1996
    Endangered
  • 1994
    Endangered
    (Groombridge 1994)
  • 1990
    Endangered
    (IUCN 1990)
  • 1988
    Endangered
    (IUCN Conservation Monitoring Centre 1988)
  • 1986
    Endangered
    (IUCN Conservation Monitoring Centre 1986)
  • 1982
    Endangered
    (Thornback and Jenkins 1982)
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Current Listing Status Summary

Status: Endangered
Date Listed: 10/19/1976
Lead Region: Foreign (Region 10) 
Where Listed: Entire


Population detail:

Population location: Entire
Listing status: E

For most current information and documents related to the conservation status and management of Saguinus oedipus , see its USFWS Species Profile

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The main problems contributing to the cotton-top tamarin's status as endangered is the clearing of their forest habitat and population depletion from animal trade. Nature reserves have been set up to help maintain populations of Saguinus oedipus.

US Federal List: no special status

CITES: appendix ii

IUCN Red List of Threatened Species: critically endangered

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Status

Classified as Endangered (EN B1 + 2abcde, C2a) on the IUCN Red List 2002 (1), listed as endangered by the USDI (3) and listed on Appendix 1 of CITES (4).
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Population

Population
In the late 1960s and early 1970s, 20,000-30,000 individuals were exported to the United States for biomedical research (Hernández-Camacho and Cooper 1976). Current population estimates for the species are 6,000 individuals (approximately 2,000 mature individuals).

Population Trend
Decreasing
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Threats

Major Threats
Saguinus oedipus occurs in an area of intensive colonization and forest loss. Neyman (1978) estimated that 75% of the original distribution of S. oedipus had been cleared for agriculture and pasture, and that the remainder of its range was represented by small isolated forest patches along with its main stronghold, the Paramillo National Natural Park of 460,000 ha. Cerquera (1985) reported on the threats regarding the construction of two hydroelectric dams, Urra I and Urra II, on the Ríos Sinu and San Jorge, in the south of its range. Urra II is sited within the Paramillo National Natural Park and is expected to flood more than 54,000 ha of primary and secondary forest, within what is considered to be the last major stronghold for the species.

The three protected areas where they occur have lost a significant portion of their forests (Barbosa et al. 1988). Paramillo has lost approximately 42% of its original forested habitat and Montes de Maria and Los Colorados lost 70 and 71%, respectively. To date, almost 200,000 ha of the original forested areas within protected boundaries of the parks and reserves dedicated to Cotton-top Tamarin conservation efforts have been lost. This suggests, therefore, that there is less than 2,600 km² that will be protected in perpetuity for Cotton-top Tamarins by the Colombian Ministerio del Medio Ambiente. Although these areas are protected, they continue to suffer from the pressure of the growing local populations to extract resources or clear areas for agricultural activities.

Defler (1994, 2004; pp.196-201) discusses the conservation status and threats to this species (see also Defler and Rodríguez-Mahecha 2003; Defler et al. 2003).
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Deforestation is this species' greatest threat (6). It has already lost most of its habitat through forest clearing for timber, charcoal, human settlement, agricultural land and industry (3). The forest areas in which it now exists are so fragmented, it is believed that they are too small to maintain the tamarin populations (3). Sadly the continuous expansion of human settlement in northern Colombia has brought the cotton-headed top tamarin more bad luck. With easier access to the tamarin's habitat, animal collectors trap these small monkeys and sell them in port cities, either for export or local trade (10). Populations in the past have also suffered from the export of significant numbers for biomedical research in the 1960s and 1970s (5) (9).
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Management

Conservation Actions

Conservation Actions
Legally protected in Colombia since 1969. Major threat in the past was export for the pet trade, zoos and biomedical research, but export was banned in 1974. Listed on CITES Appendix I.

There are three protected areas where Saguinus oedpipus occurs: Paramillo National Natural Park (460,000 ha), decreed in 1977; Los Colorados Fauna and Flora Sanctuary (1,000 ha) decreed in 1977; and Reserva Forestal Cerro de Coraza-Monte de Marja (7,460 ha) decreed in 1983. They were also introduced to Tayrona National Natural Park in 1974 (Defler 1994).

Proyecto Tití, a conservation programme for the Cotton-top Tamarin in Colombia, was established in 1987 to begin the first long-term field study on this species in collaboration with Colombian biologists, educators, NGO?s and government authorities (INDERENA, Ministerio del Medio Ambiente) (Savage 1988, 1993, 1995, 1996, 1997; Savage et al. 1996a,b, 1997, 2001a,b). Initial research focused on understanding the factors influencing reproductive strategies of Cotton-top Tamarins, but it quickly grew into a comprehensive conservation programme including educational efforts, capacity building, training Colombian students, development of economic alternatives, and the development of an agricultural training programme to decrease the pressure on the forest by local communities (Savage and Giraldo 1990; Savage et al. 1990, 1996, 1997).

In addition to the studies of Cotton-top Tamarins in the field, there has been a major and comprehensive assessment of the remaining habitat within the historic distribution of the Cotton-top Tamarin in Colombia, along with surveys to assess population numbers remaining. This information has provided important insights into the long-term viability of this population given the current rate of habitat destruction.
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Conservation

The cotton-headed tamarin has been listed as endangered since 1970 by the International Union for Conservation of Nature and Natural Resources (IUCN) (1). It is also recognised as endangered on the USDI (3), and its listing under Appendix I of the Convention for International Trade of Endangered Species (CITES) means that international trade of this species is prohibited (3). However, its numbers have continued to dwindle away, as has its habitat and hope of survival. If this species is to survive, it is essential that immediate conservation measures are implemented (3) (8).
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Relevance to Humans and Ecosystems

Benefits

Economic Importance for Humans: Negative

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Economic Importance for Humans: Positive

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Wikipedia

Cotton-top tamarin

The cotton-top tamarin (Saguinus oedipus) is a small New World monkey weighing less than 0.5 kg (1.1 lb). One of the smallest primates, the cotton-top tamarin is easily recognized by the long white sagittal crest extending from its forehead to its shoulders. The species is found in tropical forest edges and secondary forests in northwestern Colombia where it is arboreal and diurnal. Its diet includes insects and plant exudates and it is an important seed disperser in the tropical ecosystem.

The cotton-top tamarin displays a wide variety of social behaviors. In particular, groups form a clear dominance hierarchy where only dominant pairs breed. The female normally gives birth to twins and uses pheromones to prevent other females in the group from breeding. These tamarins have been extensively studied for their high level of cooperative care, as well as altruistic and spiteful behaviors. Communication between cotton-top tamarins is sophisticated and shows evidence of grammatical structure, a language feature that must be acquired.

It is thought that up to 40,000 cotton-top tamarins were caught and exported for use in biomedical research before 1976 when CITES gave them the highest level of protection and all international trade was banned. Now the species is at risk due to large-scale habitat destruction, as the lowland forest in northwestern Colombia where the cotton-top tamarin is found has been reduced to five percent of its previous area. It is currently classified as critically endangered and is one of the rarest primates in the world with only 6,000 individuals left in the wild.

Taxonomy and naming[edit]

Saguinus oedipus goes by the common names "cotton-top tamarin" and "cotton-headed tamarin" in English. Its name comes from the white hair that spans its head flowing down past the neck.[3] In Spanish, Saguinus oedipus is commonly called "bichichi", "tití pielroja", "tití blanco", "tití cabeza blanca", or "tití leoncito".[2][4] In German-speaking areas, the cotton-top tamarin is commonly known as "Lisztaffe" (literally "Liszt monkey") most likely due to the resemblance of its hairstyle with that of Hungarian composer and piano virtuoso Franz Liszt.[5]

The species was first described by Linnaeus in 1758[2] as Simia oedipus.[6] Linnaeus chose the species name oedipus, which means swollen foot, but as the species does not have particularly large feet, it is unknown why he chose this name. (Linnaeus often selected names from mythology without any particular rationale, and he may have used the name of Oedipus, the mythical Greek king of Thebes, more or less arbitrarily.)[7] In 1977, Philip Hershkovitz performed a taxonomic analysis of the species based on fur coloration patterns, cranial and mandibular morphology, and ear size. He classified Geoffroy's tamarin Saguinus geoffroyi as a subspecies of Saguinus oedipus.[8] Subsequent analyses by Hernández-Camacho and Cooper (1976),[9] Mittermeier and Coimbra-Filho (1981),[8] and later Grooves (2001)[10] consider the oedipus and geoffroyi types to be separate species.

Some researchers, such as Thorington (1976),[8] posit that S. oedipus is more closely related to the white-footed tamarin (S. leucopus) than to S. geoffroyi. This view is supported by Hanihara and Natoria's analysis of toothcomb dental morphology (1987) and by Skinner (1991), who found similarities between S. oedipus and S. leucopus in 16 out of 17 morphological traits considered.[8]

This species of white-headed tamarin is thought to have diverged from the other Amazonian forms such as S. leucopus. This is supported by morphological considerations of the transition from juvenile to adulthood, during which the fur coloration patterns change significantly and are similar between the two species.[11] Hershkovitz proposed that the separation of the two species happened in the Pleistocene at the height of the Atrato River, where it intersected the Cauca-Magdalena. At that time, the area was covered by a sea, which created a geographic barrier that caused the species to diverge through the process of allopatric speciation. Today, the two species are principally separated by the Atrato River.[11]

Physical characteristics[edit]

The cotton-top tamarin is part of the most diminutive family of monkeys, Callitrichidae, the marmosets and tamarins; it weighs 432 g (15.2 oz) on average. Its head–body length is 20.8–25.9 cm (8.2–10.2 in) while its tail—which is not prehensile—is slightly longer at around 33–41 cm (13–16 in).[11] The species is not sexually dimorphic, the male and female are of a similar size and weight.[4] Members of the Callitrichinae subfamily (including this species) have sharp nails (tegulae) on all digits except the big toes, which have the flat nails (ungulae) common to other primates. Tegulae resemble a squirrel's claws and help with movement through trees.[4][2]

The white hair on the back of the head and neck inspire its common name, "cotton-top".

The cotton-top tamarin has a long sagittal crest, consisting of white hairs, from forehead to nape flowing over the shoulders. The skin of the face is black with gray or white bands located above the eyes. These bands continue along the edge of the face down to the jaw.[12] Tamarins are generally divided into three groups by their facial characteristics: hairy-face, mottled-face, and bare-face. The cotton-top tamarin has fine white hairs covering its face, but they are so fine it appears naked, thus is considered a bare-face tamarin. Its lower canine teeth are longer than its incisors, creating the appearance of tusks.[13] Like other callitrichids, the cotton-top tamarin has two molar teeth on each side of its jaw, not three like other New World monkeys.[2]

The cotton-top tamarin has fur covering all of the body except the palms of the hands and feet, the eyelids, the borders of the nostrils, the nipples, the anus, and the penis. The back is brown, and the underparts, arms and legs are whitish-yellow. The rump and inner thighs and upper tail are reddish-orange. The fur is distributed with varying densities throughout the body: the genital region (scrotum and pubic zone), axilla, and the base of the tail have lower densities, while the forward region is much higher. Many individuals have stripes or whorls of fur of striking coloration on their throat. The cotton-top also has whiskers on its forehead and around its mouth.[11]

Habitat and distribution[edit]

A sign in Tayrona National Natural Park in northern Colombia pointing out the tamarin's endangered status in the only part of the world where it still exists.

The cotton-top tamarin is restricted to a small area of northwest Colombia, between the Cauca and Magdalena Rivers to the South and East, the Atlantic coast to the North, and the Atrato River to the West. Historically, the entirety of this area was suitable for the cotton-top tamarin, but due to habitat loss through deforestation, it survives in fragmented parks and reserves. One of the most important areas for the cotton-top is the Paramillo National Park, which consists of 460,000 hectares (1,800 sq mi) of primary and secondary forest.[2]

The cotton-top tamarin is found in both primary and secondary forests, from humid tropical forests in the south of its range to tropical dry forests in the north. It is seldom found at altitudes above 400 metres (1,300 ft), but has been encountered up to 1,500 metres (4,900 ft).[2][9] It prefers the lower levels of the tropical forests but may also be found foraging on the ground and anywhere between the understory and the canopy. It can adapt to forest fragments and can survive in relatively disturbed habitats. In the dry forests there are pronounced seasons. Between December and April it is dry, while heavy rainfall occurs between August and November which can flood the forest floor. Across its range annual rainfall varies between 500 and 1,300 mm (20 and 51 in).[4]

Ecology[edit]

The cotton-top tamarin has a diet of mainly fruit (40%) and animal material (40%).[14] This includes insects, plant exudates such as gum and sap, nectar, and occasionally reptiles and amphibians. Due to its small body size and high food passage rate its diet must be high-quality and high-energy. Insectivory is common in the cotton-top and the species will hunt for insects using a variety of methods: stealth, pouncing, chasing, exploring holes, and turning over leaves.[13]

Tamarins act as seed dispersers in tropical ecosystems. While larger primates eat larger seeds, tamarins eat the smaller ones. The expelled seeds have a higher germination rate than others and it is postulated that when larger seeds are ingested it may help to dislodge and expel intestinal parasites.[4]

The cotton-top tamarin is diurnal and sleeps with its social group in trees with foliage cover. The group leaves the sleeping tree together an hour after dawn and spends the day foraging, resting, travelling, and grooming.[4][15] It is thought the species rises late and increases the speed of its foraging and travelling before dusk to avoid crepuscular and nocturnal predators. Its main predators include raptors, mustelids, felids, and snakes.[16][17] The cotton-top tamarin is extremely vigilant, always looking for potential predators. When the group is resting, one individual will move apart and act as a lookout to alert the group if it sees a threat.[4]

The cotton-top tamarin can live as long as 24 years in captivity, while its life span in the wild averages 13 years.[4]

Behavior[edit]

Two cotton-top tamarins feed at Ueno Zoo, in Japan. (video)

Social systems[edit]

The cotton-top tamarin is a highly social primate that typically lives in groups of two to nine individuals, but may reach up to thirteen members.[2][15][18] These small familial groups tend to fluctuate in size and in composition of individuals and a clear dominance hierarchy is always present within a party. At the head of the group is the breeding pair. The male and female in this pair are typically in a monogamous reproductive relationship, and together serve as the group's dominant leaders.[18]

Dominant pairs are the only breeding pair within their groups, and the female will generally have authority over the breeding male. While non-breeding group members can be the leading pair's offspring, immigrant adults may also live with and cooperate in these groups. This social grouping in cotton-top tamarins is hypothesized to arise from predation pressure.[19] Cotton-top tamarins exhibit prosocial behavior that benefits other members of the group,[20] and are well known for engaging in cooperative breeding whereby the group's subordinate adults help in rearing the offspring of the dominant pair. The dominant female is more likely to give birth to non-identical twins than a singleton so it would be too energetically expensive for just one pair to raise the young.[21]

To prevent younger, subordinate females within the group from breeding, the dominant female uses pheromones. This suppresses sexual behavior and delays puberty.[22][23] Unrelated males that join the group can release the females from this reproductive suppression; this may result in more than one female of the group becoming pregnant, however only one of the pregnancies will be successful.[24]

Cooperation[edit]

A male grooming a female as part of the species' cooperative ritual.

In cooperative breeding, the effort put into caring for the dominant breeder's offspring is shared by the group members. Parents, siblings, and immigrant adults will share child rearing duties for the breeding pair's young. These duties include carrying, protecting, feeding, comforting, and even engaging in play behavior with the group's young. Cotton-top tamarins display high levels of parental investment during infant care. Males, particularly those that are paternal, show a greater involvement in caregiving than do females.[25] Despite this, both male and female infants prefer contact and proximity to their mothers over their fathers.[25] It has been hypothesized that males invest additional support in rearing offspring as a form of courtship to win favor of the group's dominant female. However, evidence indicates that time spent carrying infants does not correlate with a male's overall copulation frequency.[26]

Since only one female in a group breeds, heavy investment in infant care ensures that all offspring survive until independence. Accordingly, cotton-top tamarins bear excessive costs in order to care for the group's young.[26][27] Male carriers, especially paternal carriers, incur large energetic costs for the sake of the group's young. This burden may cause some male cotton-tops to lose up to 10-11% of their total body weight.[28] The large weight loss may occur from reduced food intake as infant carrying inhibits foraging ability for a carrier. The trend of male-carrier weight loss and decreased food intake is in contrast to the dominant female's periovulatory period, when she gains weight after increasing her own food intake and relinquishing much of her infant carrying duties.[27]

Altruism[edit]

While caregiving by males appears to be altruistic, particularly in father cotton-tops, the costs of infant care may in fact be tolerated for selfish reasons. Namely, the costs to male weight and foraging ability may in turn promote consecutive pregnancies in dominant females, thereby providing more offspring bearing the father's genes.[27] Additionally, the cooperative breeding structure of cotton-tops can change with group size and parental experience. First-time fathers spend a greater amount of time carrying the infant than experienced fathers, and in smaller groups fathers do a greater proportion of carrying and feeding the infant than in larger groups where helpers take on more of the work. Total care for infants remains constant with varying group size, and infant outcome is not significantly different in groups that have differing levels of experience in raising offspring.[29]

Once infants reach sufficient age, they permanently leave the backs of their carriers and begin contributing to the group.

The cooperative breeding hypothesis predicts that cotton-top tamarins engage with this child rearing paradigm, and in turn naturally embrace patterns of prosocial behavior.[20] These monkeys engage in such behavior by acting altruistically within their groups in caring for infants, vocalizing alarm calls, and in sharing food. Though some studies indicate that cotton-top tamarins have the psychological capacity to participate in reciprocally mediated altruism,[30] it is unclear whether the cotton-top tamarin acts solely using judgements on reinforcement history.[31]

Other studies involving cotton-top tamarins have hinted that positive reciprocity and reciprocal altruism are irrelevant in the prosociality of these primates.[20] Some researchers believe these primates tend to cooperate for selfish reasons and in situations where they incur some benefit for themselves. That is, cooperation in cotton-top tamarins can be better described by mutualism than by true altruism.[31]

Tamarins in captivity have shown the ability to distinguish other individuals based on cooperative tendencies and past behavior. Cotton-tops ultimately use this information to guide future cooperation. Brief periods of defection tend to cause swift, irreparable breakups between these primates and their cooperators. To avoid this, it is thought that cotton-top tamarins will make economically-driven decisions based on the projected incentives of a potential cooperator.[31]

Spite and aggression[edit]

Despite an expansive array of altruistic behaviors, cotton-top tamarins will engage in great bouts of spite through negative reciprocity and punishment. Cotton-top tamarins have been observed to immediately start denying cooperation with monkeys who deny them benefits.[31] Further, in captivity these primates are not observed to increase altruistic behavior with fellow primates who are committed fully to cooperation. Based on this, researchers believe that repeated interactions in a cooperative society like that of the cotton-top tamarin can heighten the chances that an individual will designate behavioral punishments to others in its group.[32] This reaction has also been observed in other species.[33] However, these reciprocal punishments, or relative lack of altruistic actions, may alternatively happen as a result of response facilitation that increases the chances of a cotton-top punishing another primate after watching that individual perform a similar action.[34]

Dominant females may evict subordinate females from the group out of spite.

Another way to look at punishment in cotton-top tamarins is by observing their aggressive behavioral responses within and between groups, as well as between species. The cotton-top tamarin, like many marmosets, other tamarins, and specifically those in the genus Saguinus, will stage aggressive displays almost exclusively towards fellow monkeys that belong to the same gender.[35] These intra-sexual displays of aggression are more frequent in females, and are vital when a breeding female is forcing both sub-adult and adult females to emigrate out of a familial group.[15]

Though aggression can occur within groups, the response towards intruders of another species is much more drastic and can involve a sexual dimorphism in displays. Females will typically employ scent-marking intruder response tactics, whereas males are more prone to vocalizing threats, physical aggression, and piloerection.[36] Scent-marking in cotton-top tamarins is done in two ways: either using anogenital scent-marking, or suprapubic scent-marking. The ability to use both of these separate glandular fields for threat signals may indicate females have developed diverging evolutionary threats through differential use of these markings.[36] These variable signals may be used to sign a territorial encounter, or serve as a reproductive signal. The intensity of female threats are generally comparable when directed at intruders of either genders. In contrast, male cotton-tops are considerably more threatening towards fellow males than towards females.[36]

Communication[edit]

The cotton-top tamarin vocalizes with birdlike whistles, soft chirping sounds, high-pitched trilling, and staccato calls. Researchers describe its repertoire of 38 distinct sounds as unusually sophisticated, conforming to grammatical rules. Jayne Cleveland and Charles Snowdon performed an in-depth feature analysis to classify the cotton-top's repertoire of vocalizations in 1982. They concluded that it uses a simple grammar consisting of eight phonetic variations of short, frequency-modulated "chirps"—each representing varying messages—and five longer constant frequency "whistles." They hypothesize that some of these calls demonstrate that the cotton-top tamarin uses phonetic syntax, while other calls may be exemplars of lexical syntax usage.[37] Each type of call is given a letter signifier; for example, C-calls are associated with finding food and D-calls are associated with eating.[38] Further, these calls can be modified to better deliver information relevant to auditory localization in call-recipients.[37] Using this range of vocalizations, the adults may be able to communicate with one another about intention, thought processes, and emotion including curiosity, fear, dismay, playfulness, warnings, joy, and calls to young.[39]

Language acquisition[edit]

Over the first twenty weeks after a cotton-top tamarin is born, it is not fully capable of producing the range of vocalizations that an adult monkey can. Despite this limitation on speech producibility in cotton-top infants, researchers believe that language acquisition occurs early on with speech comprehension abilities arising first.[38] Infants can at times produce adult-like chirps, but this is rarely done in the correct context and remains inconsistent across the first twenty weeks of life. Regardless, infant cotton-tops are able to respond in behaviorally appropriate ways to varying contexts when presented with adult chirps. This indicates that verbal perception is a quickly acquired skill for cotton-top offspring, followed closely by auditory comprehension, and later by proper vocal producibility.[38]

Although limited in their own vocal ranges, juvenile cotton-tops respond appropriately to varying contexts provided by adult vocalizations.

Castro and Snowdon (2000) observed that aside from inconsistent adult-like chirping, cotton-top infants will most often produce a prototype chirp that differs in vocalization structure from anything seen in the full adult range of vocalizations. Infants are thought to imitate adult speakers, who use differing calls in various contexts, but by using solely the infant prototypical chirp. For instance, adult cotton-tops are known to significantly reduce the amount of general alarm calling in the presence of infants.[37] This is likely adapted so that adults that are close in proximity to the group's young do not attract attention of predators to infant-dense areas. Additionally, infants will reduce their prototype chirping in the presence of predators. Whether infants are shadowing the calling behavior of adults or they are comprehending danger remains unclear. However researchers argue that young cotton-top tamarins are able to represent semantic information regardless of immature speech production.[38]

To confirm the notion that language acquisition occurs as a progression of comprehension before production, Castro and Snowdon (2000) showed that infants will respond behaviorally to vocalizing adults in a fashion that indicates they can comprehend auditory inputs. When an adult produces a C-call chirp, used to indicate food preference and when navigating to a food source, an infant will approach the adult caller to be fed but will not use the prototype calling as a proxy for C-calls.[38] This finding argues for the idea that infants are able to understand vocalizations first, and later acquire the ability to communicate with adult vocalizations.

General calling[edit]

Among the typical cotton-top tamarin communicative vocalizations, the combination long call (CLC) and the alarm call (AC) are the most heavily represented in the literature. Combination long calls encompass a range of contact calls that are produced by isolated individuals using chirps and whistles.[37][40] This type of call is also used for seemingly altruistic alarm calls, thus adding to its range of cooperative behaviors. It is issued in the presence of kin when there is a threatening predator. Predators of the cotton-top tamarin include snakes, ocelots, tayras, and most notably, hawks.[19] Early observations by Patricia Neyman even showed that cotton-tops will produce diverse sets of alarm calls that can discriminate the presence of birds of prey versus ground-based predators.[15]

A mature cotton-top tamarin producing vocalization for group mates.

CLCs involve the production of complex sequence multisyllabic vocalizations. Researchers have argued that long calls exhibit individual differences and can thus carry information sufficient for recipient cotton-tops to determine caller identity. Using habituation-discrimination paradigms in language experiments, this theory has been confirmed multiple times in literature.[40][41] However, the individual syllables within a complete CLC vocalization in isolation of each other do not transfer sufficient information to communicate messages between monkeys. Scientists thus consider the whole, intact string of vocalizations to be the unit of perception for CLCs in the cotton-top tamarin.[42] These examinations may confirm that cotton-tops incorporate a lexical syntax in areas of their communication.

Since tamarins can discriminate between predatory threats using varying vocalizations, recipients of an AC are thought to extract various complex signals from this form of communication. Primarily, cotton-tops are able to glean the identity of the cooperating tamarin through differences in individuals' alarm calls.[19] Further, adults are able to discriminate the gender of callers from their ACs and determine the range of calls within a related tamarin's alarm calling repertoire.[19] Alarm call-based identification is postulated to play a number of functional roles in the cotton-top tamarin. Firstly, an alarm call recipient will be able to identify a cooperating tamarin and, by recognizing who in their group it is, be able to judge the reliability of the AC from past experience. This may arise from a selective pressure for being able to statistically determine the amount of risk present, and how endangered an individual and their group are.[19]

Additionally, being able to localize auditory signals may help determine predator location, especially in the presence of a second alarm call from a different tamarin in the group. This can help confirm predator presence, type (e.g. flying versus ground based), and support the recipient in triangulating a predator's location. In the context of the cotton-top's cooperatively breeding groups, this is postulated as being adaptive for determining the variable risk to one's group members.[19] For example, a call recipient will be able to determine which of its kin are and are not at risk (e.g. young offspring, mates, subordinate, relatives, carriers, etc.) and plan subsequent actions accordingly.

Food calls[edit]

The species is thought to vocalize food preference using C-calls and food retrieval and eating using D-calls.

The cotton-top tamarin makes selective, specialized vocalizations in the presence of food.[43] These include the C-call, produced when a cotton-top approaches and sorts through food, and the D-call, which is associated with food retrieval and is exhibited while eating.[37]

C-call chirping is believed to be an honest signal for communicating food preference, and a cotton-top tamarin will more often and more rapidly vocalize with these chirps when approaching a highly favored food source. Functionally, this behavior may inform other tamarins of the actions the caller will take in a feeding context and whether a preferable food source is available.[43] Despite this research indicating that food calls may be informative to fellow group mates, other observations of cotton-tops show that quantity and distribution of food and audience do not significantly alter a caller's food-centered vocalizations.[44]

The cotton-top tamarin is seen to produce food calls both in the presence and absence of group members.[44] Additionally, response to food calls will be directed back to an original caller independent of visual confirmation of a food source. While this may appear to be a result from a very primitive form of communication, Roush and Snowdon (2005) maintain that the food calling behavior confers some mentally representable information about food to recipient tamarins.

Conservation status[edit]

The wild population is estimated at 6,000 individuals, with 2,000 adults.[2] This species is critically endangered, and was listed in the "The World's 25 Most Endangered Primates between 2008 and 2012."[45] The publication lists highly endangered primate species and is released every two years by the International Union for Conservation of Nature Species Survival Commission Primate Specialist Group (IUCN/SSC PSG). The cotton-top tamarin was not selected for the 2012–2014 publication.[46]

The species is critically endangered, with a wild population of merely 6,000 individuals including about 2,000 free-roaming adults.

Habitat destruction through forest clearing is the main cause of this collapse, and the cotton-top has lost more than three-quarters of its original habitat to deforestation,[2] while the lowland forest in which it lives has been reduced to five percent of its historical range. This land is then used for large-scale agricultural production (i.e. cattle) and farming, logging, oil palm plantations, and hydroelectric projects that fragment the cotton-top tamarin's natural range.[47]

The illegal pet trade and scientific research have also been cited as factors by the IUCN/SSC PSG. While biomedical studies have recently limited their use of this species, illegal capture for the pet trade still plays a major role in endangering the cotton-top. Before 1976, when CITES listed the species under Appendix I banning all international trade, the cotton-top tamarin was exported for use in biomedical research.

In captivity, the cotton-top is highly prone to colitis, which is linked to an increased risk of a certain type of colon cancer. Up to 40,000 individuals were caught and exported for research into those diseases as well as Epstein-Barr virus, for the benefit of humans. The species is now protected by international law. Although there are enough individuals in captivity to sustain the species, it is still critically endangered in the wild.[47]

The Proyecto Tití ("Project Tamarin")[48] was started in 1985 to provide information and support in conservation of the cotton-top tamarin and its habitat in Northern Colombia. Proyecto Tití's programs combine field research, education and community programs to spread awareness about this endangered species and encourage the public to participate in its protection. It now has partner status with the Wildlife Conservation Network.[49]

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