BUFFY-HEADED MARMOSET

Callithrix flaviceps

Geographic Distribution and Habitat

Native to Brazil, the rare buffy-headed marmoset (Callithrix flaviceps) occurs in the Serra da Mantiqueira (Mantiqueira Mountain range) south of the Rio Doce in southern Espírito Santo, its range here reaching the state boundary of Rio de Janeiro. Other southeastern populations have been reported in the municipality of Pingo d’Água, approximately 6.2 mi (10 km) from the east bank of the Rio Doce.

The species’ northern and western ranges extend into eastern Minas Gerais, reaching the municipality of Manhuaçú. Populations are dispersed throughout various localities within highly fragmented forests of the Rio Manhuaçú basin. Two possible populations occur in localities in southern Minas Gerais, but researchers are unsure whether these primates are buffy-headed marmosets or hybrids of the buffy-tufted-ear marmoset (C. aurita), who is also a resident of this region, known as a natural hybridization zone.

Researchers speculate that these New World monkeys may have once occupied Rio de Janeiro’s northern municipalities of Natividade and Porciuncula, with an extended range north of Bom Jesus do Itabapoãna—back when all these regions were still densely forested. A lone individual collected back in 2011 from the municipality of Varre-Sai in Rio de Janeiro’s northernmost region has led researchers to speculate about an established buffy-headed marmoset population there. But a thorough investigation is necessary to confirm the species’ presence.

Of all marmoset species, the buffy-headed marmoset has the smallest geographic distribution. They dwell within patches of dense vegetation at the edge of montane Atlantic coastal forests and within forests of the inland plateau at altitudes from 1,312 ft (400 m) up to 3,937 ft (1,200 m) where temperatures fall close to freezing during the dry season.

Preferred habitats of buffy-headed marmosets are disturbed secondary forests, as opposed to old growth, or primary, forests. 

TAXONOMY IN TRANSITION

Prior to attaining full species status, the buffy-headed marmoset had been considered a subspecies of the common marmoset (C. jacchus), whose other members once included the black-tufted marmoset (C. penicillata), the white-headed marmoset (C. geoffroyi), and the buffy-tufted-ear marmoset. Each is now considered a full species.

Some researchers had contended that the buffy-headed marmoset should be classified as a subspecies of the buffy-tufted-ear marmoset. They cited similarities in pelage patterns, ear tufts, facial mask, and vocalizations. But a greater number of researchers rejected this contention, successfully arguing that the buffy-headed marmoset is, in fact, a distinct species. To support their argument, they cited extensive ecological and behavioral studies of both buffy-headed and buffy-tufted-ear marmosets—thereby snuffing out this taxonomic kerfuffle. Today, the buffy-headed marmoset continues to bask in its own full species status glory.

Buffy-headed marmoset range, IUCN 2008

Size, Weight, and Lifespan

Marmosets, along with tamarins, are distinguished from other New World monkeys by their small size. Marmosets hold the distinction as the world’s smallest primates.

The miniature buffy-headed marmoset is about the size of a kitten, weighing from 14 oz to 1 lb (0.4–0.45 kg), with a head-to-body length between 7.1 and 11.8 in (18–30 cm). Its long tail adds another 6.8–15.9 in (17.2–40.5 cm). Males and females are similar in size. 

Lifespan in the wild is up to 10 years, and up to 16 years in captivity.

What Does It Mean?

Gummivore:
A class of omnivore whose main diet is tree gum, sap, and resin with bugs for protein.

Visit the Glossary for more definitions

Appearance

The buffy-headed marmoset may have one of the most charming faces of the primate world. Cream-colored fur covers the forehead, cheeks, and chin, while darker fur surrounds its amber eyes, before daubing a flattened nose that is accented with downward-flaring nostrils. The resulting mask-like appearance has inspired comparisons to the face of a sad clown. But really, it’s the long, yellowish tufts of hair that flail out wildly from the temples that bear resemblance to the crazy coiffure of a certain children’s jokester: Bozo the Clown. (Any resemblance to Bozo ends here.)

A thick, buff-colored mane covers the head and buries this monkey’s ears. The delicate frame is cloaked by a gray-brown fur coat, with lighter-colored fur covering the underside. Alternating bands of black and white fur give accent to the long tail. Unlike many New World monkeys, the tail of the buffy-headed marmoset is nonprehensile. And if you could peek inside its mouth, you’d see only two molar teeth, rather than three, on either side of their jaw. Claws on each of their digits, except for the big toes which have nails, help these marmosets cling to trees while they feed. Their thumbs are non-opposable.

Photo credit: Peter Schoen/Creative Commons
Diet

Buffy-headed marmosets are omnivores. Included in their meal plan are fungi, insects, spiders, fruits, nectars, flowers, tree gums and saps, bird eggs and nestlings, and the occasional tree frog or lizard. The foods they choose to eat depend on their habitat.

While most marmosets are primarily gummivores (feeding on tree gums), buffy-headed marmosets are primarily mycophagists-insectivores, a fancy way of saying that they eat a lot of fungi (mushrooms) and insects. While eating mushrooms (mycophagy) is rare behavior for most nonhuman primates, buffy-headed marmosets have adapted to this ecological specialization in habitats where fungi are plentiful and likely provide greater nutrition than other available food sources. As example, within Augusto Ruschi Biological Reserve in Espírito Santo in southeastern Brazil, where fungi grow at the base of neotropical bamboo plants, researchers found that the diet of these marmosets consisted of about 65 percent fungi, about 26 percent animal prey, 6 percent tree gums, and just over 3 percent fruit.  

In other areas, however, including Caratinga Biological Station in the state of Minas Gerais, gum is a year-round dietary staple for these tiny primates, followed by fruits (only plentiful during the months of January and February), and a sprinkling of insects for protein. Most of the gum in the buffy-headed marmoset’s diet comes from acacia trees (Acacia paniculata), which are prevalent in the secondary forests where these little monkeys reside.

But tree gums, which contain complex carbohydrates (polysaccharides), are not easily digested. Gums can take more than 17 hours to completely digest! Fortunately, the digestive system of the buffy-head marmoset has evolved to break down this plant-based material and extract essential macronutrients through a process known as microbial fermentation. Naturally occurring gut bacteria (microbes) and a specialized cecum (the pouch in the lower abdominal cavity that processes undigested food from the small intestine before connecting to the colon) aid in the fermentation process.

Because they aren’t forced to expend a lot of energy in acquiring their food, the daily caloric needs of buffy-headed marmosets are relatively low.

Behavior and Lifestyle

These shy, miniature monkeys are mostly arboreal (tree-dwelling), scampering from tree to tree quadrupedally (on all four limbs) in jerky motions, similar to squirrels. But buffy-headed marmosets might outperform squirrels. Thanks to their adaptive primate anatomy (known as “tegulae” in science-speak), they are able to hang vertically from a branch by digging their claws into the bark. (Of course, many of us have likely seen an intrepid squirrel hanging from a backyard bird feeder!)

Buffy-headed marmosets are active during daylight hours, making them diurnal. A big part of their day is spent foraging and eating, followed by resting and socializing.

For those who rely on tree gum for nourishment, foraging is about skill and strategy. While their dentition might be less specialized for tree-gouging to obtain gum—compared to that of the common marmoset and the black-tufted marmoset—buffy-headed marmosets are equipped to get the job done, if they must. They are opportunists who will exploit an already-gouged tree for its gum source, and they are known to return to established feeding sites. Nevertheless, their short canine teeth and their long lower incisors, which function as a chiseling tool (a morphological adaptation) enable them to gnaw through tree bark. Then, by inserting their rough tongue into a notched hole, they efficiently extract the gum from within.

Overnight, buffy-headed marmosets sleep in dense, vine-filled tangles within the trees—where, hopefully, they remain undetected.

As you would expect, their small size makes buffy-headed marmosets vulnerable to predators. Raptors, snakes, small wild cat species (including ocelots), and humans are their main predator threats. Fortunately, these small monkeys are fast and nimble as they traverse through the trees to make an escape.

Daily Life and Group Dynamics 

Buffy-headed marmosets live in family groups (or “troops”) of 3 to 20 individuals. A larger troop may include up to four breeding females, though only one is the primary breeder. She and her male partner rank as the dominant members of a troop. In addition to the dominant breeding couple, unrelated males, young offspring, and extended family members complete the family.

Little information is available about the group dynamics of buffy-headed marmosets. However, we might take some clues from that of the common marmoset, who had once been considered the parent species of the buffy-headed marmoset. Common marmosets leave their natal (or birth) groups upon reaching adulthood, unlike most primate species who leave their natal group during adolescence. When there are two breeding females, one is more dominant than the other (as we can confirm for buffy-headed marmosets). The subordinate female is often the daughter of the dominant female. A troop’s females are closely related, more so than a troop’s males. Males refrain from copulating with females to whom they are related. Following the death of a dominant breeding male, family groups merge with other troops. Social rank in a common marmoset troop is based on age.

Home ranges of 81.5–342 ac (33.9–138.3 ha) are the norm for buffy-headed marmosets and may overlap with other buffy-headed marmoset troops. Because food sources are typically readily available, territorial squabbles are uncommon.

More than 60 percent of all of Brazil’s threatened animal species live within its Atlantic Forest, a biodiversity hot spot similar to that of the Amazon Rainforest. Some of the sympatric species of the buffy-headed marmoset include howler monkeysgolden lion tamarinsmuriquis, maned three-toed sloths, Babisuris (ring-tailed wild cats), blacktailed jack rabbits, snakes (including the Espírito Santo blind snake, Trilepida salgueiroi), lizards, thin-spined porcupines, Brazilian snake-necked turtles, red-tailed parrots, blue footed boobies (marine birds), and large colonies of sea lions.

Communication

Marmosets may have perfected the art of communication, combining vocalizations with body postures.

Vocalizations include short, high-pitched alarm calls sounded to warn others of a potential predator threat; low-pitched trills sounded to locate fellow troop members; and bird-like whistles sounded to attract the attention of a potential mate.

Body postures further convey a message or signify a mood. A partial, open-mouth stare accompanies alarm calls. A frown indicates aggression, while a “slit-eye” stare indicates submissiveness. When frightened, they flatten their wild ear tufts against their heads.

To convey social and reproductive status, marmosets leave their secretions (or “calling card”) on forest substrates. Scent glands on their chests and anogenital regions facilitate this endeavor.

Like most nonhuman primates, marmosets engage in allogrooming, a practice that helps to instill social bonds. Subordinate troop members often groom superiors in an effort to curry coalitionary support from these higher-ranking members.

Reproduction and Family

Mating systems among marmosets vary among species and include monogamy (the practice of mating with an exclusive partner), polygyny (one male mates with multiple females), and polyandry (one female mates with multiple males). While instances of polygyny and polyandry have been observed in buffy-headed marmoset troops, monogamy appears to be the convention that most of these primates follow. The species breeds year-round.

Female buffy-headed marmosets are considered sexually mature (able to conceive and bare young) between 20 and 24 months of age. Males attain sexually maturity (able to sire offspring) much earlier, between 9 and 13 months of age. To entice her male partner, an ovulating female clicks her tongue.

The dominant female is the primary child bearer. Occasions of up to four females giving birth simultaneously within a single troop have been reported. However, infants of subordinate females are likely to be health compromised.

Pregnancy lasts nearly five months, and twin births are the norm. Every now and then, triplets are born. The typical birth interval is six months; that is, a female gives birth twice a year (however, the potential exists for three births a year, given the species’ practice of breeding just 10 days after giving birth).

A mother nurses her infant for about 3 months, at which time the infant is considered weaned. Some researchers have speculated that the gums contained in the female buffy-headed marmoset’s diet contain a form of “milk sugar” (galactose) that facilitates the development of mammary glands and may increase a nursing female’s body lipids, important essential fatty acids in mother’s milk.

Nursing a pair of twins, twice a year, is stressful on a buffy-headed marmoset mother. So Mother Nature has stepped in with her biological assistance. The presence of the dominant breeding couple suppresses, through aggressive interaction, sexual development of young troop members of both sexes until they leave the group. These young sexually suppressed individuals are likely related to the breeding couple, providing them with incentive to help care for newborns.

For the first two weeks of their lives, infants cling to their mothers. After that, childcare becomes a family event. An infant’s father and the entire troop help with the little ones by carrying them, babysitting them (giving the mother a much-needed rest break), and teaching them how to be a buffy-headed marmoset. This practice of everyone participating in child care is known as “alloparenting.”

At about 5 months of age, young marmosets are considered juveniles. They have increased interactions with other troop members and engage in play with others their age. 

​Ecological Role

​Buffy-headed marmosets help to replenish their forest habitat by dispersing the seeds (via their feces) of the fruits they eat. They also help to encourage plant growth by pruning the many trees they visit through their extensive foraging for plant gums.

Conservation Status and Threats

The buffy-headed marmoset is classified as Critically Endangered by the International Union for Conservation of Nature (IUCN, July 2019), appearing on the IUCN Red List of Threatened Species. Loss of habitat through anthropogenic activities is responsible for a drastic population decline in this rarest of marmoset species and remains a serious threat to the species’ survival. A further 20% decline is expected over the next five years (as reported in 2000).

Expansion of urban areas and “slash and burn” agricultural practices have led to extensive fragmentation and deforestation. Pristine, forested buffy-headed marmoset habitat has been lost, replaced by human developments, mining operations, cattle ranching, coffee and eucalyptus plantations, and tracts of farmland.

Human predation is another serious threat to these miniature monkeys, who are kidnapped and sold into the exotic, and illegal, pet trade. Sadly, buffy-headed marmosets (like so many wildlife species) do not fare well, nor do they belong, in captivity. Buffy-headed marmosets are also captured and sold to research laboratories. Unfortunately for marmosets, they are susceptible to diseases that afflict humans, such as cancer. Hence, these monkeys are popular research subjects.

The monkeys are also susceptible to other diseases that infect humans. An epidemic outbreak of yellow fever (an acute viral hemorrhagic disease transmitted by infected mosquitoes) in 2016 is responsible for a devastating toll on buffy-headed marmoset populations.

Hybridization is a sinister biological threat. Breeding with other marmosets who live in the natural hybridization zone leads to a loss of genetic characteristics and sets the buffy-headed marmoset on the perilous path toward extinction.

Finally, the world’s climate crisis is a specter that looms over the mountainous region where buffy-headed marmosets live. As temperatures here warm, the monkeys are forced to go higher in search of cooler habitat—until they have nowhere else to go.

The species’ total population is less than 2,500 adult individuals.

Brazilian conservationist Antonio Rossano Mendes Pontes has described the buffy-headed marmoset, in the company of 60 percent of all of Brazil’s threatened animal species living within the Atlantic Forest, as “the living dead.”

Conservation Efforts

The buffy-headed marmoset is listed in Appendix I of the Convention on International Trade in Endangered Species (CITES), an international agreement between governments whose goal is to ensure that international trade in specimens of wild animals and plants does not threaten their survival.

This species occurs in the following protected areas:

Minas Gerais:
Caparaó National Park (part of Espírito Santo)
Caratinga Biological Station/RPPN Feliciano Miguel Abdala Private National Heritage Reserve
RPPN Mata do Sossego Biological Station (privately owned)

Espírito Santo:
Augusto Ruschi Biological Reserve
Pedra Azul State Reserve
Forno Grande State Reserve
São Lourenço Biological Station
Santa Lucia Biological Station
Montes Verdes Florest Reserve (privately owned)

(RPPN=Reserva Particular do Patrimônio Natural.)

In 2018, the Brazilian Ministry of Environment created The National Action Plan for the Conservation of the Atlantic Forest Primates and the Maned Sloth. This conservation action plan covers 23 native species, including the Critically Endangered buffy-headed marmoset and the Endangered buffy-tufted-ear marmoset.

Other initiatives for the conservation of marmosets include the Mountain Marmosets Conservation Program, which has been working in collaboration with several researchers and national and international institutions to put into practice conservation actions. The Mountain Marmoset Conservation Center at the Federal University of Viçosa, in the state of Minas Gerais, is the first center of primatology in the world focused exclusively on both mountain marmosets, and in developing conservation activities in situ (on-site conservation) an ex situ (off-site conservation).

To date, attempts to establish a captive breeding program have to date been unsuccessful.

One proposed solution to the hybridization threat is the creation of “safe haven” forests where only “pure” buffy-headed marmosets live—no hybrids. However, experts say that such an undertaking would be difficult and costly. The sterilization of hybrid animals is another proposed solution.

Conservationists emphatically call for swift and aggressive action from Brazil’s government to safeguard the species survival. Further studies are urgently needed to determine the occurrence of hybridization, the susceptibility and impact of yellow fever, and to learn more about the overall ecology of the buffy-headed marmoset. Lastly, but no less important, enforcement of wildlife protection laws to prevent the kidnapping of these little primates must be stringently carried out.

References:
  • ​Hance, Jeremy. “Meet the kitten-sized, clown-faced monkey that’s leaping toward extinction.” Mongabay Series: Saving Life on Earth: Words on the Wild. August 10, 2021 (https://news.mongabay.com/2021/08/meet-the-kitten-sized-clown-faced-monkey-thats-leaping-toward-extinction)
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Written by Kathleen Downey, December 2021