Cebuella pygmaea
Creators: name: Russell A. Mittermeier
name: Anthony B. Rylands
name: Don E. Wilson
Publisher: name: Lynx Edicions
Year: 2013
Subjects: Biodiversity
Taxonomy
Animalia
Chordata
Mammalia
Primates
Callitrichidae
Cebuella
Cebuella pygmaea

description: 1.
Pygmy Marmoset
Cebuella pygmaea
French: Quistiti mignon / German: Zwergseidenaffchen / Spanish: Titi pigmeo Other common names: Eastern Pygmy Marmoset (niveiventris), Western Pygmy Marmoset (pygmaea)
Taxonomy. Iacchus pygmaeus Spix, 1823,
Brazil, Amazonas, near Tabatinga, Rio Solimoes, Amazonas State, Brazil.
Fur coloration used to distinguish Cebuella pygmaea is variable. Morphological, cytogenetic, and molecular genetic studies have shown that Cebuella is closely related to the Amazonian and Atlantic Forest marmosets. Healthy hybrids of C. pygmaca x Callithrix jacchus have been produced in captivity. Some regard them as congeneric, notably C. P. Groves who, in his 2001 book Primate Taxonomy, placed Cebuella as a subgenus of Callithrix. The validity of subspecies of C. pygmaea is still inconclusive, and geographic distributions are unclear. Two subspecies recognized.
Subspecies and Distribution. C. p. pygmaea Spix, 1823 — Upper Amazon in S Colombia, W Brazil, E Ecuador, and N Peru, N of the Amazon River and left bank of the Rio Pastaza, E to the mouth of the Rio Japura, and S of the Rio Japura-Caqueta to the Andes. C. p. niverventris Lonnberg, 1940 — Amazonian lowlands and Andean foothills in W Brazil, E Peru, and N Bolivia, S of the Amazon River, E of the Rio Mayo and the Rio Huallaga above the Rio Mayo, S to the upper Rio Purus, E to N Bolivia (Rio Muyumanu), and N probably through the entire interfluvium of the rios Purus and Madeira.
Descriptive notes. Head-body 12-16 cm, tail 17-23 cm; weight 85-140 g. Females are slightly larger than males. The Pygmy Marmosetis the smallest of the monkeys, generally tawny or gray-brown agouti with the upper surface of the tail barred with black. Ears are hidden by long backswept hairs on the cheeks that combine to form a mane. Eyes are large and almond-shaped. The “Western Pygmy Marmoset “ (C. p. pygmaea) is speckled greenish-brown above, with a buffy underside, described by E. Lonnberg as dirty yellowish brown, not sharply distinct from the color of the dorsum. Upperparts of the “Eastern Pygmy Marmoset” (C. p. niveiventris) are similar to the nominate form, although, according to Lonnberg who first described this subspecies, somewhat paler and more grayish on the posterior parts of the back, and especially the outer parts of hindlegs are paler. Lonnberg’s principal diagnostic feature for the Eastern Pygmy Marmoset was the color of the fur on the ventrum, which is “all over pure white with a very sharp line of demarcation as well across the foreneck as along the sides of the breast and flanks.” The white extends along the inner sides of the arms to the hands and likewise on the hindlegs to the feet, but there it becomes gradually yellowish, especially on the distal parts.
Habitat. Lowland forest near or in periodically inundated river floodplains; higher ground (terra firma) in bamboo thickets, liana forest, and secondary growth at the edges of pasture and orchards; and tree falls. It tends to travel in dense vegetation of the understory near the ground, usually below 5 m; it forages for insects and feeds on exudates in the middle strata of the forest, at heights up to 15 m; and it will often rest, play, and groom in the middle strata and lower canopy at heights of up to 20 m. In some regions, the Pygmy Marmoset shares its habitat with up to twelve other primate species. The many species of saddle-back tamarins (Saguinus) also travel and forage for insects in the lowest levels of the forest, and although they do not gouge tree trunks, branches, and vines to obtain exudates, they feed on gums from holes gouged by Pygmy Marmosets. Tamarins are generally less common in the floodplain forests preferred by the Pygmy Marmosets and more frequently occupy inland terra firma forests. Field studies on the demography, ecology, and behavior of the Pygmy Marmoset have been carried out by M. Ramirez at Mishani on the Rio Nanay and P. Soini in the Rio Maniti Basin both in north-western Peru and by S. de la Torre and colleagues at a number of localities in north-eastern Ecuador.
Food and Feeding. The Pygmy Marmoset feeds mainly on arthropods and exudates of certain trees and lianas. About two-thirds of their feeding time is dedicated to plant exudates—gouging tree trunks, branches, and lianas and eating gums that are exuded as a result. Holes they gouge with their lower incisors vary in shape and size, but they are generally oblong or circular, 10-20 mm wide, and 4-18 mm deep. The form, depth, and size of the holes depend on qualities of the bark and wood of each species. Exudate feeding is most common from ground level to ¢.7 m, but extends up to 15 m into the lower canopy of the forest. Pygmy Marmosets generally enter a tree by jumping onto the upper part of the trunk, and then they go down and work their way back up, visiting gouge holes as they go. They visit 5-8 holes/minute, eating from each for c.3 seconds and gouging for another 4-5 seconds. A large number of gum-producing trees and vines are exploited. Fifty-eight tree species were exploited by the Pygmy Marmosets during c.1400 hours of observation of groups along Rio Maniti, but just a few were used intensively, most notably species from the families Anacardiaceae (Spondias mombin), Fabaceae (Parkia oppositifolia), Vochysiaceae (Vochysia lomatophylla), and Meliaceae (Trichilia). Qualea (Vochysiaceae) and Inga (Fabaceae) are also important. A group of Pygmy Marmosets typically has one principal tree as a source of exudate and a number of secondary sources. When exudates from the principal source diminish or dry up, the group switches to a suitable secondary source or moves to a new home range. The principal exudate source of a group of Pygmy Marmosets at Mishani was a Quararibea rhombifolia (Bombacaeae) tree. Three Trichilia trees and the vine Cheiloclinwm cognatum (Celastraceae) were used secondarily, and V. lomatophylla and Inga were exploited very infrequently. Nineteen groups of Pygmy Marmosets in six localities in north-eastern Ecuador used 21 species as exudate sources; all were trees, except one. The species exploited and the number of sources varied between localities; 2-8 (mode = 2) trees of 1-5 different species (mode = 2). The principal food trees differed at each locality: Sterculia apetala (Sterculiaceae) at San Pablo, Cedrela odorata (Meliaceae) at Sacha, Inga marginata (Fabaceae) at Amazoonico, and Parkia balslevii (Fabaceae) at Zancudo. Each food source accounted for 53-93% of all the records of this activity. Choice and intensity of use of particular gum-providing species are not related to its abundance in the forest, but exudate productivity and quality are thought to be the key factors. A gouge hole in a Quararibea, for example, can produce a marble-sized glob of gum in less than 30 minutes, whereas a similar sized hole in Trichilia may produce a small drop of gum in the same time. The remaining feeding time is focused on arthropods (spiders, Coleoptera, Hemiptera, Hymenoptera, Lepidoptera, and Orthoptera) and sometimes small vertebrates (e.g. Anolis, Cnemidophorus, Gonatodes lizards, and birds). Fruits (e.g. succulent Ficus [Moraceae] and Pourouma [Urticaceae]), buds, flowers, and nectar are also eaten when they become available.
Breeding. Typical of callitrichids, Pygmy Marmosets generally give birth to twins, occasionally singletons or triplets. The single breeding female in a group is able to give birth twice a year, with interbirth intervals of 5-7 months. In captivity, mean gestation is c.142 days, time from parturition to the resumption of ovulation is c.14 days, ovarian cycles have a mean length of 27 days, and first births for females occur when they are 24-42 months old and 5-27 months after pairing with a male. Interbirth intervals of 31 full-term pregnancies in captivity were 149-746 days (mean 212-7 + 122-3 days). In captivity, Pygmy Marmosets can conceive at 19 months old, indicating that puberty occurs when they are c.1-5 years old. They give birth until they die at 11-12 years of age, although interbirth intervals increase as they age and infant survival decreases. A pair bond is formed between a female and her mate, but when there are two adult males in the group, both may copulate with her. The dominant male guards the female when she is receptive, keeping near and frequently approaching her, with occasional brief chases, smelling, and licking her genitalia and urine, which is associated with frequent genital presenting by the female (tail raised in a stiff arch). The male and female increase their scent marking, mutual huddling, and grooming at this time. In the wild, in the Peruvian Amazon at least, births occur throughout the year, but there are two peaks, one in May-June and the other in November—January. Eighty-four percent of the parous groups studied at Maniti produced twins in both birth peak periods. Females are not receptive during pregnancy or for 3-6 weeks following birth. Parturition generally occurs at night. Neonates weigh 13-15 g (head-body length 51-63 mm). Group members carry infants for the first 1-5-2 months and constantly for the first 1-2 weeks. As infants age, they may be left on their own (e.g. parked in the crown of the group’s principal feeding tree) for gradually longer intervals while group members forage. They are weaned at three months of age, begin to gouge for exudates by five months, and feed independently by six months. Group members offer food items to infants while they are learning to catch their own prey. Testes reach full size at 16 months. Females reach sexual maturity at 15-17 months and can conceive at 17 months. Infant survival rate in the wild has been estimated at 67%. Females have a postpartum ovarian cycle while still lactating, and males may show sexual interest in females nine days postpartum. Cycles of behavioral receptivity last six days.
Activity patterns. Groups are active for about twelve hours a day, starting their activities at ¢.06:00 h and retiring to their sleeping sites a little before sunset at ¢.18:00 h. Heavy rain curtails their activities. Daily activities include exudate feeding, foraging on insects, resting, playing, huddling, and social grooming. Exudate feeding takes up c.33% of their day, insect foraging 16%, traveling 11%, and resting and social activities c.40%. A typical day for a group of Pygmy Marmosets includes feeding on exudates in the morning (variably until 06:30 h or as late as 09:00 h), with a gradualshift to basking, huddling, grooming, and play, followed by insect foraging until ¢.12:00 h when they rest again until early afternoon. Feeding on exudates and insect foraging resume.16:00-16:30 h until the group movesto its sleeping site before sunset.
Movements, Home range and Social organization. Groups of Pygmy Marmosets are generally made up of a reproductive female and her mate, their offspring of up to four consecutive litters (twins), and sometimes other adults that may or may not be related to the breeding pair. Groups have 2-9 individuals, with a modal size of 6-7 (mean 5-1, n = 80 groups). Groups are often described as extended families, and most, often all, group members care for (e.g. carry) infants of the breeding female. Both sexes disperse, often as young adults, and join other groups or form new groups with other dispersing individuals. Dominance can be detected by individuals supplanting others at the exudate feeding holes. The breeding female is dominant over all group members, the breeding male is dominant over other males, and oldersiblings are dominant over youngersiblings. As with all callitrichids, grooming is an important aspect of their social life, taking up as much as 9% of their day. Groups occupy small, exclusive (no overlap with other groups) home ranges of 0-1-0-5 ha. In Ecuador, 19 groups had home ranges of 0-15—1-2 ha, with larger home rangesin igap6 (black-water inundated forest) (mean 0 74 + 0-1 ha) than in varzea (white-water inundated forest) (mean 0-42 + (0-07 ha). A home range near a river typically included a 90-m stretch of water-edge vegetation and extended away from the water ¢.20-60 m. Each day, a group may move 30-100 m, with their tortuous total travel paths of 280-300 m being determined largely by the location of exudate sources. The pattern of space use by Pygmy Marmosets differs from other callitrichids in that a group as a whole does not move around its home range but rather individuals are often scattered throughout their very small home ranges. Group members usually sleep together in a huddle in the crotch of a branch, a stump of an old broken branch, sometimes in an old termite nest, or a clump of epiphytes. These locations are generally at 7-10 m above the ground in the lower or middle crown of small (10 m high) to middle-sized (20 m) trees. Groups tend to have 1-3 habitual sleeping sites, one of which is used frequently and the others sporadically. Communication among group members is olfactory (urine and specialized skin glands), tactile, vocal, and postural. A ritualized genital display involves an individual turning its rump toward another, arching its back, raising its tail in a stiff arch, and strutting. Fur on the body and tail are ruffled, and the individual may produce a few drops of urine. This display is used by dominant males confronting subordinates, who crouch and remain still. Females display their genitals in this fashion, but without the strutting, back arching, and fur ruffling, as a sexual display/invitation to males. Adults and younger individuals of both sexes perform this display, accompanied by strutting and sit-rubbing (anogenital gland marking) toward humans. Studies of captive Pygmy Marmosets have shown patterns or sequences of calling among individuals in a group. These and various other findings indicate that they have a “conversational rule system”; in other words, they have “conversations.” Pygmy Marmosets flee, giving alarm calls, from approaching squirrel monkeys (Saimiri) and capuchin monkeys (Cebus and Sapajus). It is possible that tufted capuchins in particular are predators of Pygmy Marmosets. Although predation is very rarely seen, other potential predators include hawks and falcons, forest cats, Tayra (Eira barbara), and snakes (e.g. fer-de-lance, Bothrops atrox). Densities are 51-59 ind/km?in floodplain forest in Peru and 210-233 ind/ km?in their preferred habitats of river-edge forest. These high densities do not occur in all apparently suitable habitats, and it has been argued that the highest densities are found in areas where presence of humans has reduced numbers of predators, including capuchin monkeys, but has not resulted in excessive disturbance of the river-edge vegetation. Densities, and even the presence or absence, of Pygmy Marmosets are also dependent on distribution and abundance of exudate sources.
Status and Conservation. CITES Appendix II. Classified as Least Concern on The [UCN Red List. The Pygmy Marmoset is not hunted, except for some trade as pets. It has a patchy distribution, being abundant in some areas of river edge, scarce along inland creeks or patches of secondary, bamboo, and liana forest, and absent over large expanses of terra firma forest with sparse understories. Deforestation and disturbance of their river-edge habitats can be detrimental and even cause local extinctions. In Ecuador, habitat disturbance and fragmentation (e.g. patches of river edge forest surrounded by pastures and crops) cause gradual population declines. Disappearance of Pygmy Marmosets can be partly explained by depletion of their exudate sources and absence of accessible new sources. Pygmy Marmosets are particularly sensitive to traffic, ambient noise, and persecution and capture as pets.
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description: Published as part of Russell A. Mittermeier, Anthony B. Rylands & Don E. Wilson, 2013, Callitrichiade, pp. 262-346 in Handbook of the Mammals of the World – Volume 3 Primates, Barcelona :Lynx Edicions on pages 307-308, DOI: 10.5281/zenodo.5730714