RED-BELLIED LEMUR

Eulemur rubriventer

Geographic Distribution and Habitat
The red-bellied lemur is a species of Eulemur endemic to Madagascar. This primate inhabits a long, narrow strip of intact primary and secondary rainforest along the island’s eastern coast. While the red-bellied lemur’s distribution is not well-documented, populations are found at high altitudes in Tsaratanana Massif at the north end of the island. Red-bellied lemurs are thinly dispersed in middle-to-high altitudes throughout the band of eastern lowland forest, as far south as the Pic d’Ivohibe Special Reserve and Manampatrana River.

Madagascar’s complex geographical origins have important implications for the species who live there today. It is located in the Indian Ocean, 250 miles off of Africa’s southeastern coast. The island was originally a part of the supercontinent, Gondwana, locked between what is now Africa and India. About 165 million years ago, tectonic plate movements caused a large chunk of the landmass to split from the Africa portion. This newly separated land included Madagascar, India, Australia, and Antarctica. Additional movements of the Earth’s crust split the piece further, finally separating Madagascar and India (which moved northwards into Asia) about 88 million years ago.

Madagascar is the fourth largest island in the world and falls entirely in the southern hemisphere. The island contains four types of tropical rainforests: spiny forest in the south, dry forest and mangroves on the western coast, and moist forest in the east. The topography, location, and evolutionary path of the island gave rise to unique plant and animal species and new ecosystem dynamics. Species endemic to Madagascar, including all Malagasy primates and the red-bellied lemur, are not observed anywhere else in the world.

Red-bellied lemur geographic range. Map: IUCN, 2020 (click to enlarge)

Size, Weight, and Lifespan
Both male and female red-bellied lemurs have similar body proportions throughout their lives and reach sexual maturity at around two years of age. At birth, neonates weigh 1.9 lbs (0.85 kg). Infants are small enough to be carried by their parents for the first four months of life but quickly transition to self-sufficient movers and foragers as young sub-adults. Once fully developed, adults weigh about 4.4–5.3 lbs (2.0-2.4 kg). Their body length is roughly 17 in (43 cm) long. Measuring 20 in (51 cm) from base to tip, their tails account for slightly over half of their total body length. They are similar in size to other sympatric Eulemurs, such as the red-fronted brown lemur, as well as other Lemur species on the island, like the well-known ring-tailed lemur. In the wild, the average lifespan of this primate is 20–25 years.

Appearance
At a distance, it may be difficult to notice differences between individual adults. However, red-bellied lemurs exhibit dichromatism, meaning that males and females develop color patterns or markings distinct to their sex. In this species, sexual dichromatism is not as gaudy or pronounced as with other species. Unlike with peacocks, ducks, or even hamadryas baboons, sex differences in appearance are not important for securing mates, nor for providing camouflage.

Red-bellied male lemurs are covered by chestnut-brown fur, but females have a subtly lighter hair coat and a cream-colored underside. Only males possess the eponymic “rubriventer,” or “red-belly.” The sexes also show slight differences in facial features. Males have a white, tear-shaped marking beneath each eye and tend to have a darker muzzle and denser cheek fur. While both sexes engage in scent-marking behaviors, males possess an additional scent gland on the top of their heads. During bouts of active marking, males will adopt a slicker appearance from the scent-gland secretions.

Red-bellied lemurs also possess physical attributes that are characteristic of Madagascar lemurs, ones shared with other distant lemur relatives in Africa and Asia, and traits that are consistent with higher primates. These morphologic differences translate into functional significance when considering the evolutionary, ecological, and social contexts of species. Like all other primates, red-bellied lemurs have forward-facing eyes, which aid in binocular and stereoscopic vision. Yet relative to those of apes and other monkeys, lemurs’ eyes are large and significantly wider-angled. Their faces appear more prognathic (snouty), due to an elongated, wet nose and protruding jaw. Unlike higher primates that primarily rely on vision, lemurs retain a heightened sense of smell. Their well-developed, wetted nose is more sensitive to olfactory stimuli in the environment. For lemurs, scent-detection is important not just for finding food, but also for receiving and navigating important social cues. Their mouths contain specialized bottom incisors, which are closely grouped together and pushed outwards to form a “tooth-comb,” and their hands are equipped with a grooming claw on the second digit.

What Does It Mean?

Allogrooming:
Social grooming within a species.

Binocular vision:
Both eyes are forward-facing and have overlapping visual fields to produce a single, three-dimensional image.

Conspecific:
Belonging to the same species.

Cathemeral:
Irregularly active during night or day, dawn or dusk, depending on environmental circumstances.

Extirpated:
When a species ceases to exist in a geographic area they once occupied.

Frugivore:
An animal who feeds on fruits.

Stereoscopic vision:
Combines different inputs of the images received by each eye into a succinct, singular image with the proper size, depth, and proximity.

Sympatric: 
Occurring or living in the same area; overlapping in distribution.   

Tooth-comb:
The incisors on the lower front jaw of some animals are grouped as if to form a comb. The tooth-comb is used by these animals to groom and clean their fur or hair.

Visit the Glossary for more definitions

Diet
Red-bellied lemurs are predominantly frugivores, preferring large ripe and unripe fruits that grow on trees in moist eastern forests. While frugivory accounts for 80% of their dietary intake, they have been observed browsing on flowers and leaves of 70 different plant species and occasionally consuming invertebrates. When active in the nighttime, a red-bellied lemur locates a nearby eucalyptus tree, whose flowers only open at night to produce nectar.

Behavior and Lifestyle
Red-bellied lemurs are both arboreal (tree-dwelling) and cathemeral, meaning that they may be intermittently active in the daylight or nighttime, depending on daily environmental variation. Most of their active time is spent foraging in groups using a “sentinel” strategy: one group member watches while the others feed, taking rotations to ensure everyone is adequately satiated. The preference for nocturnal activity is likely made to avoid predators, as predation risk is reduced when the lemurs are less visible to raptors, fossa, and domestic cats and dogs. That red-bellied lemurs rest during the day in trees with dense foliage and employ strict methods of feeding vigilance supports this hypothesis. 

Red-bellied lemurs reside in a relatively small home range of 0.7 square miles (19 ha) and travel about a half-mile per day (450 m). Movement in the trees is usually accomplished by leaping horizontally to branches, walking or running on all fours along tree limbs, and sometimes by climbing up and down. They will sometimes “head-downward climb,” a type of movement not seen in other lemurids but utilized frequently by many small primate species. Compared to the heftiest of the other head-downward climbing primates, the red-bellied lemur is at least 200% larger.

A group has nearly exclusive access to their designated range, and individual group members diligently monitor and scent-mark their territory throughout the year. Both males and females mark using ano-genital scent glands to assert presence and signal neighboring cohorts to stay away. Males scent-mark more often with their scent glands during the food-abundance season, which coincides with mating season.

Fun Facts

Madagascar is about the size of California and Oregon combined.

The amount of time adult male lemurs spend in contact with infants is on par with the amount of time men in the United States spend with their infants: 15–90 min per day, or 25–35% of the time mothers spend with infants. Also, lemur infants play more with fathers than with their mothers, as do young humans.

Daily Life and Group Dynamics 
These primates form small family groups of two to six related individuals. Living groups consist of an adult male and female pair and their non-breeding offspring. Both male and female young disperse from natal groups. 

Pair-living is the rarest of primate social structures, seen in 29% of species. Among mammals in general, only 9% are both socially and reproductively monogamous. One study of red-bellied lemur groups at Ranomafana National Park sought to clarify the nature of these social pairings, specifically how prevalent they were and whether pair-bonds actually reflected reproductive monogamy. The research revealed that 81% of individuals resided in nuclear family groups. Within the groups, 75% of offspring were genetically related to both the adult male and female. The few exceptions to the trend resulted from delayed dispersal of offspring, death of the original male and subsequent replacement with a new male, and extra-group copulations. In general, red-bellied lemurs form pair-bonds that are very cohesive and stable. These partnerships last at least six years, regardless of seasonal food availability or other ecological pressures. 

The pair-bond is also characterized by low rates of male-male competition, male-infanticide, or attempts to monopolize red-bellied lemur females. Breeding females are typically intolerant of each other. Family units are egalitarian and stable; conflict is rare between members. Adult male-female pairs work together to defend their home range and care for offspring. Females consistently lead groups in travel more often than males, both in pursuit of food and in general group movement.

Communication
This species employs multiple types of signaling to maintain proximity to other group members, coordinate travel, and defend territory. Due to the social structure of red-bellied lemurs, most communication is directed towards pair-mates and offspring. Signaling is important for forming, reinforcing, and advertising social bonds. Communication may be auditory, tactile, or olfactory, often involving combinations of these modalities. 

When used, tactile communication, or physical touch, is motivated by a willingness to enhance social (and physical!) closeness with other group members. Red-bellied lemurs may mutually groom, allogroom, or huddle together closely. Special scent glands that are distributed throughout their bodies are their main agents of olfactory communication. The glands are concentrated principally in the anal and perianal region in females, while males have the additional scent-secreting region on the crown of their heads. Scent marking establishes home boundaries and also helps with group movement. Allomarking (scent marking other species members) is considered both tactile and olfactory. Its significance is complex and not fully understood. In general, strepsirrhines engage in scent marking more frequently than other primates, with the exception of tarsiers and sternal-marking species of New World monkeys, like tamarins and marmosets.

Red-bellied lemurs rely on auditory communication over short ranges, producing nasal, low-frequency grunts to close-by receivers. These cues are identity markers that travel farther than scent but are short-lived to avoid unwanted attention by predators. Travel rarely occurs without vocalizing between group members. In a captive population of pair-bonded red-bellied lemurs at Duke Lemur Center, researchers found that sound signals were used most frequently within pairs, then scent signals, then tactile communication. However, these tactile signals were used over long periods of time, and the lemurs spent about 20% of their days in some form of physical contact with one another. Though communication preferences of wild-living red-bellied lemurs may deviate slightly from these findings, this study nonetheless suggests that engaging in tactile communication is an important behavior, and reinforcing cohesion through physical touch is considered a worthy social investment in this species.

Reproduction and Family
Mating is highly predictable and seasonal, occurring annually in May through June. The gestation period for offspring is roughly 120 days, with most births occurring in September through October. Adults do not mate until after offspring are fully weaned, and females typically give birth to one infant per year. The distinct periods of mating and infant care reduce infant mortality rates. In season, infants are still vulnerable to predation or falling from trees, but infants born out of season are markedly less likely to survive to weaning age. Infants receive most care from their mother in the first few weeks of life, but other group members are important contributors. The adult male (and presumed father) helps especially with parenting responsibilities, through grooming, holding, and playing. Males allogroom infants more frequently than adult females, holding the infant closely and using their toothcomb or hands to clean and smooth the infant’s thick fur.

Ecological Role
Madagascar hosts a mosaic of unique plants and animals, but the rainforest lacks traditional seed-dispersal vectors, such as rodents, ungulates, and large frugivorous birds that are found in other prominent rainforests. Instead, forest integrity relies on the activities of the abundant Malagasian primate species to promote plant growth. Frugivorous red-bellied lemurs consume both ripe and unripe fruits and pass viable seeds in their feces. For their small size, they prefer some of the largest fruits available in the rainforest. Once eaten, the large seeds contained within these fruits are not destroyed by mechanical or chemical digestive processes, emerging from the lemur’s digestive tract unscathed. Large seeds are excreted in individual units on the forest floor with a negligible amount of fruit or fecal matter attached. Approximately 80% of these seeds then germinate successfully. Other types of smaller seeds are passed in clumps and also have high successful germination rates.

Some scientists have hypothesized that during the red-bellied lemur’s nighttime foraging, they may also play an important role in pollinating flowering plants that only open in low-light conditions. While red-bellied lemurs typically consume flowers fully, they are also messy eaters. The pollen smeared on their faces and hands could theoretically be carried and transmitted to other plants.

Conservation Status and Threats
The International Union for Conservation of Nature lists the red-bellied lemur as Vulnerable (IUCN, 2018). While demographic distributions of this species is currently incomplete and the true number of wild-living red-bellied lemurs unknown, populations are uncommon, declining, and sparse. Deforestation threatens species survival significantly by isolating groups from each other and increasing the forest periphery. In peripheral forest areas with fewer trees, there is greater light exposure, higher temperatures, and reduced access to food. Unsurprisingly, red-bellied lemurs do not do well in these zones. Conservative estimates place the number of wild-living red-bellied lemurs today as 70% of the population size 24 years (three generations) ago. With intact family groups occupying precarious habitats and neighboring conspecifics located a hundred miles away, newly minted adults dispersing in search of a partner face bleak prospects. Maintaining viable populations is near-impossible, and declines are likely irreversible without urgent and systemic change in forest management and protection. These interventions are also necessary for the survival of all species on Madagascar, 90% of which are similarly forest-dependent.

Forest coverage maps are not available after the year 2000, but using other metrics, conservationists estimated that from 1953–2014, Madagascar lost 44% of its natural forest. Of the area remaining, over 46% is considered at or near the periphery. On average, Madagascar’s human population has been growing 2.8% annually. Much of the forest has been cleared as a result of slash-and-burn agriculture, illegal logging, and provisioning of wood-based fuel. A majority of Malagasy people (90%) depend on biomass to meet their energy needs. The rapidly increasing demand for fuel and food, as well as recent political instability in the area, makes conservation policies both untenable and difficult to enforce.

Red-bellied lemurs are killed by hunters and are sometimes taken in locally as pets. Hunting is very prominent in areas like Mantadia.

Conservation Efforts
Protected areas and designated conservation zones encompass a large proportion of Madagascar’s eastern rainforest. Even in these protected sites, populations of red-bellied lemurs are declining or have been extirpated. Population disappearance is not well accounted for or explained, as is the case with red-bellied lemur extirpation from the protected Vohibe forest fragment and the Andriantantely lowland forest. 

This species is listed in Appendix I of the Convention on International Trade in Endangered Species (CITES), meaning red-bellied lemurs are classified as most endangered, and commercial international trade is prohibited. However, species survival is threatened at a local level rather than an international level. International protections are unlikely to impact the survival status of red-bellied lemurs without involving targeted, locally based changes that negate hunting and destruction of habitat. Fortunately, there are a few initiatives that are using a community-based approach to tackle species preservation. The Aspinall Foundation recruits and funds Malagasy scientists, students, and local community members to survey lemur populations and study feeding habits and social dynamics. Other NGOs as well as the IUCN driven SOS Lemurs project are also working to obtain population data and grow sustainable engagement and practices in Malagasy communities.

References:

  • ​Dew, J. Lawrence, and Wright, Patricia. “Frugivory and Seed Dispersal by Four Species of Primates in Madagascar’s Eastern Rain Forest1.” Biotropica, vol. 30, no. 3, 1998, pp. 425–437.
  • Fleagle, John G. Primate Adaptation and Evolution. 3rd ed., Elsevier/Academic Press, 2013.
  • Jacobs, Rachel L, et al. “Parentage Complexity in Socially Monogamous Lemurs ( Eulemur Rubriventer ): Integrating Genetic and Observational Data.” American Journal of Primatology, vol. 80, no. 2, 2018, pp. e22738-n/a.
  • Lamb, Michael E, et al. “Paternal Behavior in Humans.” American Zoologist, vol. 25, no. 3, 1985, pp. 883–894.
  • Lukas, D, and Clutton-Brock, T. H. “The Evolution of Social Monogamy in Mammals.” Science (American Association for the Advancement of Science), vol. 341, no. 6145, 2013, pp. 526–530.
  • Overdorff, Deborah. “Preliminary Report on the Activity Cycle and Diet of the Red‐Bellied Lemur (Lemur Rubriventer) in Madagascar.” American Journal of Primatology, vol. 16, no. 2, 1988, pp. 143–153.
  •  Singletary, Britt, and Tecot, Stacey. “Signaling across the Senses: a Captive Case Study in Pair-Bonded Red-Bellied Lemurs (Eulemur Rubriventer) at the Duke Lemur Center, NC, USA.” Primates, vol. 60, no. 6, 2019, pp. 499–505.
  •  Smithsonian Institution, National Museum of Natural History, Department of Vertebrate Zoology, Division of Mammals. Data for specimen 63335. 
  • http://collections.mnh.si.edu/search/mammals/
  •  Tecot, Stacey R, and Baden, Andrea L. “Profiling Caregivers: Hormonal Variation Underlying Allomaternal Care in Wild Red-Bellied Lemurs, Eulemur Rubriventer.” Physiology & Behavior, vol. 193, no. Pt A, 2018, pp. 135–148.
  •  Tecot, Stacey R, and Romine, Natalie K. “Leading Ladies: Leadership of Group Movements in a Pair-Living, Co-Dominant, Monomorphic Primate Across Reproductive Stages and Fruit Availability Seasons.” American Journal of Primatology, vol. 74, no. 7, 2012, pp. 591–601.
  • Tilden, Christopher D. “A Study of Locomotor Behavior in a Captive Colony of Red‐Bellied Lemurs (Eulemur Rubriventer).” American Journal of Primatology, vol. 22, no. 2, 1990, pp. 87–100.
  •  Vieilledent, Ghislain, et al. “Combining Global Tree Cover Loss Data with Historical National Forest Cover Maps to Look at Six Decades of Deforestation and Forest Fragmentation in Madagascar.” Biological Conservation, vol. 222, 2018, pp. 189–197​

Written by Cookie Koch, December 2020