Black Lemur

Eulemur macaco has two subspecies: Eulemur macaco macaco (E. macaco) and Eulemur macaco flavifrons (E. flavifrons) (Rabarivola et al., 1991). E. flavifrons is part of the Lemuridae family. The species has two common names: the blue-eyed black lemur and Sclater's lemur; but blue-eyed black lemur is more often used. The medium-sized, 2 Kg species (Schwitzer et al., 2007b) was first described in 1867, by Gray (Mittermieier et al., 2008) and shortly after it was described, it was lost for about 100 years. In 1985, the species was rediscovered (Volampeno et al., 2011a). This species of Eulemur is of interest because it is known to be one of the least-studied species in the genus (Volampeno et al., 2010). Endemic to the north-western part of Madagascar (Schwitzer et al. 2007b; Schwitzer et al. 2012; Volampeno et al., 2010), habitat destruction reduces the species’ success. Logging, slash-and-burn agriculture, forest fragmentation and erosion after deforestation are all forms of habitat destruction that affect the species. Hunting and trapping also reduce the species’ success (Schwitzer et al., 2012; Volampeno et al., 2010; Volampeno et al., 2013). These direct and indirect human effects have decreased the population size of the Eulemur flavifrons species, placing them on the list of critically endangered species (IUCN 2014).

The majority of E. flavifrons populations reside on the Sahamalaza Peninsula and adjacent land (Schwitzer et al., 2012 and Volampeno et al., 2013), in the primary and secondary forests (Schwitzer et al., 2012) of northwestern Madagascar (Schwitzer et al. 2007b; Schwitzer et al. 2012; Volampeno et al., 2010). A typical primary forest contains tall, densely packed trees with high species diversity whereas a secondary forest is typically much less densely forested as a result of logging, with less diversity (Schwitzer et al., 2007b). A 2700 Km² zone comprises most of the habitat of E. flavifrons. This zone includes the Radama National Park, a dry, deciduous forest within the Ankarafa Forest. Most individuals reside in the park (Schwitzer et al. 2012 and Volampeno et al., 2013). The species’ range is almost surrounded by waterways, including the Maevarano, Andranomalaza, and Sandrakota Rivers (Schwitzer et al., 2012). This distribution of E. flavifrons is the smallest among all Eulemur species (Volampeno et al., 2013).

E. flavifrons lives in fragmented areas of primary and secondary forest. Primary forest contains more densely packed trees and less human disturbance, whereas secondary forest is less dense and has had more human disturbance, such as logging (Schwitzer et al., 2007b). The primary forest fragments have many benefits for E. flavifrons. The many trees that have been left undisturbed in the primary forests are often very tall, about 10-15 m. This allows E. flavifrons to spend a large portion of their day at high elevations in the trees, especially when they are sleeping and eating (Schwitzer et al., 2007b). Likewise, tall, old trees are often unaffected by storms and high winds on the island (Volampeno et al., 2013). Also, a higher diversity of trees in primary forests allows for more food diversity for feeding and more choices for sleeping trees (Schwitzer et al., 2007b). When species move within the primary forests, there are many options to choose from for food and shelter because there is so much variety (Volampeno et al., 2013).

Tree density also plays a large role in E. flavifrons habitat preferences (Seiler et al., 2013). When tree density is higher, there tend to be more individuals. This correlation may arise because trees provide refuge from predators as well as increased food availability (Seiler et al., 2013). A study by Schwitzer et al. (2012) showed that the secondary forest fragments have fewer individuals, supporting the idea that greater tree density in primary forests plays a large role in habitat selection by E. flavifrons (Schwitzer et al., 2010 and Schwitzer et al., 2012). As E. flavifrons prefers primary forests over secondary forests, they are vulnerable to the destruction of the primary forests (Schwitzer et al., 2007b, Seiler et al., 2013, & Volampeno et al., 2013).

E. flavifrons individuals tend to travel to areas where there is more food, which can be difficult in Madagascar because there are both dry and wet seasons (Randriatahina and Roeder, 2013). The wet season, which is the summer season, falls from December to March. The rainfall during this time is very unpredictable, and includes serious storms and monsoon winds. The rain contributes to a plentiful food supply during the wet season (Volampeno et al., 2011a). In contrast, the dry season contributes to a food shortage from the months of May to September, the winter season, which can be very windy (Volampeno et al., 2011).

E. flavifrons has the shortest distance between lemurs, meaning that they live in a small range of habitat compared to other species. One study of lemur populations surrounding Radama National Park, a dry deciduous foreset, found 29 different groups (about 8 individuals per group), and 228 individuals total, with 97.3 lemurs per Km². The population was shown to be greater on the inside of the park compared to the outside of the park (Volampeno et al., 2010). This indicates that the lemurs tend to reside inside the national park, where they are safer from human interference.

The two subspecies of Eulemur macaco, E. flavifrons and E. macaco, may share a common habitat hybrid zone, as determined by an ecological niche model, based on climate and type of forest. Both of the species could potentially survive in this habitat hybrid zone. However, the actual habitat locations of the populations for both species do not overlap with each other at this time (Blair et al., 2013).

E. flavifrons is known to have a bi-modal activity pattern, where they are active during both the day and night, with most activity occurring at dusk and dawn (Schwitzer et al., 2012 & Schwitzer et al., 2007a). This activity pattern makes the species cathemeral, which means they distribute their activity over the 24-hour day (Schwitzer et al., 2007a). They are known to forage and feed for about 32% of their day (Goodchild and Schwitzer), which is necessary due to their previously discussed, low-energy diet (Goodchild and Schwitzer, 2008; Volampeno et al., 2011a). A study by Schwitzer et al. (2012) showed that the lemurs’ total daily activity was higher in the secondary forest fragments compared to the primary forest fragments (Schwitzer et al., 2012), which could be due to lower food availability and wider home ranges in the secondary forests. It is also known that during the windy winter season in Madagascar, E. flavifrons has decreased activity on the ground and increased residence in the high trees. In the dry, summer season, the lemurs have an increased activity overall, because they must migrate in search of food (Schwitzer et al., 2007a). Females are known to be dominant in E. flavifrons populations (Digby and Kahlenberg, 2002; Archie and Digby, 1999). When the sexes interact, Digby and Kahlenberg (2002) showed that 99% of the interactions led to the males being subordinate and submissive to the females. The females would use aggression in order to control the males’ actions. All of their seven test groups showed the same results. The females were also aggressive at more times of day than just feeding time, suggesting that they show dominance over all types of interactions (Digby and Kahlenberg, 2002). Juvenile dominance is also present in this species. A study collected data for male offspring that were born to a dominant female and a female offspring that were born to a subordinate female. The study looked at the interactions between the juveniles and other individuals in the population. They found that maternal rank determined whether the juvenile would be dominant in conflicts. Offspring born to the dominant female had a dominant adult to help them in altercations, which made them dominant over others. They reached this conclusion because the juvenile female born to the subordinate mother was more submissive to other individuals in the group compared to the juvenile males with dominant mothers (Archie and Digby, 1999). Behavior between groups is interesting for this species. Each group is composed of about 8 individuals, sometimes a few more or a few less (Randriatahina and Roeder, 2013 & Volampeno et al., 2010). These populations are very stable, with no more than 3 adult females and 2-5 males in one group at a time. Encounters between groups occur at feeding and resting sites, with each group remaining intact, without switching or wandering into another group. Females act antagonistically toward other groups, exerting their dominance (Randriatahina and Roeder, 2013). More research needs to be done in this area to determine if the females limit populations of lemurs from feeding and migrating. If some populations or individuals are not thriving because of females, then management of the populations could include food distribution to see that all individuals are able to eat. E. flavifrons was included in a study of cognitive ability and the similarity between 3 lemur species, old world monkeys, and humans. The study showed that there is conservation among the primate order of the approximate number system, which was used to indicate cognitive ability. The study mentioned that lemurs do not demonstrate deception, or advanced visual communication, or coalition within groups. However, lemurs are capable of transitive learning (understanding that if A>B and B>C, then A<C; Bryson and Leong, 2007), object displacement, and learning contingency (stimulus-based, associative behaviors similar to Pavlovian conditioning; Penn and Povinelli, 2007) when participating in a food-rewarding task (Jones et al., 2012). This study relates to their small group size and feeding habits, indicating that they understand the numerical availability of food (Randriatahina and Roeder, 2013 & Volampeno et al., 2010).

The life span for E. flavifrons is about 27 years (Volampeno et al., 2011b), and the oldest individual at this time is 21 years old (Volsampeno et al., 2011b).

As of June 2007, the species habitat was protected in some areas, including the Sahamalaza Peninsula and some surrounding forested areas in the north and the east. Being a UNESCO Biosphere Reserve, the Sahamalaza Peninsula also gives extra protection to the lemurs. There is also a chain of European zoos that are trying to conserve lemur populations by improving and protecting the lemur habitat that is left. A field station in Sahamalaza is also maintained by the group of European zoos, and it is dedicated to current research on lemurs and conservation of the remaining populations (Schwitzer et al., 2012).

Often, parasite levels are used to define stress levels of populations. E. flavifrons was determined to have intestinal parasites in the primary forest fragments and a higher number in the secondary forest fragments. These parasites did not indicate adverse effects on the health of the species, but the higher intestinal parasites in the lemurs that occupied the older, secondary forests could indicate that the environment in the secondary forests is less appropriate for this species (Schwitzer et al., 2012). Forest fragments can be selected for protection based on lemur parasite load. Forest fragments with many parasites can also indicate which populations of the species are especially in need of management (Schwitzer et al., 2012).

As primary forests have been shown to have the highest occupancy of this species, they should be a priority for protection (Schweitzer et al., 2007b). The use of secondary forests as buffer zones and corridors between primary forests would create an ideal dispersal/migration environment for the lemurs. The protection of trees is also a good mechanism to save the lemurs so they will be able to find protection and food (Volampeno et al., 2013). If more research shows that particular primary or secondary fragments of land are more valuable than others, those areas of the habitat should be first priorities for protection and management.

In order to learn more about the species, there needs to be long-term studies in the secondary forests that Eulemur flavifrons occupies (Schwitzer et al., 2007b). If some individuals are kept in captivity, they can be used to appropriately contribute to reintroduction and reinforcement projects (Schwitzer et al., 2013). However, it has been determined that holding lemurs in captivity is not the best option for conservation because they become obese in captive environments, which threatens their health (Goodchild and Schwitzer, 2008). If individuals are to be held captive for research and observation, a proper diet is necessary in order to avoid obesity.

More research is necessary to determine the correct ways in which lemurs need to be managed and conserved. It would be ideal to create a buffer zone around their geographic range to decrease human destruction of their already-fragmented habitat.

E. flavifrons is forced to relocate in order to find food at different times of the year. For example, during the dry season, the food and water shortages causes individuals to travel between primary and secondary forests and between different primary forests in search of food (Volampeno et al., 2011a). During the wet season, however, food is very plentiful. The fruiting trees meet the needs of the lemurs and they will remain in or travel to primary forest fragments to have a more widespread selection of trees to sleep and eat in (Volampeno et al., 2011a).

E. flavifrons could benefit from more research in this area. If the migration of the species for food is causing them to be more vulnerable to threats, then there could be preventative measures taken in order to decrease the need for movement and/or create a way to move between areas safely.

The molecular difference between E. flavifrons and E. macaco is about 70 base-pairs. According to a genetic analysis, subpopulations of E. flavifrons have been shown to not have a significant difference in their DNA (Fausser et al., 2000). This means that the existing genetic diversity within E. flavifrons is minimal, so it needs to be conserved. This is especially true because E. flavifrons, as of 2000, was not included in many reserves like E. macaco was (Fausser et al., 2000).

E. flavifrons is distinguishable from its close genetic relative, E. macaco by its beard, sideburns (Ravarivola et al., 1991), non-tufted ears, and grey-blue eyes (Mittermeier et al., 2008, Rabarivola et al., 1991, Volampeno et al., 2011a). There is also a missing flexion-fold in the palm of E. flavifrons when compared to E. macaco (Rabarivola et al., 1991). E. flavifrons females tend to have a white forehead and lighter fur color than E. macaco (Mittermeier et al., 2008). Females and males experience sexual dichromatism, similar to all but one species of lemur (Mittermeier et al., 2008 and Volampeno et al., 2011b). To have sexual dichromatism, females and males must differ in color. In E. flavifrons, females are reddish-orange whereas males are entirely black (Volampeno et al., 2011b), though they are both medium-sized (2 Kg; Schwitzer et al., 2007b).

E. flavifrons has a flexible visual system that functions in both dim and bright light, confirming that they have both rods and cones within the retina of the eye. More active lemurs have higher visual acuity (Veilleux and Kirk, 2009). E. macaco does not have acute color vision, as it is a prosimian, a primate. This feature is indicated by the way in which the species chooses its foods; bright-colored fruits are not more appealing than dull-colored fruits (Birkinshaw, 2001). These findings are likely applicable to E. flavifrons as it is a subspecies of E. macaco, and also a prosimian.

It is documented that this species of lemur has the smallest population remaining within the genus. There are about 450-2,300 individuals total, with 24 individuals per km² as the mean density in 8 different forest fragments. In the Ankarafa forest, there are about 97 individuals per km² (Schwitzer et al., 2012). The captive population contained 75 individuals as of 2013 (Schwitzer et al., 2013).

E. flavifrons individuals mate and give birth during the dry season, in which there is decreased food availability. Mating and birth may prevent individuals from foraging and moving in order to find food. This is a problem because less food is available close to home during the dry season, and more traveling is needed to find food (Volampeno et al., 2011a; Volampeno et al., 2011b; Volampeno et al., 2013).

At three years of age, females mate and give birth for the first time (Volampeno et al., 2011b). Before mating season, males migrate toward females. After male migration, there is a male-biased sex ratio which may ensure that the females’ fitness will be higher (Randriatahina and Roeder, 2013). After mating occurs, females disperse throughout the habitat from August to September, which is within the birthing season. Gestation lasts approximately 120 days (Volampeno et al., 2011b), and births occur at the end of August to the end of October, during the dry season (Schwitzer et al., 2012 & Volampeno et al., 2011b). Presumably, in order to avoid predators and excessive attention from group members, females have their babies nocturnally.Many infants are killed by predation, mostly at the time of birth (Volampeno et al., 2011b).

A baby lemur is dependent on its mother until it is 4 weeks old. Afterwards, they can move objects and travel short distances. Mothers need food in order to feed the infants, especially because they are lactating. Birth in the dry season complicates the search for food, as it requires a lot more energy, so instead, the females will rest when they are caring for their baby, instead of traveling far for food, to save energy (Volampeno et al., 2011b). Babies start to explore their environment when they are about 7 weeks old, and are independent at 10 weeks old (Schwitzer et al., 2012; Volampeno et al., 2011b). Females care for their infants by feeding and grooming them until the baby is old enough to do so on its own (Archie and Digby 1999; Volampeno et al., 2011b).

The largest threats to the Eulemur flavifrons population are due to human activities. Humans cause forest destruction and fragmentation, which is usually owed to slash-and-burn agriculture and logging. Trapping and hunting are also a problem (Schwitzer et al., 2012). Currently, 80-90% of the forests that used to exist on Madagascar have been destroyed (Volampeno et al., 2010). A major cause of the destruction of these forests is erosion of the land after logging (Volampeno et al., 2010). There has been a decrease in forest cover from 12.5% to 2.8% in a 40-year time span inside the primary forests, where the lemurs tend to be found more frequently (Volampeno et al., 2013). This reduction in cover means that the lemurs will be more likely to be preyed upon because they are unable to find coverage during sleeping and eating. Since the primary forest fragments are considered the more favorable environment for the species due to the species richness of the fragments, including the presence of fruiting trees and trees for sleeping, human involvement and damage in this ecosystem will reduce the survival of lemur individuals (Schwitzer et al., 2007b).

E. flavifrons has a diet that mostly consists of fruits, leaves, and flowers (Goodchild and Schwitzer, 2008; Schwitzer et al., 2007b; Volampeno et al., 2011a). In a one-year study, they ate approximately 72 species of plants in the wild. About half of their diet was fruits and the other half was leaves and flowers (Schwitzer, 2012). Volampeno et al. (2012) confirmed that during the wet season, fruit was a large part of the lemurs’ diets, with Magnifer indica as the most-consumed species, aiding in the dispersal of its seeds (Volampeno et al., 2012). Given that E. flavifrons mainly eats fruits and leaves, it seems to be able to survive on a low-energy diet, with a basal metabolic rate that is about 50% lower than most other placental mammals of the same size (Goodchild and Schwitzer, 2008; Volampeno et al., 2011a). E. flavifrons has also been shown to eat small amounts of insects, plant exudates, and fungi (Schwitzer, 2012).

During the day and night, E. flavifrons individuals have to protect themselves from potential predators such as hawks, buzzards, and tree boas. Coverage by trees is essential to protect the lemurs from being preyed upon (Seiler et al., 2013).