Natural History of the Mantled Howler Monkey (Alouatta palliata)
by Iris Broekema, November 2002
An adult female howler monkey (Alouatta palliata)
Alouatta palliata is listed in CITES (Convention on International Trade in Endangered Species of Wild Flora and Fauna) Appendix 1 (CITES 2002a). Appendix I includes all species threatened with extinction which are or may be affected by trade. Trade in specimens of these species must be subject to particularly strict regulation in order not to endanger further their survival and must only be authorized in exceptional circumstances (CITES 2002b).
lower risk status according to the Convention of International Trade in Endangered Species (CITES) guidelines.
Countries of existence
Alouatta palliata exist through southern Mexico, southern Guatemala, and south through the rest of Central America to the west coast of Colombia and Ecuador. (Smuts, 1987).
Mantled howlers are black except from a fringe of long, gold to buff hairs on the sides. The tail is prehensile; the tail is able to grasp by wrapping around; often refers to the tail of some larger Neotropical monkeys. When males reach adulthood, the scrotum turns white. In females the color of the genital area changes from white to pink during estrus. (Rowe, 1996).
Table 1: Physical characteristics shows the values of the different parameters for physical characteristics.
Table 1: Physical characteristics
|Head and body length||
Males: 508-675mm (Rowe, 1996). Females: 481-632mm (Rowe, 1996)
Males: 545-605mm (Rowe, 1996). Females:563-655mm (Rowe, 1996)
Males: 4.5-9.8kg (Rowe, 1996). Females: 3.1-7.6kg (Rowe, 1996)
98 (Rowe, 1996)
|Adult brain weight||
55.1kg (Rowe, 1996) The hyoid bone is smaller than in other howlers (Rowe, 1996).
Alouatta palliata, is arboreal, which means adapted to life in trees. They use all forest levels, but most frequently the upper canopy and emergents. (Mittermeier, 1988). The upper third of the canopy is preferred. Mantled howlers live in evergreen rain forest, cloud forest, dry lowland deciduous forest, and coastal mangrove forest up to 2000m. (Rowe, 1996). They routinely cross open areas between forests. Howlers can also swim. (Mittermeier, 1988).
Mantled howlers eat mature and young leaves, petioles, pulvini, buds, flowers, fruits, seeds, stems and twigs. Fruit is known to comprise up to 95% of the diet of the species at certain times of the year. Throughout the year, they spend an equal proportion of time consuming leaves and fruits, with young leaves and mature fruits contributing 39% and 41% of their feeding time. (Mittermeier, 1988). Leaves are the principal source of protein and fruits the principal source of easy energy and of protein. There is evidence that howler prefer to eat both leaves and fruit (and/or flowers) each day, presumably to get the required balance of energy and other nutrients. (Milton, 1980). Howlers' daily food choice leads to a balance between foods which are rich in protein and those rich in digestible carbohydrates. (Mittermeier, 1988). The seasonal foods howlers prefer, are generally of a relatively high nutritional quality. The protein/fiber ratio seems to be the most important factor in determining howler leaf choices. (Milton, 1980). Young leaves the principal dietary item during the second half of the wet season, and in the dry season, contribute up to 90% of the total feeding time. Mature leaves are eaten throughout the year, but contribute least to the diet during the first half of the wet season when ripe fruit was the main food type eaten. Young fruit contributed 8.5%, mature leaves 10%, and flowers only 0.2% of the total feeding time. Young leaves eaten by howlers are richer in protein content per dry weight, contain a higher proportion of digestible nutrients, more digestible energy and less fiber than mature leaves. The diet consisted of 9.6% protids, 3.2% lipids, 21.7% reducing glucids, 13.6% cellulose, and 51.9% complimentary fractions. Mantled howlers spent 19.4% of their feeding time eating mature leaves, 44.2% eating new leaves, 12.5% eating fruits, 18.2% eating flowers, and 5.7% eating petioles and pulvini. (Mittermeier, 1988).
Howlers eat foods from a great number of different species, a minimum of 109 in the overall sample, and 7 to 8 on a daily basis. There is a high turnover in the species used as food sources. Leaf species have a much higher turnover rate than fruit species, and flower species even higher. These differences correlate with the supply and duration of the three food categories on individual plants The monthly turnover in food species is even higher than the daily rate. A few food species are used rather heavily (more than 10 percent of the overall feeding time), but most were used hardly at all. There is a daily pattern of having 1 or 2 primary food sources (20 percent or more of feeding time) and 5 to 6 secondary sources. The primary sources changed from month to month. (Milton, 1980).
Seasonal differences have been reported. The mature leaf use is higher in the wet season and lower in the dry season. Howlers ingest fewer mature leaves as more new leaves and flowers are eaten and new leaf use decrease as fruit use increase. Rainfall influences the availability of fruit and flowers but not new leaves. Both flowers and fruits provided easily digestible carbohydrates, but neither are eaten all year since each is only seasonally available. The amount of time spent feeding on flowers and fruits increases or decreases as a function of their availability. (Mittermeier, 1988).
Alouatta have long colons and a slow passage rate of food through the get to permit sufficient fermentation by cellulolytic microorganisms. Fermentation end products are believed to be important sources of energy during times when fruit availability is low. The standard metabolism if Alouatta is similar to other mammals of the same body mass. Adaptations to leaf-eating in this genus are mainly behavioral. These behavioral adaptations include a selective diet, preferably a mixture of fruit and immature leaves, using a wide range of species which are not necessarily the most common ones in the group's home range and ranging, and activity patterns which optimize their use of these resources. (Mittermeier, 1988).
The latter part of the pregnancy can increase nutritional requirements by some 25 percent, while lactation can increase them by 50 percent. For this reason, female howlers often have a harder time meeting their energy requirements than males. (Milton, 1980).
Howling monkeys obtain their water either from their food or by licking rain from leaves or themselves. Howlers have been reported to drink from arboreal reservoirs. (Mittermeier, 1988).
Table 2: Life development shows the values of the different parameters to indicate the live development of Alouatta palliata.
Table 2: Life development
|Infant||0-6 months (Rowe, 1996)|
|Juvenile||6-20 months (Rowe, 1996)|
30-48 months (Rowe, 1996)
|Weaning||21 months (Rowe, 1996)|
Males: 42 months (Rowe, 1996). Females: 36 months (Rowe, 1996)
|Estrus cycle||11-24 days (Rowe, 1996)|
180-194 days (Rowe, 1996)
|Age of first birth||
48 months (Rowe, 1996)
22.5 months (Rowe, 1996)
|Life span||20 years (Rowe, 1996)|
Dominant males have ‘priority access to estrous females (Rowe, 1996). Births are more frequent in late December and January, as opposed to April or May. Births are scattered during some years and clumped in others. (Mittermeier, 1988). Births sometimes occur in clusters, that are not sufficiently predictable to warrant labeling seasonal peaks. (Smuts, 1987).
Mothers handle and lick presumably just-born infants, who actively climb up their ventrums. Females become less aggressive and drop in dominance during the week prior the parturition, and new mothers continue to avoid confrontations after birth. Infants are carried by their mothers, but cases have been reported that adult and immature palliata carried infants. Newborns are relatively immobile; their tails, which later play such an important role in locomotion and suspension, tend to dangle in nonfunctional corkscrews. At first, the infant's tail is so short that when it is carries well forward on his mother's ventrum, and cannot be employed in any case in the classic wrap-around-the-base of its mother's tail which it uses later. The tail tip begins to be appropriately used at about one and one-half to two months of age. The classic dorsal riding position involves the infant mounted on the lumbar-dorsal section of its mother's back with its tail wrapped around her tail root. Mantled howlers leave their mother after 15 to 66 days. Thereafter, the infant's independence and its degree of interaction with other monkeys increases rapidly. During the first four months the infant is rarely more than two meters from its mother. The frequency and duration of nursing did not decline through the ninth month. Even through an infant begins eating solid foods as early as the second month. (Mittermeier, 1988).
Males reportedly mother infants by carrying them. More females than male infants survive to the age of one year. Infanticide is the cause of 40% of infant mortality. Infants are often killed after a new male takes over a group. Other females attracted to an infant may often prevent a new mother from feeding and sleeping. (Rowe, 1996).
Locomotion of mantled howlers consists of quadrupedal (using four limbs for locomotion), walking and climbing. They use suspensory feeding; hanging, climbing or moving below tree branches. (Rowe, 1996). Palliata is most frequently active on small, flexible, nearly horizontal supports the periphery of tree crowns. Howlers walk 70% of their time during locomotion, with the weight being supported by diagonally opposite limbs. Dropping or leaping are about equally frequent. Feeding postures are usually suspensory using various combinations of limbs and tail involving a number of anatomical traits which had been suggested as related to brachiation or forearm suspension. Large males were more likely to use large supports. Resting was the predominant activity and was most often done in a sitting or lying posture. Quadrupedal walking and running was the most frequently used way of locomotion, even on branches only a few centimeters thick. Arm swinging and upside-down quadrupedalism are used occasionally, the latter especially during play, but never brachiation (swinging with arms from one branch to another (Mittermeier, 1988, Rowe, 1996).
The category climbing is subdivided into quadrupedal ascent and descent, horizontal climbing, bridging, supported bidepal walking and lowering extremity of a support and adopting a suspensory posture at the tip; frequently to obtain a food item. Lowering is very rare and supported bipedal walking has never seen. (Mittermeier, 1988).
Howlers on the ground appear relatively awkward. the fingers are loosely spread in front of them, their elbow and knee joints remain slightly flexed, and they are relatively slow. However, they can outrun a human. Despite the dangers of being on the ground, they may cover relatively long distances between food trees, and gain access to a water source. (Mittermeier, 1988).
Palliata feeds by grabbing a branch about 30cm from its tip and bend it back to bring fruit, leaves, buds or flowers close to their mouth and pick the food with their lips or teeth. the food is manipulated in the mouth, usually without the aid of hands, and may be rejected by spitting it out of the mouth. (Mittermeier, 1988).
The prehensile tail of howlers appears to serve a dual function to reduce locomotor costs and to increase the efficiency of food harvesting. In traveling, by using the prehensile tail as an additional appendage, the howler is able to distribute its weight over a greater number of supports, including supports too far distant to be reached with either the arms or the legs. This enables howlers to use arboreal routes which could not otherwise support their weight and thus to reduce travel costs by opening more potential routes to food sources. Further, by using the long prehensile tail in locomotion to maintain a gripe on terminal branches when crossing between trees, howlers may reduce the need for leaping and other strenuous activities that would increase locomotor costs. In feeding, the prehensile tail enables howlers to hang below branches and harvest food items otherwise inaccessible. Tail-hanging can increase the size of an animal's feeding sphere by as much as 150 percent over sitting or standing postures and hence greatly increase harvesting efficiency. (Milton, 1980).
Alouatta palliata form multimale-multifemale groups. Females form a hierarchy in which the youngest adult is the most dominant, although it may have less reproductive success than the older females. The females of middle rank have the greatest reproductive success. The tenure of the alpha male is 2.5-3 years, during which time he may sire 18 offspring, or more than two times the average female’s offspring. It is to a female’s reproductive advantage to have male offspring during periods of social instability or drought and female infants during stable periods with sufficient food. Mantled howlers do not maintain exclusive territories; overlap is up to 100%. They defend the place where they are, rather than an exclusive area. (Rowe, 1996). Different parameters can be used to determine the social structure of mantled howler monkeys. Emigration, group size, population density, home range, day range, and sleeping sites are described below.
Both genders emigrate as juveniles of subadults. (Rowe, 1996). Males, and less frequently females, disperse, including juveniles, and more frequently, subadults and adults disperse. Group transfer patterns are sometimes complex, with males for example, invading and leaving groups successively. The progress can be prolonged that whereas males tended to come and go from a group for several months prior to emigration, females tended to leave abruptly. (Mittermeier, 1988).
4.2-21 (in 12 different studies). (Rowe, 1996).
26-31 individuals/sq.km. (Mittermeier, 1988).
The home range of howlers is 9.9-60ha. (Rowe, 1996). Howler monkeys are not so much territorial, but rather antagonistic towards conspecifics not of their own group. They defend the place they are. (Mittermeier, 1988). Studied troops of howler monkeys used their supplying areas very selectively, using about 40 percent of the total area and heavily using only several hectares. The areas used more heavily than others appeared to have higher densities of preferred food species. (Milton, 1980).
In the dry season, the daily path length; the total distance traveled, has an average exceeding 200m/day, with some days over 1000m. Day ranges varying from 46 to 830m, with an average of ca 180m for the group, during the dry season. The mean travel rate is 360m per hour, and a mean travel distance of 443m per day. (Mittermeier, 1988).
Howlers appear to use the horizontal branches of medium to large-sized trees, often ones in which they have been foraging. They sleep singly or in small groupings, with occasional shifts of location during the night. (Mittermeier, 1988).
Alouatta palliata are diurnal (active during the day) and arboreal (adapted to live in trees). Mantled howlers will occasionally travel on the ground, where they can outrun a human. They can also swim. Anna, the female in the picture at the top of this page, swam back from bohio island to the dock on Isla Tigre to return to her human caretakers. They are subject to high levels of botfly larvae infestation in May-October, which may increase adult and infant mortality. All age groups have been reported to fall out of trees (Rowe, 1996). One of our female howlers broke her left femur during a fall. Several parameters for behavior, including activity pattern, relationship among Alouatta palliata, communication, and relationships among other animals are discussed below.
Alouatta delays for long periods in suitable trees. In the driest and sunniest month, a very district feeding bout during the first few hours after dawn and another, less district, in the late afternoon is reported. Resting peaked at midday. In rainier July and August, the frequencies tended to smooth out, with feeding perhaps showing three peaks: shortly after dawn, late morning, and late afternoon. Activity was depressed during rainfall and also during periods of intense sun. The most intensive foraging is soon after awakening, during which time movement in the general area of the sleeping tree may occur. However, a nap will often follow, and later around midday there will be two naps in the rainy season, and one in the dry season. (Mittermeier, 1988). Mantled howlers are travel minimizers, energetically constrained because the foliage part of their diet is low in ready energy. (Smuts, 1987). They minimize travel and thereby minimizing the cost of foraging. Because of the patchy distribution of howlers' food in both space and time, it is expected that howlers would be goal-directed in their travel, and very selective in their use of supplying area. (Milton, 1980). Activities may occur any time throughout the day. Resting takes at least 74% of the daytime, searching for and consuming food 15 to 22%, and engaging in social activities only 4%. (Mittermeier, 1988). Howlers also show little activity at night. (Smuts, 1987).
Seasonal changes in activity patterns occur. Howlers spend progressively more time feeding and less time resting during a typical day in the wet season. Groups tended to arrive at their sleeping tree later in the day and remain active for longer in the dry season. (Mittermeier, 1988). More time was spent feeding during the transition season than in the wet and dry season. This may be related to the greater proportion of leaves in the diet during the transition season, the time of lowest overall production of seasonal foods. (Milton, 1980).
Relationship among Alouatta palliata
Howling monkeys appear strikingly docile in their intragroup behavior. Females form a hierarchy in which rank correlates negatively with age; a rare type of social system for primates. All adult females are subordinate to adult males. Palliata groups form a hierarchy in which rank correlates negatively with age, which is a rare type of social system for primates. The maintenance of this hierarchy is evidently achieved through subtle behaviors and rarely through overt aggression. A few aggressive interactions have been reported. (Mittermeier, 1988).
Palliata very rarely groom. (Mittermeier, 1988). Less than 2% of a howler's daytime is spent on grooming others, and bout durations average only about one minute. Most allogrooming is performed by females, especially adults, and the principal recipients are the females' own infants or adult males. Grooming by adult and immature males is very rare. (Smuts, 1987). Dominants usually groom subordinates. (Mittermeier, 1988). Mothers give infants little grooming. (Rowe, 1996).
Mantled howler groups tend to avoid each other. Dawn calls are somehow used in this avoidance. (Smuts, 1987).
Mantled howlers scent-mark by rubbing their throats and other parts of their body on branches. Urine washing is reported by palliata, which was performed more by adults than immatures and particularly often by adult males during social stress. Feces could also be involved to indicate that the accumulation of excrement may be important in denoting sleeping sites. The various rubbing activities, carried out predominantly by adults, are undoubtedly important in olfactory communication; frequently involving the distribution of urine and also, in the case of throat rubbing, scent glands. The motivations for these behaviors are evidently multiple and probably include aggression, dominance assertion and sexual relations. (Mittermeier, 1988).
Throat-rubbing is performed in both inter-and intragroup hostile interactions. Both males and females roar. (Mittermeier, 1988). The long-distance territorial roar is produced mostly when exhaling. Infants have a play vocalization. (Rowe, 1996). The female calls are softer than those of adult males, and especially in palliata, they are higher pitched. Both males and females rubbed equally on the approach of males, but females rubbed more than males on the approach of females. Roaring by troop females is directed at solitary females, and indicates that the function is probably similar to that for a male roaring. Roaring between group females may also occur as a means of preventing access to the dominant male, and simultaneous roaring with males is important in strengthening the pair bond. Females roar with males with whom they had recently mated and with the father of their infant, even if he is not the dominant male. The preponderance of howling is mostly around dawn, or during the hour after sunrise, but can often be heard at other times during the day, and even at night. Howling seems to be important in maintaining a distance between the groups and influenced the daily panning patterns of each. Howling of another group or solitary individual increased the probability of howling. Close groups may even approach each other. (Mittermeier, 1988).
Relationships among other animals
Healthy adult howlers in trees are probably only threatened by Felidae, large Mustelidae, and snakes among the non-human predators. Young howlers, however, could potentially be carried off by large birds. Interactions with other animals are rare. (Mittermeier, 1988).
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