Howler Monkeys Part 4: References and Cited Works

I hope if you read this far in this four part series, that you enjoyed reading about one of the most enigmatic New World monkeys. Below is the list of works cited in the previous three parts, but I’m also going to include a few sources that are Internet accessible for those without quick access to the books and journal articles.

Internet Sources

Google Image Results for “howler monkey”

Wikipedia Entry for howler monkey. This link includes some images including the one used to show schizodactyly.

Honolulu Zoo Fact Sheet

The Loudest Animal In the World, an article by Terry Dunn hosted by the Smithsonian National Zoological Park website.

Cited References

Carpenter, C. R. (1934). A Field Study of the Behavior and Social Relations of Howling Monkeys. New York: AMS Press.

Fleagle, J. G. (1999). Primate Adaptation and Evolution, 2nd Ed.. San Diego, CA: Academic Press.

Gilbert, K. A., & Stouffer, P. C. (1989). Use of a ground water source by mantled howler monkeys (Alouatta palliata). Biotropica, 21(4), 380.

Kinzey, W. G. (1997). New World Primates: Ecology, Evolution, and Behavior. New York: Aldine De Gruyter.

Kitchen, D. M. (2004, 19/03). Alpha male black howler monkey responses to loud calls: Effect of numeric odds, male companion behavior and reproductive investment. Animal Behavior, 67, 125-139.

Milton, K. (1980). The Foraging Strategy of Howler Monkeys: A Study in Primate Economics. New York: Columbia University Press.

Pinto. Liliam P., & Setz, E. Z. (2004, December). Diet of Alouatta belzebul discolor in an Amazonian rain forest of Northern Mato Grosso State, Brazil. International Journal of Primatology, 25(6), 1197-1211.

Regan, B. C., Julliot, C., Simmen, B., Viénot, F., Charles-Dominique, P., & Mollon, J. (1998, November). Frugivory and colour vision in Alouatta seniculus, a trichromatic platyrrhine monkey. Vision Research, 38(21), 3321-3327.

Richard-Hansen, C., Vié, J.-C., & de Thoisy, B. (2000). Trnaslocation of red howler monkeys (Alouatta seniculus) in French Guiana. Biological Conservation, 93, 247-253.

Howler Monkeys Part 2: Dietary Needs and Habits

Howler Photo by princessangel

Milton’s Study on and Island in the Panama Canal

Milton studied two groups of mantled howlers on Barro Colorado Island in the Panama Canal (1980) and discovered that while howlers don’t have to pursue their foods, neither can they use a “sit and wait” strategy. Their preference for seasonal foods presents them with a continual problem of locating foods they like. Food location and monitoring was their main reason for travel and the alpha male in her study groups would initiate travel with a “low, almost inaudible, cough (p. 102).” The members of the troop would gather in one area of a tree and move out, single file, in a direction indicated by the alpha male. The troop’s travel through trees was in single file, which suggested to Milton a “goal-oriented” endeavor rather than a phalanx formation as with other primate species that would want to cover as much area as possible in their search for food. She also notes, however, that the single file is less risky because the relatively massive howler monkey is in danger of falling should it grab a branch that is brittle or dead, which breaks. The single file formation could be a method of providing a safe, proven route for the troop and the troop often used the same routes for other travel events, reinforcing this hypothesis.

Recharging the Batteries

In Milton’s study (1980), 90% of all travel events were followed by feeding events. She found that her observed groups traveled 1.23 mean hours per day at a mean distance of 443 meters at a mean rate of 360 meters per hour and she referred to howlers as “travel minimizers.” The howlers slept wherever they happened to find suitable spots at nightfall and at their last feeding location. While feeding, howlers generally orient themselves around 1 or 2 “pivotal” trees, moving to different pivotal trees once depleted.

Milton (1980) reported that, of the Howlers she observed during her Barro Colorado Island study, 91.4% of their feeding time was spent on seasonal foods: young leaves, fruits and flowers. They spent 1.6% of their feeding time on perennial foods or foliage that could be considered mature even though perennial foods were more abundant than seasonal and always available, showing a clear preference for specific foods. In a study along the Teles Pires River in Brazil (Pinto and Setz 2004), red-handed howlers (Alouatta belzebul discolor) were similarly observed to prefer seasonal fruits, leaves and flowers over perennial in which the howlers of the study spent 72-92% of their feeding time on the seasonal foods even though perennial were always available. Kinzey (1997) noted that howlers “are either folivore-frugivores or frugivore-folivores, depending on the population and season (p. 179).” He also indicated, as Milton did, that there are food preferences that influence the decisions of howler foraging strategies and that young leaves are preferred over mature but that there is clear exclusivity correlated to seasons, habitat, species and populations within species. At times, howlers prefer fruits or flowers over leaves, while during the same season but in different habitats, the same species might prefer leaves over fruit. Kinzey cites an unpublished dissertation that revealed the howlers of the study required 15.6% of their diet to consist of protein and that this is a driving force in their food choices.

Couch Potatoes?

The howler diet limits their activity and, indeed, dominates it. On average, howlers spend over 60% of their day resting and traveled mainly to locate or monitor food sources (Milton 1980). Howlers of the Barro Colorado (Milton 1980) and the Teles Pires (Pinto and Setz 2004) both preferred products of species of Ficus: leaves, fruits and flowers. However, they were also noted to feed on other species as well. Milton documented 87 leaf sources, 36 fruit sources, and 25 flower sources in her study of the mantled howler while the red-handed howlers in the Pinto and Setz study consumed leaves from 27 sources, fruits from 35 sources, and flowers from 8 sources. Milton observed to eat some leaf species only once, however, and hypothesized that the monkeys could have been sampling other leaf sources within their habitat and, perhaps, gauging them for palatability and nutritional value. She cited the specialized receptors in rats that can recognize potential nutrient-rich foods, sending information to the central nervous system and suggested that Alouatta may have a similar adaptive function. Howlers also appear able to detoxify secondary compounds in food sources, such as terpene, an unsaturated hydrocarbon found in plants. Other New World primates haven’t developed this function (Milton 1980).

See-Food Diet

Trichromatic primates, which include humans as well as Alouatta, have three specialized cones for color vision (Fleagle 1999, pp. 25-26). In a study of the red howler, in the rainforest of French Guiana, (Regan et al 1998), it was concluded that trichromacy in Alouatta allows howlers to locate and identify fruits among foliage from long distances. Regan et al admitted that, while their results were conclusive with regard to the ability of red howlers to consistently identify specific fruits and that specific fruits were optimally colored, they could not demonstrate whether trichromacy was an evolutionary adaptation to the fruit or whether the fruit colors were adapted to the trichromacy. The did, however, underscore the unknown cause of dichromacy among other Platyrrhines, where there are only two color cones rather than three, thus limiting the ability of dichromats to see certain colors effectively.

Washing it all down? Not for the Howler.

Howlers generally obtain water from their food (Carpenter 1934; Milton 1980; Kinzey 1997; Gilbert and Stouffer 1989), leaves and fruit can contain up to 95% water by weight or from arboreal sources following a rain where the monkeys lick their fingers after wetting them in the runoff (Carpenter 1934). Rarely, howlers have been observed coming to drink at standing ground water sources (Gilbert and Stouffer 1989; Carpenter 1934), but in a very cautious manner. The observation by Gilbert and Stouffer was that the monkeys left the trees one at a time to drink with a male, probably the alpha, standing watch. They hypothesized that the dry conditions of that year imposed a water stress that inhibited growth of new leaves, forcing the howlers to obtain water from other sources.

Howler Monkeys Part 3: Vocalizations

Howler Photo by JeanKearn

Perhaps the most familiar characteristic of the howler monkey are their vocalizations for which they are named. Howlers, both male and female, use their loud, lion-like roars (Fleagle 1999 p150) to advertise their presence and to warn or intimidate intruders (Kitchen 2004). Vocalizations may also provide auditory cues that reveal fighting ability of a group or an individual (Kitchen 2004). Vocal battles may culminate or result in actual physical combat in which an intruder makes an effort to usurp the group’s alpha male. Most howler troops consist of several adult males, but have a single alpha male that mates with the troop’s females, putting any dependent offspring in the alpha’s lineage. The immigrant male that forcibly replaces the group’s alpha can kill the dependent infants of the ousted alpha male (Fleagle 1999, p152; Kitchen 2004, p126). Infanticide of offspring under 9 months old hastens the female’s return to estrus, allowing the immigrant alpha male the opportunity to establish his own lineage according to data that is both circumstantial and observational (Kitchen 2004).

The Influence of Offspring

Kitchen discovered that the presence of small offspring had an influence on the alpha male’s vocal responses in that the alpha was quicker to begin howling, howled more often, and for longer periods when small offspring were present in the group. If the odds were against the alpha, howling was done only when small offspring were present, suggesting that an assessment was made by the monkey regarding the value of winning before escalating the conflict. Kitchen concluded that howling displays are costly with regard to energy, but the benefits outweigh the costs if intruders can be impeded. She also noted that males of small offspring stood their ground and, while did not advance upon aggressors, did not flee, indicating that stationary displays might be a compromise between fight and flight.

Keepin’ it on the ‘Down Low’

Kitchen also observed that howlers didn’t always respond to howling neighbors during natural encounters. This, she reasoned, could be due simply to conservation of energy since the howler’s diet limits activity. In general, howlers spend more than 60% of their day resting (Milton 1980; Kitchen 2004). Kitchen also suggested that the lack of vocal response could be a part of a strategy to remain hidden and quiet not only to conserve energy but to avoid facing superior opponents, which could, in turn, suggest that acoustic characteristics might be present in vocalizations which reveal fighting ability.

Loud calls occur most frequently at dawn and may serve the purpose of announcing a group’s location, establishing territory and distance between groups, and revealing a group’s actual composition. They can also serve the purpose of strengthening pair bonds between mates through “duets.” Vocalizations at night, however, occur at a higher rate than the day and calls have been measured to be as high as 90 dB and below 1 kHz (Kinzey 1997).

Conservation and Protection for the Howler

Howlers are reported to have been preyed on by both the harpy eagle and the jaguar (Kinzey 1997), but their most serious threat is, perhaps, habitat loss due to human activity. The construction of the Petit Saut hydroelectric dam in French Guiana flooded over 365 square kilometers of forest by 1995 destroying the natural habitats of many species, including that of the red howler (Richard-Hansen, Vié, and de Thoisy 2000). The red howlers in the inundated habitat were previously hunted to the point of serious reduction of population and the decision was made to translocate the remaining groups in the region to a new habitat. Though all but one of the translocated groups split up after being released in a new home range, the overall operation was considered a success since many of the distinctive behaviors of individuals within the groups were re-observed following the translocation. Richard-Hansen, Vié and de Thoisy (2000) demonstrated that such translocations were viable in situations of habitat destruction or other conservation needs exist.

Howler Monkeys Part 1: General Characteristics

 Afarensis has been doing his weekly “Know Your Primate” series, so I hope he won’t mind if I toss in my bit on the howler monkey. It was his series that inspired me and reminded me that I had this from a paper I wrote a while back. I’ll post this in two, maybe three, parts with references and I hope the information will be of value to students writing high school and college papers or for those who are simply fascinated by primates or howlers in particular. Please also feel free to comment on these posts as well!

Howler Photo by lemai13

Taxonomy and morphology

The howler monkey consists of six separate, allopatric species in the family Atelinae of the infraorder Platyrrhini: Alouatta seniculus (red howler), A. belzebul (black-and-red howler), A. fusca (brown howler), A. pigra (Mexican black howler), A. caraya (black howler), and A. palliata (mantled howler).

The Ateline genera also include woolly monkeys, spider monkeys, and the woolly spider monkey along with the howler. Atelines are the largest of the Platyrrhines and the largest average 10 kg. All Atelines have long, prehensile tails with friction ridges used in gripping tree branches during climbing and suspension. According to Fleagle (1999, p 150), Atelines exhibit similarities to extant apes with regard to many characteristics of their limb and trunk anatomy and suspensory behavior.

Of the Atelines, the howling monkeys (Alouatta) are the most distinct genus (Fleagle 1999 p150) and are often placed in a separate subfamily. Their distribution is wide-ranging from southern Mexico to northern Argentina. Their biomass ranges from 6 to 10 kg and color differences can be distinctive between and even within species. Fleagle notes that the colors range from red to brown and from black to blond (p150). Howler dentition includes small incisors and large, sexually dimorphic canines. The lower molars consist of a narrow tigonid section and a large talonid while the upper molars have four cusps with prominent shearing crests consistent with a foliverous diet.

The howler skull consists of a relatively small cranial capacity and a lack of cranial flexion. The mandible is large and deep and an enlarged hyoid bone creates a hollow resonating chamber where the howler’s characteristic vocalizations are produced. Post cranial characteristics include forelimbs and hind limbs that are similar in length, a long, prehensile tail, and schizodactyly caused by a poorly differentiated thumb, which facilitates grasping branches between the second and third digits, but precludes fine manipulation of objects (Fleagle 1999; Milton 1980; Kinzey 1997). The howler prehensile tail reduces the need for leaping or jumping, which have higher energy costs and provides the monkey with an additional appendage in distributing its weight during arboreal activity. The howler can also use the tail to suspend itself from branches to obtain otherwise inaccessible foods (Milton 1980).

Habitat

Howler habitat is varied because of the wide distribution of the six allopatric species and includes primary rain forests, montane forests, deciduous forests, secondary forests and llanos. They live at altitudes that range from sea level to 3200 meters and prefer the canopy levels of forests, though species in the dryer habitats regularly come to ground and cross open areas as they travel between patches of forest. Locomotion with howlers is generally slow and quadrapedal and they rarely leap. Howlers use suspensory locomotion, mostly climbing, during feeding and occasionally during travel (Fleagle 1999).

Social Behavior

Socially, howlers live mostly in groups of several adults of both males and females with dependent offspring. The size of the group varies dependent upon the productive value of the environment as well as the age of the group, and can range from 12 to 30 individuals as with A. palliata and smaller troops as with A. seniculus and A. caraya. Depending upon the group’s size, the howler home range can be between 10-50 acres and their day ranges are small at less than 100 meters. The home range is considered to be small for their biomass (Fleagle 1999, p. 150) and some can be as little as 3 to 15 acres depending upon species and habitat with up to 60% overlap between one or more groups (Kitchen 2004). Range needs are met more easily because of their ability to subsist on diversified food items which are very common such as leaves. Because of their small ranges, howlers travel little but spend long periods resting and digesting (Fleagle 1999; Milton 1980; Kinzey 1997).

Gorillas Get Sodium From Tree Bark

I remember my Primate Evolution class and the mention that Gorillas chew bark and spit it out. The hypothesis, according to my professor, was (if I remember correctly) possibly they do this for some nutrient they cannot get elsewhere.

As it turns out, new research has shown that decayed wood provides over 95% of the gorilla’s dietary sodium.

Sodium is important for the healthy functioning of living organisms, and is involved in muscle contractions, regulating blood pressure and maintaining water and acid-base balance, among other things.

Read more in this Livescience article.