Black Howler Monkey Alouatta Pigra

1. Black Howler MonkeyAlouatta Pigra Stephanie Larocque Joseph Leung Daniel Tremblay-Sher Myriam Tremblay-Sher Diana Yin http://www.cs.mcgill.ca/~dtremb8/apigra.ppt

2. Taxonomy Primates Haplorrhini Strepsirrhini Simiiforms Tarsiiforms Catarrhini Platyrrhini Aotidae Atelidae Cebidae Pitheciidae Alouattinae Atelinae Alouatta

3. Species Description • Alouatta genus is defined in large part by characteristic howling, hence the common name Howler. • Several species exist in Central America including: • A. belzebul, A. caraya, A. coibensis, A. paliatta, A. pigra, A. sara, A. seniculus. • Until 1970, A. pigra was considered a subspecies of A. paliatta, but enough distinctive traits warrant its reclassification as a seperate species.

4. Species DescriptionGeographical Distribution

5. Species DescriptionGeographical Distribution • Central America: • Yucatan Peninsula, Mexico • Guatemala • Belize • Tropical evergreen, semi-evergreen forest • Altitudes below 400m. • Riverine areas with seasonal flooding

6. Species DescriptionPhysical Characteristics • Prehensile Tail • Weight: 6-8kg • Length: ~60cm + 80cm tail • Coat: Black fur with traces of brown on shoulders, cheeks, and back. Distinctive white scrotum by the age of 4 months. • Upper molars have sharp shearing crests which aids in grinding leaves. • Opposable thumbs and big toes. • Large salivary glands break down tannin in leaves.

7. Species DescriptionDiet • Varied diet: • Hybrid frugivore/folivore as well as flowers. • Composition of diet depends on season and availability of different foods. • Research suggests that A. Pigra prefer fruit but will supplement with leaves when needed. • Fruit abundance is highest from July to December. • Flower abundance is highest from April to June.

8. Species DescriptionDiet

9. Species DescriptionActivity 1.5

10. Social OrganizationGroup composition • Small troops of 4-8 individuals • Troop composition is usually 1-4 males, with numerous females and their offspring. • Many groups featuring a single male and 1-3 females • Sometimes exhibit monogamous behaviour, in contrast to A. palliata's multiple male/female group composition. • Bands of roaming bachelor males challenge the males of mixed groups for dominance.

11. Social OrganizationTerritoriality • A. Pigra's territory: • Depending on size of group, territory size can range from 2-25 acres. • Territory provides food and living spaces. • Is A. Pigra territorial? Certain evidence points to the use of howling for territorial defense.

12. Social OrganizationReproduction • A. Pigra reaches reproductive maturity at age 4 • Gestation period is 180 days • Females in social group often tend to infants who are not their own. • Individuals from both genders usually disperse from their natal groups as early as 25-30 months of age or as late as adulthood. • In some cases individuals remain with their natal group.

13. Social OrganizationMating Rituals • Sexual Behaviour • Following: A male follows a female in estrus closely, often within physical reach. During this time the male focuses on the female often ignoring other individuals, social activities, and even eating. • Urine Sniffing: Typical male behaviour while following.

14. Social OrganizationMating Rituals • Sexual Behavour (cont.)‏ • Male Herding: A male stands closely or directly in front of a female, forcing her to recognize/acknowledge him and preventing her from walking towards another male • Adulterous Breeding: Documented examples of females from one troop mating with males from neighbouring troop.

15. Social OrganizationCopulation

17. Special Feature: HowlingBackground • Human anatomy: • the hyoid bone is suspended in the neck and is under the mandible bone, which is the bone structure at the bottom of our face. Its function is to support the tongue.

18. Special Feature: HowlingAnatomy • In A. Pigra, the hyoid bone is enlarged, and resides within in an enlarged pouch beneath the throat, which is hidden by a thick beard. • This cavity acts as a resonance box which generates lower frequencies, and amplifies the howl.

19. Special Feature: HowlingTaxonomy, Phylogeny and Evolution • Defining feature of Alouatta genus. • Unique hyoid bone morphology has been used historically to classify species within the genus Alouatta in three groups: • seniculus group • A. seniculus, A. belzebul, A. fusca • palliata group • A. palliata, A. pigra, A. coibensis • caraya group • A. caraya

20. Special Feature: HowlingTaxonomy, Phylogeny and Evolution • Molecular and phylogeny studies imply a slightly different grouping: • A. belzebul and A. seniculus form a clade with A. fusca as the sister taxon • A. palliata is the sister taxon to the remaining taxa. • Establishes A. palliata (and closely related A. pigra) as more primitive species within the genus, and A. seniculus as more evolved.

21. Special Feature: HowlingEvolution and Specialization • Further down the evolutionary tree, hyoid bone is more developed. • This contributes significantly to differences in calls between species: • A. seniculus produces calls with frequencies ranging from 350 to 3500 Hz, and spectral energy concentration on 350-1100Hz • A. caraya, which is more primitive, produces strongest calls in the more limited 310-328 Hz range

22. Special Feature: HowlingRange • These low frequency calls carry better in dense, humid, tropical forest. • Long distance call can be heard at least 1km away • Calls often repeated by monkeys at top of trees, making them louder than what is heard by observers below canopy. • Calls carry farthest in the morning, intermediate distances in the evening, and shortest midday due to differences in humidity.

23. Special Feature: HowlingInformation Content • The frequency and volume of the call is influenced by the size and shape of the hyoid bone and the throat. • In adult males, this cavity is larger and allows the individual to generate the loudest and lowest frequency calls. • Therefore when listening to a chorus of howlers, by listening for the different frequencies, one can get basic information about troop size and composition.

24. Special Feature: HowlingPurpose • Howling can be provoked by extrinsic factors: • airplanes passing • falling trees • rain showers • nearing of tourists, other howlers or spider monkeys • responding to human mimicry

25. Special Feature: HowlingBimodality and Territoriality • Most monkeys with long range calls exhibit a strong early morning peak in calling activity • A. Pigra additionally exhibits a strong late afternoon peak, so its calls follow a bimodal distribution. • During the rainy season, the peaks are less sharply defined (more calling midday); attributed to rain, lower sunlight.

26. Special Feature: HowlingBimodality and Territoriality • Horwich and Gebhard (1983) note: • Of all the species with long range vocalizations, there appears to be a correlation between those with bimodal calling distributions and those which exhibit territorial defense. • Recorded three incidents in A. pigra of troops being chased across boundaries, followed by increased howling within 100m of the border. • Conclusion: A. Pigra exhibits signs of territoriality

27. Special Feature: HowlingTerritoriality • Cornick and Markowitz (2002): • No significant evidence of territoriality • Typically large overlap of home ranges • Folivorous species rarely territorial: • Passive lifestyle for digestion • Leaves not usually a depletable resource • Conclusion: not territorial. • Compromise: Klein (1974) describes an active calling response following an incursion into a shifting “group space” surrounding the troop.

28. Conservation • Good news: • Not in immediate danger • Cause for concern: • Increasing forest fragmentation • Estrada shows that between 1984, and 2001, there was a loss of 3351 ha of rain forest vegetation. Most is because of humans. Converting forest land to open field. This change leads to a great increase in forest fragments.

29. ConservationPrimates and Fragmentation • In general, forest fragmentation can ... • prevent a primate species from living in or traveling to different forest fragments, can cause localized extinction. • alter group size, or population densities • alter the dietary strategies of the species • affect gene flow amount populations

30. ConservationFragmentation and A. Pigra • More good news: • According to studies by Silver and Marsh, Howler monkeys do much better in forest fragments compared to other primate species. • In this study, 2 troops of Howler monkeys living on a community Baboon Sanctuary (CBS) were transferred, radio transmitter collars were placed on them, and then they were Tran located to the Cockscomb Basin Wildlife Sanctuary. (CBWS)‏

31. ConservationAdaptations • Flexible diet: • Try novel foods very quickly, making unfamiliar goods readily exploitable to Howler monkeys. • Restricted energy expenditure when food sources become scarce: • Avoiding moving more than necessary. • Even in times of food abundance Howlers have been seen to rest a lot, perhaps as a way to maintain reserves in times of seasonal fluctuations.

32. ConservationConclusions • Howler monkeys appear very capable of living in small forest fragments. (Being able to live in smaller environments may make it easier to breed howler monkeys in zoological gardens, but further research is needed.)‏ • Despite techniques that permit howler monkeys to do well in forest fragments, it is possible that howlers are unsafe on a long-term basis. Under fragment conditions they are more vulnerable to being hunted, disease, predation, food shortages, and inbreeding.

33. Bibliography Books and Journals: Baumgarten, A., & Williamson, G.B. (2006). The Distribution of Howling Monkeys (Alouatta pigra and A.Palliata) in Southeastern Mexico and Central America. Primates,48, 310-315. Bearder, S.K., Campbell, C.J., Fuentes, A., Mackinnon,C.K., & Panger, M. (2007). Primates in Perspective. New York: Oxford University Press. Bramblett, C.A. (1976). Patterns of Primate Behavior. Palo Alto, California: Mayfield Publishing Company. Castellanos, L., Estrada, A., Garcia, Y., Mendoza, A., Munoz, D., Pacheco, R., & Van Belle, S. (2002). Population of the Black Howler Monkey (alouatta pigra) in a Fragmented Landscape in Palenque, Chiapas, Mexico. American Journal of Primatology, 58, 45-55. Estrada, A., Garber, P.A., Luecke, L., & Pavelka, M. (2006). New Perspectives on the Study of Mesoamerican Primates : Distribution, Ecology, Behavior, and Conservation. New York: Springer Science & Business Media, Inc. Fleagle, J.G. (1988). Primate Adaptation and Evolution. Academic Press. Gonzalez-Kirchner, J.P. (1998). Group Size and Population Density of the Black Howler Monkey (alouatta pigra) in Muchukux Forest, Quintana Roo, Mexico [Electronic version]. Folia Primatol, 69, 260-265.

34. Horwich, R.H., & Gebhard, K. (1983). Roaring Rhythms in Black Howler Monkeys (alouatta pigra) of Belize [Electronic version]. Primates, 24(2), 290-296. Horwich, R.H. (1983). Breeding Behaviors in the Black Howler Monkey (alouatta pigra) of Belize [Electronic version]. Primates, 24(2), 222-230. Horwich, R.H., & Johnson, E.D. (1986). Geographical Distribution of the Black Howler (alouatta pigra) in central America [Electronic version]. Primates, 27(1), 53-62. Kinzey, W.G. (1997). Alouatta. in New World Primates: Ecology, Evolution, and Behavior. New York: Aldine de Gruyter. Marsh, L.K. (2003). Primates in Fragments: Ecology and Conservation. New York: Kluwer Academic/plenum publishers. Pavelka, M., & Knopff, K.H. (2004). Diet and Activity in Black Howler Monkeys (Alouatta pigra) in Southern Belize: Does Degree of Frugivory Influence Activity Level? [Electronic Version]. Primates, 45, 105-111. Bibliography

35. Silver, S.C., Ostro, L.E.T., Yeager, C.P., & Horwich, R. (1998). Feeding Ecology of the Black Howler Monkey (Alouatta pigra) in Northern Belize [Electronic Version]. American Journal of Primatology, 45, 263-279. Sleeper, B. (1997). Primates: The Amazing World of Lemurs, Monkeys, and Apes. San Francisco: Chronicle Books. Strier, K.B. (2007). Primate Behavioral Ecology. Boston: Pearson Education, Inc. Villalobos, F., Valerio, A.A., & Retana, A.P. (2004). A Philogeny of Howler Monkeys (Cebidae: Alouatta) Based on Mitochondrial, Chromosomal and Morphological Data [Electronic Version]. International Journal of Tropical Biology and Conservation, 52(3), 665-677. Internet Websites: Animal Diversity Web (n.d.) Retrieved October 2, 2007, fromhttp://animaldiversity.ummz.umich.edu/site/accounts/classification/path/Alouatta.html#Alouatta Black Howler Monkey (n.d.) Retrieved September 15, 2007, fromhttp://www.belizezoo.org/zoo/zoo/mammals/how/how1.html Guatemalan Howler Monkey (Alouatta Pigra) (n.d.) Retrieved September 25, 2007, fromhttp://www.theprimata.com/alouatta_pigra.html Bibliography

36. Medicalook (n.d.) Retrieved September 30, 2007, fromhttp://www.medicalook.com/human_anatomy/organs/Facial_bones.html Primate Evolution (n.d.) Retrieved September 24, 2007, fromhttp://www.theprimata.com/evolution.html Primate Info Net (n.d.) Retrieved October 2, 2007, fromhttp://pin.primate.wisc.edu/factsheets/links/alouatta San Francisco Zoo Website (n.d.) Retrieved September 20, 2007, from http://www.sfzoo.org/cgi-bin/animals.py?ID=41 Treves, A. (2001). Tourist Impacts On The Behaviour Of Black Howler Monkeys (Alouatta Pigra) at Lamanai, Belize. Retrieved October 1, 2007, from http://www.coex-wildlife.org/docs/Treves%20&%20Brandon.pdf Bibliography