Transcript apigra - McGill, University of

Black Howler Monkey
Alouatta Pigra
http://www.cs.mcgill.ca/~dtremb8/apigra.ppt
Stephanie Larocque
Joseph Leung
Daniel Tremblay-Sher
Myriam Tremblay-Sher
Diana Yin
Taxonomy
Primates
Haplorrhini
Simiiforms
Catarrhini
Strepsirrhini
Tarsiiforms
Platyrrhini
Aotidae
Atelidae
Alouattinae
Alouatta
Cebidae
Atelinae
Pitheciidae
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.
Species Description
Geographical Distribution
Species Description
Geographical Distribution

Central America:

Yucatan Peninsula, Mexico

Guatemala

Belize

Tropical evergreen, semi-evergreen forest

Altitudes below 400m.

Riverine areas with seasonal flooding
Species Description
Physical 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.
Species Description
Diet

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.
Species Description
Diet
Species Description
Activity
Percent age of t im e spent on daily act ivit ies
averaged over one m ont h
1.5 2.3
9.8
25
61.9
Resting
Feeding
Traveling
Social Affiliative be haviours
Vocalizing
Social Organization
Group 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.
Social Organization
Territoriality

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.
Social Organization
Reproduction

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.
Social Organization
Mating 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:
following.
Typical male behaviour while
Social Organization
Mating 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.
Social Organization
Copulation
Special Feature: Howling
Background

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.
Special Feature: Howling
Anatomy


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.
Special Feature: Howling
Taxonomy, 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


palliata group


A. seniculus, A. belzebul, A. fusca
A. palliata, A. pigra, A. coibensis
caraya group

A. caraya
Special Feature: Howling
Taxonomy, 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.
Special Feature: Howling
Evolution 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
Special Feature: Howling
Range




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.
Special Feature: Howling
Information 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.
Special Feature: Howling
Purpose

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
Special Feature: Howling
Bimodality 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.
Special Feature: Howling
Bimodality 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
Special Feature: Howling
Territoriality



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.
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.
Conservation
Primates 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
Conservation
Fragmentation 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)
Conservation
Adaptations

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.
Conservation
Conclusions


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.
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.
Bibliography
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
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#Aloua
tta
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
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/cgibin/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.coexwildlife.org/docs/Treves%20&%20Brandon.pdf