ISSN 1 4 1 3 -4 7 0 3
NEOTROPICAL
primates
VO LUM E 9
N U M BER 3
DECEM BER 2 0 0 1
A Jo urna l a nd N e w sl e tte r o f the
N eotropical Section of the IUCN / SSC
Pri ma te Sp e c i a li st G ro up
Editors: Anthony B. Rylands and Ernesto Rodríguez-Luna
PSG Chairman: Russell A. M ittermeier
PSG Deputy Chairmen: Anthony B. Rylands and W illiam R. Konstant
Neotropical Primates
A Journal and Newsletter of the Neotropical Section of the IUCN/SSC Primate Specialist Group
S
Center for Applied Biodiversity Science
Conservation International
1919 M. St. NW, Suite 600, Washington, DC 20036, USA
ISSN 1413-4703
Abbreviation: Neotrop. Primates
Editors
Anthony B. Rylands, Center for Applied Biodiversity Science, Conservation International, Washington, DC
Ernesto RodrÌguez-Luna, Universidad Veracruzana, Xalapa, Mexico
Assistant Editor
Jennifer Pervola, Center for Applied Biodiversity Science, Conservation International, Washington, DC
Editorial Board
Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK
Adelmar F. Coimbra-Filho, Academia Brasileira de CiÍncias, Rio de Janeiro, Brazil
Liliana CortÈs-Ortiz, Universidad Veracruzana, Xalapa, Mexico
Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA
Stephen F. Ferrari, Universidade Federal do Par· , BelÈm, Brazil
Eckhard W. Heymann, Deutsches Primatenzentrum, Gˆ ttingen, Germany
William R. Konstant, Conservation International, Washington, DC
Russell A. Mittermeier, Conservation International, Washington, DC
Marta D. Mudry, Universidad de Buenos Aires, Argentina
Hor· cio Schneider, Universidade Federal do Par· , BelÈm, Brazil
Karen B. Strier, University of Wisconsin, Madison, Wisconsin, USA
Maria EmÌlia Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil
Primate Specialist Group
Chairman Russell A. Mittermeier
Deputy Chairs Anthony B. Rylands & William R. Konstant
Co-Vice Chairs for the Neotropical Region Anthony B. Rylands & Ernesto RodrÌguez-Luna
Vice Chair for Asia Ardith A. Eudey
Vice Chair for Africa T homas M. Butynski
Vice Chair for Madagascar Jˆ rg U. Ganzhorn
Design:
Glenda P. F· bregas, Center for Applied Biodiversity Science, Conservation International, Washington, DC.
Production:
Kim Meek, Center for Applied Biodiversity Science, Conservation International, Washington, DC.
Editorial Assistance:
John M. Aguiar, Department of Wildlife and Fisheries Sciences, Texas A& M University, Texas.
Front Cover:
Photo, Ateles geoffroyi geoffroyi, courtesy of Vince Sodaro, Primate Department, BrookÝeld Zoo, Brookville, Illinois, 60513, USA.
T his issue of Neotropical Primates was kindly sponsored by the Margot Marsh Biodiversity Foundation, 432 Walker Road, Great Falls, Virginia 22066, USA,
the Houston Zoological Gardens Conservation Program, General Manager Rick Barongi, 1513 North MacGregor, Houston, Texas 77030, USA, and the Los
Angeles Zoo, Director Manuel Mollinedo, 5333 Zoo Drive, Los Angeles, California 90027, USA.
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93
Neotropical Primates 9(3), December 2001
SHORT ART ICLES
B ODY WEIGHTS OF ADULT FEMALE ALOUATTA
C OSTA RICA INCREASE WITH AGE
PALLIATA IN
Evan L. Zucker
Margaret R. Clarke
Kennneth E. Glander
Introduction
Body weights are often used as correlates of general health,
as well as being predictive, perhaps, of future reproductive
success (Trivers and Willard, 1973; Bercovitch et al., 1998).
For female nonhuman primates, the long-term monitoring
of body weights constitutes an integral part of the study of
life histories (Harvey et al., 1987). With respect to female
mantled howling monkeys (Alouatta palliata ), they emigrate
from their natal groups as juveniles (Glander, 1980, 1992;
Scott et al., 1978), as do males, later immigrating into other
social groups after a period of living alone. In order to stay in
these new social groups, immigrating females must become
dominant to all resident females, a process that can take up
to a year (Jones, 1980; Glander, 1992; Zucker and Clarke,
1998). As group membership is a competitive process, the
sizes (weights) of immigrant females might contribute to their
competitive abilities and eventual successful immigrations.
Newly immigrant females weigh less than resident females;
but after two years, this difference disappears (Zucker et al.,
submitted).
T his process of juvenile emigration from natal groups, with
subsequent immigration into other groups as young adults,
results in reversed, age-graded hierarchies for each sex (Clarke
and Glander, 1984; Jones, 1980; Zucker and Clarke, 1998).
T he most dominant individual of each sex is typically the
youngest, while the least dominant is the oldest, usually
having the longest tenure in the group (Clarke and Glander,
1984; Jones, 1980; Zucker and Clarke, 1998). T hus, age
and status are inversely (negatively) related, unlike the
positive relationship common in Old World genera, such as
Macaca and Papio; that have been more extensively studied
with respect to physical growth and development (Altmann
et al., 1977; Bercovitch, 1987; Bercovitch et al., 1998; Rawlins
et al., 1984; Small, 1981).
In this report, we present body weight data for adult females,
which have successfully immigrated and resided in one social
group at Hacienda La Pacifica, Guanacaste Province, Costa
Rica. T hese females were residents between 1985 and 1993,
during which time various age and sex classes were the
subjects of behavioral and physiological studies.
Methods
Study Site and Subjects
Hacienda La Pacifica, located 5 km northwest of Cañas,
in Guanacaste Province, Costa Rica, is a 1,980-ha ranch
(Glander, 1992) in the lowland tropical dry forest zone
(Holdridge, 1967). T he majority of adult mantled howlers
on the ranch have been captured and marked for reliable
identification (Scott et al., 1976; Glander et al., 1991;
Glander, 1992). Upon capture, all monkeys were weighed,
measured, and tattooed, and adult females were palpated to
detect pregnancies (Glander, 1980, 1992). Adults are marked
with unique, color-coded leg chains (males) or collars and
tags (females). Individuals captured for the first time are
aged, based on dental characteristics (Pope, 1966). Monkeys
have usually been captured during the months of February
and July.
Study of Group 2 at La Pacifica began in 1985, after census
work in 1984 provided the group’s demography (Clarke
et al., 1986). During the 9-year period covered in this report
(1985–1993), mean group size was 17.3 monkeys (sd = 3.8),
including an average of 8.4 adult females (sd = 1.6). T his
group inhabits an L-shaped home range of upland forest (see
Fig. 1 in Glander, 1992, for a map of the ranch showing the
location of this group). Home range size was estimated to be
24 ha (Zucker et al., 1996), although this was decreased by
approximately 10% in 1991 following deforestation related
to the construction of a major canal system through La
Pacifica and other parts of Guanacaste Province (Clarke
et al., 2002).
Data Set
Six adult females were captured and marked in 1985.
In 1986, four more adult females were captured and marked,
including two females believed to be recent immigrants.
Two marked adult females from 1985 were not present in
1986. T hus, beginning in 1986, all adult female residents in
this group were marked and identifiable. In calculating the
mean weight of adult females in this group, the first weights
obtained for these 10 females (1985–1986) were used, in
addition to the first weights obtained for the subsequent six
immigrants. Only the body weights of nonpregnant females
are included.
Longitudinal assessment of body weights became possible
after all of the adult females in Group 2 were marked.
Weights for 12 females which were in the group for a
minimum of two years are presented here, with multiple
weights available for eight of them. As we have minimized
the number of times animals in this group are captured,
weights are not available for all individuals in all years of
study. After the initial two years, weights of some females
were obtained in 1989, 1991, 1992, and 1993. Animals
new to the group were captured for permanent marking, as
were residents which needed damaged or lost collars, tags, or
chains to be replaced.
T he affiliative and agonistic interactions of the adult females
in Group 2 were studied systematically between 1988 and
1992 during portions of June, July, and/or August (Zucker
and Clarke, 1998). T hus, dominance relationships of the
7–9 females in the group during this period are also known,
94
Neotropical Primates 9(3), December 2001
Discussion
and results generally fit the expected reversed, age-graded
hierarchy, although the hierarchies were variable over time.
Yearly dominance ranks are given in Zucker and Clarke
(1998, Table III).
Results
Taking into account only the first weights, the mean body
weight for the 16 females, which were residents in Group
2 at some time between 1985 and 1993, was 4.09 kg (sd =
0.49; range 3.18–5.10 kg). Using all body weights obtained
during the study period for these 16 females (n = 26), the
mean body weight of an adult female was 4.30 kg (sd = 0.53;
range 3.18–5.70 kg). Yearly means and standard deviations
are presented in Table 1.
Multiple body weight measurements were available for eight
Group 2 females. Seven of them increased their weight
over time. T he last body weights of these females were, on
the average, 16.46% greater than their first weights, with
increases ranging from 4.65% to 40.67% (sd = 14.98%).
T he female who lost weight experienced a decrease of 3.92%
over two years. Weights over time for the older females in
the group are shown in Figure 1a, while weights for the
younger females are shown in Figure 1b. It is evident that the
females’ weights increased over the years, regardless of length
of tenure in the group. Taking into account the number of
years in the group, the mean increase per year was 3.64%
(sd = 2.72%) for the seven females that showed increases.
For mantled howlers, status decreases with increased tenure
in the group (Clarke and Glander, 1984; Glander, 1980;
Jones, 1 80; Zucker and Clarke, 1998), so there would be an
inverse relationship between status and body weight.
Adult female mantled howling monkeys increased their body
weights throughout their lives, although the proximate causes
of these changes have not yet been assessed in this sample
(or population). Increases could be due to increased bone
growth and overall size, decreased lean body mass, increased
amounts of fat, or changes in bone densities (see Schwartz
and Kemnitz, 1992).
During the latter portion of the study period, constructionrelated deforestation produced some major changes in the
group’s home range (Clarke et al., in press) and, despite
the loss of a major Spondias tree and a number of other
fruit trees, body weights of the adult females continued to
increase, regardless of their specific age or social status. Mean
daily path length increased following deforestation (Clarke
et al., 2002), so these weight increases occurred even with
increased activity, and were not due to decreased activity that
might accompany increased age.
T he weight increases with age described for this one group of
howlers might not be found in groups consuming different
diets or living in different microhabitats, such as those
inhabiting the riverine forests at La Pacifica. Howlers in the
drier, upland forests spend more time feeding than do the
howlers living near the rivers (Teaford and Glander, 1996),
which could be compounded further by increased feeding
time per day during the dry season by the upland groups.
T he volume of food consumed, which would contribute to
body weight, might not reflect the nutritional value of the
food, or alternatively, the relationship between volume and
nutritional value could vary seasonally. Intergroup differences
Table 1. Adult female Alouatta palliata at Hacienda La Pacifica, Guanacaste Province, Costa Rica. Ages, years weighed, yearly means,
and standard deviations.
Female
*
1985
1986
1989
1991
1992
1993
*
Burgundy
Cherry
Goldenrod
Indigo
Marigold
Violet
Oregano
Pansy
RC
T ulip
Chicory
JQ
Sage
Wisteria
Azalea
Bamboo
9-R
15-R
12-R
6-R
9-R
18-R
Mean (kg)
Sd
N
3.85
0.55
6
7-R
14-R
22-R
4-I
12-R
9-I
19-R
15-R
12-R
11-I
4-I
16-R
25-R
13-R
4-I
5-I
6-R
7-R
4-I
20-I
4.08
0.21
5
4.70
0.70
5
4.47
0.38
3
Numbers indicate estimated age, in years; “R” = resident in group, “I” = recent immigrant.
4.35
0.64
2
4.56
0.11
5
95
Neotropical Primates 9(3), December 2001
old. With larger sample sizes, Schwartz and Kemnitz (1992)
corroborated this curvilinear pattern, finding that weight
increased over the first 14 years, then decreased. Females
over 20 years old were significantly lighter than other adult
females (Schwartz and Kemnitz, 1992). T hus, howlers and
rhesus differ during the latter portion of adulthood in
this relationship between age and weight. Rhesus females
decrease in weight as they approach their twenties, whereas
the weights of howler females continue to increase. T he
sample of La Pacifica howlers included two females (Violet
and Tulip) over 20 years old (Table I), which continued to
increase in weight during their twenties. Testable hypotheses
about these species’ differences during latter adulthood might
center on differences in activity levels, quality and types
of foods eaten, psychosocial stresses, and/or physical forces
associated with arboreal (howler) versus more terrestrial
(rhesus) ways of life.
Acknowledgments
Figure 1. Weights over time of adult female howling monkeys in
Group 2 at Hacienda La Pacifica. Weights of older females are
shown in (a) and younger females in (b).
in the consumption of different food types were found even
within microhabitats (Teaford and Glander, 1996).
Studies of rhesus monkeys (Macaca mulatta ) provide some
comparable data relating body weight to status, although
differences in the life histories and social systems of these two
species produce different patterns. For rhesus females living
in an outdoor field cage, Small (1981) found a significant
positive correlation between rank and fat index (composite
fat score from skinfold measurements/body weight). Higher
fat indexes for high ranking females were attributed to
preferential access to food, resulting in them being more
healthy. For mantled howlers, immigration patterns produce
an inverse relationship between status and weight, although
this is clearly confounded by age. In Small’s (1981) study, the
ages of the higher ranking females were not given, nor was
the upper age limit of the adult females studied, although no
significant relationship was found between fat index and age
(Small, 1981).
Cross-sectional data for provisioned rhesus monkeys on Cayo
Santiago, in Puerto Rico, indicated that age and weight
were positively related for adult females until they were
approximately 13 years old, then weight declined gradually
(Rawlins et al., 1984, Table II). In this study by Rawlins
et al., sample sizes were quite small for females over six years
T his research was supported in part by NIH Grant RR00164
to the Tulane Regional Primate Research Center. Some of the
capturing and weighing of monkeys was done in conjunction
with dental microwear studies; see Teaford and Glander
(1996) for sources of support for that work. We thank
Jennifer Conkerton for assistance with data tabulation, the
management of La Pacifica for their continued support and
permission to work at this site, and the Hagnauer family for
all their assistance in numerous ways over the many years.
Some of these data were presented at the 1998 meeting of
the American Association of Physical Anthropologists, Salt
Lake City, UT (USA).
Evan L. Zucker, Department of Psychology, Loyola
University, New Orleans, LA 70118, USA, e-mail:
<zucker@loyno.edu>, Margaret R. Clarke, Department
of Anthropology, Tulane University, New Orleans, LA
70118, USA, e-mail: <mrclarke@tulane.edu>, and Kenneth
E. Glander, Department of Biological Anthropology and
Anatomy, Duke University, Durham, NC 27708, USA,
e-mail: <glander@duke.edu>.
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S. A. 1977. Life history of yellow baboons: Physical
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Bercovitch, F. B. 1987. Female weight and reproductive
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Bercovitch, F. B., Lebron, M. R., Martinez, H. S. and Kessler,
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Clark, M. R., Collins, D. A. and Zucker, E. L. 2002.
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Clarke, M. R. and Glander, K. E. 1984. Female reproductive
success in a group of free-ranging howling monkeys
(Alouatta palliata ) in Costa Rica. In: Female Primates: Studies
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Alan R. Liss, New York.
Clarke, M. R. and Zucker, E. L. 1994. Survey of the howling
monkey population at La Pacifica: A seven-year follow-up.
Int. J. Primatol. 15: 61–73.
Clarke, M. R., Zucker, E. L. and Scott, N. J., Jr. 1986.
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Glander, K. E. 1980. Reproduction and population growth
in free-ranging mantled howling monkeys. Am. J. Phys.
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Glander, K. E. 1992 . Dispersal patterns in Costa Rican
mantled howling monkeys. Int. J. Primatol. 13: 415– 436.
Glander, K. E., Fedigan, L. M., Fedigan, L. and Chapman,
C. 1991. Field methods for capture and measurement
of three monkey species in Costa Rica. Folia Primatol.
57: 70–82.
Harvey, P. H., Martin, R. D. and Clutton-Brock, T. H.
1987. Life histories in comparative perspective. In: Primate
Societies, B. B. Smuts, D. L. Cheney, R. M. Seyfarth,
R. W. Wrangham and T. T. Struhsaker (eds.), pp.181–196.
University of Chicago Press, Chicago.
Holdridge, L. R. 1967. Life Zone Ecology. Tropical Sciences
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Jones, C. B. 1980. T he functions of status in the mantled
howler monkey Alouatta palliata Gray: Intraspecific
competition for group membership in a folivorous
Neotropical primate. Primates 21: 389– 405.
Pope, B. L. 1966. T he population characteristics of howler
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Rawlins, R. G., Kessler, M. J. and Turnquist, J. E. 1984.
Reproductive performance, population dynamics and
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macaques. J. Med. Primatol. 13: 247–259.
Schwartz, S. M. and Kemnitz, J. W. 1992. Age- and genderrelated changes in body size, adiposity, and endocrine
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Grouping behavior and sex ratio in mantled howling
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London.
Scott, N. J., Jr. Scott, A. F. and Malmgren, L. A. 1976.
Capturing and marking howler monkeys for behavioral
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Small, M. F. 1981. Body fat, rank, and nutritional status
in a captive group of rhesus monkeys. Am. J. Primatol.
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Teaford, M. F. and Glander, K. E. 1996. Dental microwear
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VARIATIONS IN GROUP SIZE IN W HITE -FACED SAKIS
( PITHECIA PITHECIA): EVIDENCE FOR MONOGAMY
OR SEASONAL C ONGREGATIONS?
Shawn M. Lehman
Waldyke Prince
Mireya Mayor
Introduction
T here are few longitudinal data on the social structure and
behavior of white-faced sakis (Pithecia pithecia pithecia ).
Synecological studies have found that they tend to live
in small groups of 2– 4 animals (Buchanan et al., 1981;
Mittermeier, 1977; also Oliveira et al., 1985, who studied
the golden-faced subspecies, P. p. chrysocephala ), which
have led some researchers to suggest that white-faced sakis
are monogamous (e.g., Napier and Napier, 1986; Robinson
et al., 1986; Dunbar, 1988). Besides group size, support for
monogamy in white-faced sakis comes from field studies in
which males and females responded in a territorial manner to
loud calls during vocal playback experiments (Rosenberger
et al., 1997).
Data from historic accounts and recent surveys indicate that
some groups of white-faced sakis contain more than four
individuals. T here have been reports as early as the mid-19 th
century of groups with 6 –10 members (Schomburgk, 1848;
Schomburgk, 1876). More recent field accounts confirm that
some groups have more than one adult member of each sex
(Buchanan, 1978; Oliveira et al., 1985; Kinzey and Norconk,
1993; Gleason and Norconk, 1995; Ryan, 1995; Norconk
et al., 1997; Norconk et al., 1998), leading to suppositions that
this species may not be monogamous. It has been suggested
that groups with more than four animals may represent
seasonal congregations of smaller groups (Buchanan, 1978;
Fleagle and Meldrum, 1988). T herefore, it is not surprising
that Rosenberger and coworkers (1997) recommended that
97
Neotropical Primates 9(3), December 2001
we reevaluate the white-faced saki as a “typical” monogamous
primate.
Although preliminary surveys have provided invaluable data
on the size and composition of white-faced saki groups (e.g.,
Mittermeier, 1977; Oliveira et al., 1985; Kessler, 1998), they
are difficult to interpret because the studies were typically
conducted during only one season, and few sightings were
made due to the shy and cryptic nature of the animals.
Moreover, there are few recent data for populations of whitefaced sakis in Guyana (Muckenhirn et al., 1975; Sussman and
Phillips-Conroy, 1995), where there are, surprisingly, some
of the earliest descriptions of large group sizes (Schomburgk,
1848; Schomburgk, 1876).
If there is a seasonal effect influencing group congregations
in white-faced sakis, then surveys conducted throughout the
year may provide important preliminary data on their social
structure. In this report we present longitudinal survey data
on group size for white-faced sakis in Guyana and summarize
results from previous surveys. We then suggest directions for
future studies.
Methods
T he data analyzed in this paper are from a literature review
and 1,725 km of surveys we conducted at sixteen sites in
Guyana (Fig. 1). Guyana is a small country of 215,000
km2 situated on the northeastern coast of South America,
between 56°20’ and 61°23’W and 1°10’ and 8°35’N. Mean
annual precipitation is between 2,000 and 3,400 mm (ter
Steege, 1993). T here are generally two wet seasons (May
to August and December to January) and two dry seasons
(September to November and February to April).
Data were collected during three periods: (1) November
1994 to June 1995; (2) September 1995 to June 1996;
and (3) June to August, 1997. When surveying forests, we
used randomly selected and predetermined transect lines.
Although most studies of the distribution of animals use
only random selection of transects (e.g., Anderson et al.,
1979; Burnham et al., 1980; Krebs, 1989; Peres, 1997),
we also used predetermined transect lines to ensure that
biogeographic features, such as rivers that may be barriers
to dispersal, were included in the data set. Predetermined
transect lines often ran along paths in the forest to maximize
survey time in remote areas. Two types of surveys were
conducted: (1) unique and (2) repeat. Unique surveys were
made along transects, such as trails or riverbanks, where
one to two transits were made during a census. During
repeat surveys we conducted more than two transits of a
transect line. Repeat surveys were conducted along paths at
five locations: (1) Timehri; (2) Dubulay Ranch; (3) Kaieteur
Falls National Park; (4) Mabura Hill Ecological Reserve and
(5) Sebai River. We walked slowly along unique and repeat
transects lines at a rate of 1.0 km/h, stopping every ten
minutes to listen for the sounds of movement in the forest.
Figure 1. Locations of study sites.
We surveyed rivers by paddling slowly (1.5–2.0 km/h) along
riverbanks. During river surveys, randomly selected areas
were chosen on each bank for land surveys. Non-linear
transect lines in the forest were used because travel costs
are very high in Guyana. T hus, it was cost-prohibitive to
cut and mark trails when only 2– 4 weeks were available
for data collection. Furthermore, in protected areas such as
Kaieteur Falls National Park, Mabura Hill Forest Reserve,
and Iwokrama Forest Reserve, it is illegal to cut trails. Hence,
established trails were used in these protected areas.
During surveys, data were recorded on: (1) primate species;
(2) time of day; (3) weather; (4) vegetation height; (5) general
height of group; (6) number of animals in group; (7) cue by
which animals were detected; (8) activity; (9) perpendicular
distance from the transect [meters]; (10) sighting angle;
and (11) habitat type. When a primate group was seen, a
standardized time of 10 minutes was spent observing the
behavior of individuals in the group (NRC, 1981). Ad libitum
notes on behavior, obvious individual physical characteristics,
and vocalizations were also collected. T he location of
primate groups seen during surveys was determined using
LANDSAT-5 satellite photographs, 1:50,000 topographic
maps of the region, and a Magellan NAV 5000D GPS. If
monkeys were observed feeding, then fruit and/or voucher
specimens were collected. Specimens were placed in plastic
zip-lock bags and preserved with 80% ethanol. T hey were
deposited for identification at the Center for the Study of
Biological Diversity at the University of Guyana. Habitat
descriptions were made using soil features, a vegetation map
(Huber et al., 1995), various monographs on Guyanese flora
98
Neotropical Primates 9(3), December 2001
(Van Roosmalen, 1985; de Granville, 1988; Mennega et al.,
1988; ter Steege, 1990, 1993), and LANDSAT-5 satellite
imagery of survey areas.
Group sizes are given as the mean ± one standard deviation.
Nonparametric statistics were used because survey data
violate assumptions of normality (Ludwig and Reynolds,
1988). Spearman correlation coefficients (rs) were computed
for monthly data on mean group size (dependent variable)
versus rainfall and fruiting records (independent variables)
in Guyana. Rainfall and fruiting records are based on
100 years of data collected in Guyana (ter Steege, 1993).
Data on group sizes from the three groups seen by Kinzey
(1988) and Norconk (1997) in Venezuela were combined
to facilitate comparisons. A Kruskal-Wallis (H ) test was
used to determine variations in group sizes between studies.
Mann-Whitney U (U ) tests were run to document pair-wise
differences in group sizes for each of the published studies.
Statistics were computed using SPSS 8.0 statistical software.
All statistical tests were two-tailed and the alpha level was set
at p<0.05.
Results
Table 1 shows the group size and composition of whitefaced sakis we sighted in Guyana. We observed a total of 21
groups. Group size ranged from 2–12, with a mean of 4.8
± 2.4 animals. T he total average sex ratio was 1.1:1. Of the
Table 1. Size and composition of Pithecia pithecia pithecia groups
censused in Guyana.
Group
Number
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
Total
Range
Mean
1 SD
Adult
males
1
2
2
3
1
2
2
2
1
5
3
2
2
1
1
3
1
2
1
3
1
41
1-5
2.0
1.0
Number of Animals
Adult Juvenile Juvenile
Infants
females males females
1
2
2
3
1
2
1
2
2
5
3
2
0
0
2
2
1
2
1
2
1
37
0-5
1.8
1.1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
1
1
1
1
4
0-2
1.3
0.6
9
0-1
1.0
0.0
1
1
9
0-1
1.0
0.0
T otal
2
5
4
7
3
4
3
5
5
12
6
6
2
3
3
9
4
5
4
6
2
100
2-12
4.8
2.4
21 groups censused, 52.3% (N = 11) contained more than
one adult of each sex. A total of 71.4% (N = 15) groups
contained more than one adult male or adult female. Mean
monthly group size was not correlated with either rainfall (rs
= -0.145, p = 0.78) or fruiting records (rs = 0.464, p = 0.35).
On April 17, 1996, a group of twelve white-faced sakis were
sighted by SML in riparian forest near the Madewini River
in northern Guyana (6°29’N, 58°13’W). T he animals were
not shy and were followed easily for one hour. T he group was
composed of five adult males, five adult females, a juvenile
male, and a juvenile female. T he animals were traveling
slowly as a cohesive group in the understorey at a height of 15
m. Two adult males foraged for ripe fruits in a kokerite palm
(Attalea maripa ) within 1 m of each other. Each male bit into
and dropped fruits over a 45-second period before moving
off to join the rest of the group. No social interactions were
observed among any of the group members.
Average group size for all records of white-faced sakis was
3.8 ± 2.1 animals (Table 2). T here is significant variation in
group size for white-faced sakis across the study sites in NE
South America (Kruskal-Wallis H (5) = 12.650, p = 0.027).
T his variation is driven by significantly larger group sizes in
Guyana compared to those reported by Mittermeier (1977)
in Suriname (Table 3).
Discussion
Some groups we surveyed in Guyana contained only one
adult of each sex, whereas others contained more than one
adult of each sex. We found no evidence of a seasonal effect
on group size. Our data on group size are comparable to
those collected by Kinzey et al. (1988) in eastern Venezuela
and Muckenhirn et al. (1975) in Guyana. T his continuity
in grouping patterns for white-faced sakis in the western
Guiana shield (eastern Venezuela and Guyana) indicates that
the observations we made are not a phenomenon unique to
only our study sites and time period. Surprisingly, average
group size for white-faced sakis in Suriname, which is also
part of the Guiana Shield (Norconk et al., 1997), was
significantly smaller than that seen for conspecific groups
in Guyana. T he reasons for these regional differences in
social structure are poorly documented, but may be due
to variations in plant species composition and diversity
(Terborgh and Andresen, 1998). T herefore, our data support
white-faced sakis as not being representative of a “typical”
monogamous primate (Rosenberger et al., 1997). However,
it must be noted that only limited interpretations of social
behavior can be made based on survey data. Detailed data
on the feeding ecology and behavior of habituated groups are
needed to determine the causal factors affecting intraspecific
variation in group structure.
It should not be assumed that white-faced sakis are alone
in challenging our views on primate monogamy. Fuentes
(1999) conducted a review of primate monogamy and found
that many supposed monogamous species exhibit a variety
of grouping types and mating patterns. A notable example
99
Neotropical Primates 9(3), December 2001
T able 2. Size and composition of Pithecia pithecia groups censused in South America.
Group Size
Mean ± 1 SD
Range
Country
Guyana
Guyana
Venezuela
Venezuela
Suriname
French Guiana
Brazil
Brazil
4.8 ± 2.4
3.3 ± 1.7
9.0
5.5 ± 2.5
2.7 ± 0.8
2.8 ± 1.0
2.6 ± 0.5
6
2-12
1-5
3-8
2-4
1-4
2-3
N
AM
AF
21
10
1
2
9
4
3
1
1-5
0-5
3
1
1-2
1
0-2
1
0-2
1-3
Group Composition
SA
J
0-2
1-2
I
0-2
0-1
0-1
0-1
0-2
0-2
0-1
0-2
Sources
Present study
Muckenhirn et al. (1975)
Norconk (1997)
Kinzey et al. (1988)
Mittermeier (1977)
Kessler (1998)
Oliveira et al. (1985)
Setz and Gaspar (1997)
AM=adult male, AF=adult female, SA=subadult, J=juvenile, I=Infant
T able 3 . Mann-Whitney U scores for intersite differences in group size for Pithecia pithecia pithecia . Sites are expressed by country to
facilitate comparisons. Numbers above the diagonal refer to the U score. Numbers below the diagonal indicate the corresponding p
value for each test.
Country
Venezuela
Venezuela
Guyanaa
Guyanab
Suriname
French Guiana
Brazil
a
0.214
0.155
0.042
0.105
0.142
Guyanaa
Guyanab
Suriname
French Guiana
Brazil
25.5
6.0
60.0
48.0
68.5
33.0
1.5
32.5
15.5
17
2.0
11.5
10.0
12.5
6.0
0.053
0.019
0.119
0.076
0.310
0.509
0.370
0.865
0.364
0.544
b
Present study, Muckenhirn et al. (1975)
of this social diversity can be found among hylobatids.
Despite gibbons being described as invariably monogamous
(Leighton, 1986), recent field studies indicate that some
species are not exclusively monogamous and/or pair-bonded
(Jiang et al., 1999; Palombit, 1994; Palombit, 1999; Sommer
and Reichard, 2000). For example, Jiang and colleagues
(1999) report the coexistence of monogamy and polygyny
in black-crested gibbons (Hylobates concolor). T herefore,
contrary to assumptions of obligate monogamy in gibbons,
the social system of these primates may be characterized
by flexible grouping and mating patterns (Sommer and
Reichard, 2000).
How then can we interpret a social system for white-faced
sakis that contrasts large group size, at least in some parts
of its range, and monogamy? Monogamy in primates has
been explained as: (1) an anti-infanticide strategy (Van
Schaik and Dunbar, 1990; Palombit, 1999); (2) a strategy
to elicit male parental care (Kleiman, 1977); (3) a means of
protecting resources that are scarce and uniformly dispersed
(Wittenberger and Tilson, 1980); and (4) a response to
human predation (Kinzey, 1987). Fuentes (1999) reviewed
these models and identified the following six characteristics
of monogamy: exclusive one-male/one-female groups; pair
bond and reinforcement behavior; sexual monomorphism;
exclusive mating; territoriality; and paternal care. Whitefaced sakis do not meet the criteria for three of the six
monogamous characteristics: exclusive one-male/one-female
groups (present study; Kinzey et al., 1988; Norconk, 1997;
Rosenberger et al., 1997); pair bond/reinforcement behavior
(Gleason and Norconk, 1995); and paternal care (Ryan,
1995). Monomorphism is the only one of Fuentes’ (1999)
criteria that P. p. pithecia meets. T he lack of longitudinal data
on territoriality and the exclusivity of mating between two
adults highlight some of the directions to be undertaken in
future studies of this species. Social systems in white-faced
sakis will be better understood when longitudinal data are
also collected on: (1) demography and social behavior,
(2) population genetics and paternity, and (3) ecological
correlates to social structure.
Acknowledgments
We thank the Office of the President, University of Guyana,
Ministry of Amerindian Affairs, Ministry of Health, National
Parks Commission, Tropenbos Guyana, Demarara Timbers
Ltd., Iwokrama Rain Forest Reserve, and the Wildlife
Division of the Department of Health for permission to
conduct our study. We greatly appreciate the support of Dr.
Vicki Funk and Carol Kelloff of the Biological Diversity
of the Guianas Program at the Smithsonian Institution.
We gratefully acknowledge our many field guides. Pascale
Sicotte provided valuable comments on the manuscript. T his
project was supported in part by the Lincoln Park Zoo Scott
Neotropic Fund, the Biological Diversity of the Guianas
Program of the Smithsonian Institution, USAID, GEF,
University of Miami Women's and Minorities Fellowship,
and a NSF predoctoral fellowship.
Shawn M. Lehman, Department of Anthropology,
University of Toronto, Toronto, Ontario, Canada M5S
3G3, Waldyke Prince, Iwokrama International Centre for
100
Rain Forest Conservation and Development, Georgetown,
Guyana, and Mireya Mayor, Interdepartmental Doctoral
Program in Anthropological Sciences, Department of
Anthropology, Stony Brook University, Stony Brook, NY
11794, USA.
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DIURNAL ACTIVITY BUDGETS
MONKEYS, ATELES CHAMEK,
AMAZONIAN TROPICAL FOREST
OF
IN
BLACK SPIDER
A SOUTHERN
Robert B. Wallace
Introduction
In the last twenty years an increasing number of field studies
have demonstrated the potential behavioral flexibility within
individual primate species. Until recently few published
studies existed for any one primate genus, and thus all
populations of a given species were inevitably ‘tarred with
the same behavioral brush’ of just one focal study group.
Whilst detailed behavioral studies of some primate genera
are still scarce, for example the incredibly wide ranging
Cacajao in the Neotropics (but see Ayres, 1989), today many
primate genera have been studied at a number of long-term
field sites. In this paper, I present data on diurnal variations
in black spider monkey activity budgets from a previously
unstudied focal study group in eastern Bolivia, and compare
these results with other long-term Ateles study sites.
Study Site
T he study was conducted in the Noel Kempff Mercado
National Park of 15,300 km² in the north-eastern corner
of Departmaento Santa Cruz, Bolivia (see Fig. 1). T he
Río Iteñez defines the park’s eastern and northern edges,
and represents the border with the neighboring Brazilian
states of Rondônia and Mato Grosso. T he region is situated
on the Brazilian Shield geological formation, which is
characterized by poor kaolinitic clay and podsol soils (PLUSCORDECRUZ, 1994; Peres, 1997). T he region has been
characterized by a marked dry season in the austral winter,
a mean annual temperature of c.26°C, and an annual
precipitation of c.1,600 mm (Wallace, 1998).
Figure 1. Map showing the location of the Noel Kempff Mercado
National Park, Bolivia.
Research was based at Lago Caiman (13°36’S, 60°55’W),
a large oxbow lake at the base of the northern tip of the
Huanchaca escarpment, and approximately 21 km upstream
from an international tourist centre “Flor de Oro”. A 400
ha study plot (2 x 2 km) with a grid system of trails spaced
every 100 m was set up approximately 3.5 km from camp.
Subsequently, trails were cut to include a further c.100 ha
to cover parts of the focal spider monkey community range
not encompassed by the 400-ha grid. T he Lago Caiman
study plot contained a number of structurally and floristically
distinct habitats: tall forest, low vine forest, sartenejal or
swamp forest, piedmont forest and cerrado forest (Wallace,
1998).
102
Neotropical Primates 9(3), December 2001
Methods
Following habituation, data was collected on the behavioral
ecology of a focal spider monkey community for 11 months
between June 1996 and April 1997. T he focal spider monkey
community was made up of approximately 55 individuals
at the beginning of data collection (June 1996). Subadults
were visibly smaller than adults and, following McFarland
Symington (1988a), were considered subadult until they
reached 80–90% the size of adults. All other young animals
were considered juveniles except infants that were carried
ventrally or laterally by their mothers.
Ateles has a fission-fusion social system and subgroup
size and composition change frequently throughout the
day (Chapman, 1990; McFarland Symington, 1988b; Van
Roosmalen, 1985). To control for this aspect of their
behavioural ecology I made individual monkeys the focus of
all-day follows. T hus, each month I attempted to follow four
adult females (F), four adult males (M), and one sub-adult
male (SAM) for a total of nine days during two temporally
distinct sessions of up to five days. Attempts were made to
randomize the data sampling regime; in the pre-dawn one of
five radio-collared males was randomly selected as the initial
spider monkey contact and a focal follow animal (FFA)
was selected from the animals present at the sleeping site.
Whenever possible the age/sex class of the FFA corresponded
with a randomly ordered list of the nine day standard
monthly sample.
number of animals included in any one scan depended on
subgroup size and ranged between 1–11 animals per scan. At
each scan, data on the following parameters were recorded:
climate, location and habitat type, subgroup size, spread,
and dominant activity, and the presence of other frugivorous
species, as well as the activity of each scanned individual
(Wallace, 1998).
Monthly activity budgets were calculated for each of
the following age/sex classes: adult and subadult females
combined, adult males, subadult males, and non-infant
juveniles. In order to provide information on diurnal activity
budgets each age/sex class sample was divided into hourly
intervals and calculated as follows:
(records for activity i)
x 100
(records for all activities)
where i = feeding, resting, travelling or other behaviours. An
average activity budget for the spider monkey community
was established by averaging the activity budget of the four
age/sex classes, weighted by their proportion within the focal
community.
Unless otherwise specified the data presented was analysed
using non-parametric statistical tests (Siegal and Castellan,
1988). T he standard probability level of p<0.05 was set,
although non-significant trends are also discussed.
Results and Discussion
FFAs were followed from dawn to dusk (approx. 0515– 0615
to 1745–1845). If an FFA was lost I continued with another
individual of the same age/sex class from the same subgroup.
If this was not possible I made attempts to rapidly locate
another subgroup and continue. T hese two scenarios were
considered ‘broken’ all-day follows. Occasionally it was not
possible to continue, either because the subgroup climbed the
inaccessible escarpment and/or it was not possible to rapidly
locate a second subgroup. T he day was then considered a
‘half ’ or ‘quarter’ day. If necessary AM ‘half ’ or ‘quarter’ days
were made up at a later stage with an afternoon follow on
the same age/sex class. Between January–March 1997 I was
unable to collect nine days of data due to illness and other
research commitments.
Point scan sampling (Altmann, 1974; Dunbar, 1976) at 15minute intervals was used to gather data on activity budgets,
diet and social behavior. Scans lasted five minutes and data
were collected on as many animals as possible. T he total
Age/Sex Class Activity Budget Variations
Overall, at Lago Caiman spider monkeys spend on average
18.9% of daylight hours feeding, 29.7% moving, 45.5%
resting, and 5.9% engaged in other activities such as
social behavior, vocalization, defecation and urination. T hus,
approximately half of the day is spent either resting or
engaged in other activities, with the other half divided
between feeding and moving. T he overall activity budget
displayed by the focal spider monkey community at Lago
Caiman appears to be fairly typical of previous long-term
studies of the genus (see Table 1).
Nevertheless, there were variations in activity budgets
between age/sex classes (see Fig. 2). Most strikingly, juveniles
spent over double the amount of time in ‘other’ activities than
other age/sex classes. Given that juveniles spent the majority
of the day in the same subgroup as their mother, I compared
juvenile and adult female time budgets. T here were no
Table 1. Comparison of activity budgets for five Ateles long-term study populations.
Activity
%
%
%
%
Feeding T ime
Moving T ime
Resting T ime
Other T imea
Bolivia1
Peru2
Colombia3
Brazil4
Venezuela5
18.9
29.7
45.5
5.9
29
26
45
no data
22.2
14.8
63
no data
18
36
45
no data
50.5
18.1
23.7
7.7
1
T his study (Ateles chamek ), 2McFarland Symington (1988b) (A. chamek ), 3Klein & Klein (1977) (A. belzebuth), 4Nunes (1995)
(A. belzebuth), 5Castellanos (1995) (A. belzebuth). aIncludes social and physiological function behavioral categories.
103
Neotropical Primates 9(3), December 2001
significant differences in monthly activity budget proportions
for feeding and moving, but resting and other behaviors
were significantly different (Rest - Wilcoxon T = 0, p<0.005,
N = 11; Other - Wilcoxon T = 0, p<0.005, N = 11). T he
majority of juvenile ‘other’ time was spent in play behavior
(77.8 %), which usually consisted of wrestling and chasing
involving up to five individuals. Indeed, juveniles were most
frequently observed playing together whilst their mothers
slept towards the end of prolonged rest periods.
60
50
40
30
20
10
Move
Rest
Other
Feed
0
Subadult males were also frequently observed playing (45.9%
of ‘other’ activities) and this accounts for the relatively
high ‘other’ portion of the activity budget. When monthly
activity budget proportions were compared with adult males
(see Fig. 1), subadult males spent significantly more time
moving and feeding and significantly less time resting (Move
- Wilcoxon T = 0, p<0.005, N = 11; Feed - Wilcoxon
T = 5, p<0.02, N = 11; Rest - Wilcoxon T = 0, p<0.005,
N = 11). T hese results may reflect the subordinate status of
subadult individuals (Eisenberg and Kuehn, 1966). Subadult
males may have to spend more time feeding because they are
restricted to fringe areas of fruiting resources. Alternatively,
these increases may be linked to the energetic costs of growth
(Dunbar, 1988). T he fact that they spend less time resting
than adult males is partly explained by the increases in
feeding and ‘other’ activities, but more so by the increase in
proportion of time spent moving. Subadult males and to a
lesser extent large juvenile males were frequently observed
in male-dominated subgroups which often appeared to be
patrolling the focal community home range extensively.
T his feature of spider monkey behavior has been previously
reported (Eisenberg, 1976; McFarland Symington, 1990)
and may represent a form of sub-adult male recruitment in a
male philopatric primate society.
Male
60
% Time
50
40
30
20
10
Move
Rest
Other
Feed
0
Activity
Subadult Male
60
% Time
50
40
30
20
10
Move
Rest
Other
Feed
0
Activity
Juveniles
60
% Time
50
40
30
20
10
Move
Rest
Other
Feed
0
Activity
Figure 2. Age/sex class variations in overall activity budgets.
Males spent significantly more time resting than females
(Wilcoxon T = 11, p<0.005, N = 11) and significantly
less time moving (Wilcoxon T = 7, p<0.05, N = 11),
whilst females spent more time feeding, although this was
only approaching significance (Wilcoxon T = 12, p = 0.07,
N = 11). Males and females showed very similar levels
of ‘other’ behaviors and this similarity extended to the
overall breakdown of the miscellaneous activities within this
category (Wallace, 1998). T he additional costs of lactation
and pregnancy offer the best explanation as to why females
spend more time feeding than adult males; however, an
explanation for the differences in resting and moving is
more problematical. One possibility is that females are forced
to travel at slower rates than adult males because of the
additional costs of carrying non-independent infants and
juveniles. Even in the case of females with independent
juveniles, the need to slow down and wait for these smaller
individuals may increase moving time, thereby cutting into
resting time.
Diurnal Activity Patterns
Diurnal variations in the spider monkey activity budget are
depicted in Figure 3. Spider monkeys show an initial early
morning peak in feeding, which then drops off, remaining
104
Neotropical Primates 9(3), December 2001
constant until mid-morning. Feeding behavior then falls
considerably until mid- to late afternoon when it increases
to a smaller peak. During this second period spider monkeys
are presumably attempting to maximize food ingestion prior
to the prolonged overnight fasting period (Chapman and
Chapman, 1991).
In a review of the genus, Van Roosmalen and Klein, 1988,
suggested that Ateles are selecting for dietary variability, with
subgroups consistently eating more than one fruit type per
follow day. In fact, patterns of diurnal dietary diversity
were apparent at Lago Caiman; spider monkeys appeared to
concentrate on one or two resources for most of the day and
then feed for brief periods on a greater variety of resources
towards the end of the day, especially on their way to the
sleeping site. T his observation could be seen as a way of
opportunistically maintaining a full stomach right up until
retiring for the long night. Alternatively, once daily energy
intake has been maximized Ateles may select for some dietary
diversity in order to provide a more varied nutrient and
mineral intake.
In Costa Rica, spider monkeys ingested relatively more
leaves immediately prior to periods of prolonged rest. T his
diurnal pattern of folivory has been attributed both to the
difficulty and added time involved in digesting folivorous
material, and of the need to maintain sufficient stomach
space for more energetically profitable fruit during foraging
sessions (Chapman and Chapman, 1991). T he tendency
for spider monkeys to consume folivorous material later in
the afternoon was also noted by Van Roosmalen (1985) in
Suriname. At Lago Caiman a similar diurnal pattern emerges
(see Fig. 4), with spider monkeys clearly consuming more
leaves in the afternoon, although a very early morning peak
in leaf eating also occurs. Folivory is usually rare and the
pattern may be less clear because of the months where leaf
eating was more important. T hus, I examined the diurnal
distribution of the start times of all observed leaf feeding
sessions (see Fig. 5), and this shows a much more dramatic
pattern which concurs with the above hypothesis.
An alternative explanation regarding diurnal patterns of
leaf consumption by primates was suggested by Ganzhorn
and Wright (1994). T heir results only partially supported
the hypothesis that temporal variations in folivory might
be linked to varying diurnal protein concentrations in leaf
material. However, species which are maximizing energy
intake (in the form of sugars) should apparently eat leaves
late in the day (Ganzhorn and Wright, 1994), as spider
monkeys seem to do. Most folivorous material consumed was
FEEDING
OTHER
8
28
26
7
24
22
% Time
% Time
6
20
18
5
16
14
4
12
3
10
06:00 07:00 08:00 09:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00 17:00
RESTING
60
55
% Time
50
45
40
35
30
06:00 07:00 08:00 09:00 10:00 11:00 12:00 13:00 14:00 15:00 16:00 17:00
Sample Hour
Figure 3. Diurnal variations in spider monkey activity budgets.
105
Neotropical Primates 9(3), December 2001
the younger leaves of several high canopy liana species, along
with young leaves of a few tree species (Wallace, 1998). T his
pattern of leaf selection is similar to several primate species
including Ateles (Van Roosmalen, 1985; Chapman, 1987;
Castellanos, 1995). Young leaves are known to be easier to
digest than those more mature (Hladik, 1978), contain fewer
toxins (McKey et al., 1981), higher levels of protein and
energy (Milton, 1982), and may also be an important source
of minerals and nutrients such as potassium, magnesium,
phosphorus and nitrogen (Waterman, 1984).
Time spent moving shows two pronounced peaks, one in
the very early morning and another in mid to late afternoon
as spider monkeys are traveling from and to sleeping sites
respectively. From an energy conserving point of view these
two periods represent the coolest times of the day and
travel costs would thus be significantly reduced. Otherwise
time spent traveling remains fairly constant and the overall
pattern of moving is inversely related to the diurnal pattern
of resting. Resting time increases throughout the day
showing a first peak in the mid-morning (0900 –1000) by
which time monkeys may well have filled their stomachs.
A second more pronounced resting peak occurs at midday
continuing into early afternoon (1200 –1400), before
dropping off dramatically later in the day. T his second
peak dominates the activity budget at this time of day and
is best explained by the corresponding peak in ambient
temperatures which, along with high humidity levels,
Climatic Effects on Activity Patterns
Extremes in the ambient temperature also affected diurnal
activity budgets, for example, during the mid-austral winter
cold southerly winds can occasionally lower temperatures
to as little as 6°C. In such conditions spider monkeys
often remained resting in overnight sleeping sites or high
up in large emergents for 3 – 4 hours after day break, as if
waiting for the day to warm up and/or maximizing insolation
potential. On one extremely cold and wet morning (28 June
1996) the focal subgroup remained motionless until as late
as 13:00 hrs.
As has been demonstrated for other diurnal arboreal primate
species (Raemakers, 1980; Barrett, 1995), rainfall also affected
spider monkey behavior. Although during light drizzly rain
the spider monkeys continue apparently unaffected (unless
also particularly cold at the time), more typical heavy tropical
downpours result in the monkeys taking shelter and resting
motionless until the rain stops. In summary, the focal follow
animal's subgroup was dominated by resting individuals in
76% of those scan samples that occurred during rainfall.
Two other behaviors were directly associated with rain,
firstly, a ‘bathing’ form of autogrooming was often witnessed
during and immediately following rainfall, especially if the
rainfall was the first for several days. T his behavior has
been previously reported for free-ranging spider monkeys
(Eisenberg and Kuehn, 1966) and is particularly notable
given the relatively low grooming frequencies displayed by
spider monkeys at Lago Caiman (1% of the overall activity
budget), and in general (Symington, 1988a; van Roosmalen
and Klein, 1988).
20
15
% Feed
presumably inhibits thermoregulation, thereby discouraging
strenuous activity such as travel. Overall these patterns are
fairly typical for diurnal primate species living in tropical
conditions (Clutton-Brock, 1977), and extremely similar
to those documented for Ateles paniscus in Suriname (Van
Roosmalen and Klein, 1988).
10
5
0
4
3
2
1
5
7
6
Hour No
8
9
10
11
1
Figure 4. Diurnal variations in degree of folivory in the spider
monkey diet.
No. Leaf Feeding Bout Starts
50
40
30
20
10
0
1
2
3
4
5
6
7
8
9
10
11
1
Hour No
Figure 5. Distribution of start times for folivory patch feeding
sessions.
T he second behavior was rare but extremely dramatic;
several pilo-erecting adult and subadult males would
repeatedly charge around particularly open and connected
emergent and upper canopy trees. T his movement included
running but was dominated by brachiating and, along
with inter-community disputes, was the fastest that spider
monkeys were ever seen traveling during the study. On the
few occasions this behavior was witnessed it appeared to
correlate with the coming of rains, which often also brought
heavy winds. T he fact that only males were observed in this
activity suggests the possibility that this behavior serves as
an intra-community male display. Intriguingly, an extremely
similar behavioral response to the arrival of rains has been
described for adult male chimpanzees (Pan troglodytes) at
Gombe (Goodall, 1986) and termed a ‘rain dance’. Spider
monkeys and chimpanzees have been frequently compared
in the past due to the fission-fusion nature of their social
systems (McFarland Symington, 1990, Chapman et al.,
1995).
106
Acknowledgements
T his research was funded by the Wildlife Conservation
Society (WCS) through a grant from the Bolivian Sustainable
Forestry Project (BOLFOR), which is jointly financed
through USAID and the Bolivian Government. I would like
to thank the Bolivian National Secretariat for Protected Areas
for permission to work in Noel Kempff Mercado National
Park and the National Directorate for the Protection of
Biodiversity for help in acquiring necessary research permits.
Field work was also facilitated through logistical support
from the Fundación Amigos de la Naturaleza (F.A.N.). Many
thanks to the following individuals who helped during field
work: Lilian Painter, William Karesh, Damian Rumiz, Chris
Stromquist, Angel Saldania, Nicolas Tagua, Walter Perez,
Bonifacio Mostacedo. A special debt of gratitude to Jose
Chuvina, my research assistant.
Robert B. Wallace, Wildlife Conservation Society, 185 th
Street and Southern Boulevard, Bronx, New York 10460,
USA. Address for correspondence: Wildlife Conservation
Society – Madidi, 3-35181, San Miguel, La Paz, Bolivia,
e-mail: <wcsmadidi@mail.zuper.net>.
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DISTRIBUCIÓN PARCIAL DEL TITÍ GRIS ( SAGUINUS
CALLITRICHIDAE ) EN EL D EPARTAMENTO
DE ANTIOQUIA, C OLOMBIA
LEUCOPUS,
Carlos A. Cuartas-Calle
Introducción
Saguinus leucopus fue descripto en la localidad tipo de
Medellín (Bella Villa) departamento de Antioquia por Günter
(1877), la especie era muy numerosa en dicho poblado.
El crecimiento de la población humana y la construcción de
vías y sitios de vivienda fueron acabando con los remanentes
de bosque y aislando y desplazando a las poblaciones de tití
gris amenazando la permanencia del tití en dicho hábitat.
Los últimos grupos de S. leucopus fueron observados en la
ciudad de Medellín en la década del treinta (1930 –1940), a
partir de dicha fecha no se volvió a saber de la especie, la cual
fue diezmada de su localidad tipo.
Saguinus leucopus es un primate endémico de Colombia,
tiene como zona de distribución el Norte del país, entre la
parte baja del Río Cauca y el Valle Medio del Río Magdalena
(Hernández-Camacho y Cooper, 1975, Hernández-Camacho
y Defler, 1983). Según Cuervo et al., (1986) la especie
se distribuye desde el Oriente de Caldas, Norte del
Tolima, Antioquia (en el Bajo Cauca y Nechí, y la Hoya
del Magdalena). Eisenberg (1989) la ubica en el Valle
del Río Magdalena, centro y norte de Colombia, en la
margen izquierda del Río Magdalena en el departamento
de Antioquia, y en los departamentos de Bolívar y Tolima.
Emmons y Feer (1998) la distribuyen al Oriente de los
Andes en el piedemonte de la Cordillera Central, entre la
margen Oriental del Río Cauca (Bajo Cauca) y la margen
Occidental en la parte media del Río Magdalena. También se
distribuye en zonas poco anegadizas al Sur del departamento
de Bolívar y sectores del Norte del Departamento de Caldas
en el corregimiento de Norcasia, y el corregimiento de
Guarinó en la parte media y alta de la Quebrada la Burra
entre los municipios de Dorada y Honda (observación
personal); como también en el sector “Arizona” municipio
de La Dorada, Departamento de Caldas, y el sector “San
Antonio” municipio de Samaná, Departamento de Antioquia
(Vargas y Solano, 1996). Esta especie está catalogada por
la UICN y US-ESA (1994) CIT ES como “En Peligro de
Extinción”, debido a tres variables: Su marcado endemismo,
su rango de distribución restringido (uno de los más reducidos
entre los primates del mundo), y la severa reducción y
destrucción de su hábitat.En el departamento de Antioquia,
aún se conservan bosques primarios, primario intervenido
y bosques secundarios, con áreas relativamente extensas que
albergan poblaciones de esta especie, pero lastimosamente a
la fecha no se han creado áreas de reserva para la protección
y conservación de S. leucopus.
Area de Estudio
Durante el período 1995–1998 se realizaron varios inventarios
de mamíferos en la margen Oriental del Río Cauca, en las
subregiones del Bajo Cauca, Nordeste, Norte, Magdalena
Medio y Oriente del departamento de Antioquia, en áreas
con jurisdicción de CORNARE (Corporación Autónoma
Regional de los Ríos Negro y Nare) y CORANT IOQUIA
(Corporación Autónoma Regional del Centro de Antioquia).
Se visitaron 40 veredas pertenecientes a 17 municipios, con
alturas entre los 30 y 1600 msnm, y zonas de vida de bosque
húmedo tropical (bh-T ) hasta bosque pluvial premontano
(bp-PM) (Figura 1 y Tabla 1).
Resultados y Discusión
En este estudio preliminar de la distribución de S. leucopus en
el departamento de Antioquia, se observaron 95 grupos con
un total de 719 individuos (Tabla, 1). También se detectó la
presencia de otros primates como: Cebus albifrons, Alouatta
seniculus, Ateles sp. y Aotus lemurinus.
Basado en las observaciones de campo, la distribución
geográfica de S. leucopus al Sur de Antioquia, corresponde
a la margen derecha del Río Cauca, en los límites con
el departamento de Caldas (Río Samaná, municipios de
Nariño, Argelia y Sonsón), y a la margen izquierda del Río
Magdalena, en los límites con el departamento de Boyacá
(municipios de Puerto Triunfo). Al Norte se distribuye en
límites de los departamentos de Bolívar (municipios de
El Bagre y Nechí), y Sucre (municipio de Caucasia) en
la margen derecha de los Ríos Cauca y Porce (Figura 1).
Los grupos de Tití, se observaron en bosques primarios,
primarios intervenidos, secundarios y rastrojos altos y en
bosques ribereños.
Los bosques primarios observados se caracterizan por la
presencia de un estrato emergente disperso formado por
grandes árboles que superan los 30 m de altura y cobertura
total mayor del 90%. Los bosques primarios intervenidos
presentan coberturas mayores del 90% y alturas entre 7 y
30 m. Las lianas y trepadoras tienen densidades medias. Los
bosques secundarios con estados sucesionales medio y tardío
presentan alturas entre 5 y 20 m y una cobertura total del
70%. Los estratos arbustivos muestran coberturas del 50% y
108
Neotropical Primates 9(3), December 2001
T abla 1. Grupos y número de individuos de Saguinus leucopus observados en los municipios y veredas visitadas en el departamento de
Antioquia, Colombia.
Municipio
Vereda
Coordenadas
Nechí
Las Flores
8°6’N; 74°44’O
Altura
Z. V.
Bosque
G
N° Ind.
30
bh-T
Bpi, Bs, Ra
2
15
El Bagre
Amaceri
7°45’N; 74°40’O
50
bh-T
Bpi, Bs, Ra
2
16
Zaragoza
Dos Bocas
7°28’N; 74°50’O
80
bh-T
Bpi, Bs, Ra
3
21
Anorí
Liberia
7°23’N; 75°31’O
200
bh-T
Bp, Bpi
5
40
Santiago
7°10’N; 75°13’O
1120
bp-MB
Bp, Bpi, Bs
3
17
Las Juntas
7°12’N; 75°11’O
900
bp-PM
Bp, Bpi
4
40
El Jardín
7°25’N; 74°45’O
850
bh-PM
Bp, Bpi, Bs
3
20
La Vetilla
7°12’N; 74°53’O
540
bh-T
Bp, Bpi
3
26
Arenas Blancas
6°52’N; 74°51’O
1060
bh-PM
Bpi, Bs, Ra
2
16
Los T oros
7°8’N; 75°3’O
400
bh-T
Bpi, Bs, Ra
3
25
Yarumal
El Cedro
7°13’N; 75°18’O
800
bp-T
Bs, Ra
1
8
Sto. Domingo
Los Naranjos
6°40’N; 75°12’O
1450
bp-MB
Bs, Ra
1
5
San Roque
San José del Nús
6°30’N; 74°45’O
400
bh-T
Bpi, Bs, Ra
2
14
La T rinidad
6°32’N; 74°40’O
450
bh-T
Bs, Ra
2
10
La Clara
6°20’N; 75°10’O
1500
bp-MB
Bs, Ra
1
7
Amalfi
Concepción
La Sonadora
6°18’N; 75°9’O
1600
bp-MB
Bs, Ra
1
5
San Rafael
Jaguas
6°21’N; 74°48’O
600
bh-T
Bpi, Bs, Ra
3
23
San Carlos
La Florida
6°15’N; 75°0’O
1400
bh-PM
Bpi, Bs, Ra
1
6
Las Camelias
6°17’N; 75°3’O
1400
bh-PM
Bpi, Bs, Ra
1
5
Miraflores
6°9’N; 74°40’O
500
bh-T
Bp, Bpi, Bs
5
45
El Prado
6°10’N; 74°42’O
450
bh-T
Bp, Bpi, Bs
6
50
La Aguada
6°16’N; 74°55’O
700
bh-T
Bp, Bpi, Bs
2
13
Cocalito
6°12’N; 74°58’O
1100
bh-PM
Bs, Ra
1
7
San José
6°11’N; 74°45’O
970
bh-T
Bpi, Bs, Ra
3
24
Santa Elena
6°12’N; 74°56’O
1100
bh-PM
Bs, Ra
2
16
La Gaviota
6°4’N; 75°4’O
1400
bh-PM
Bs, Ra
1
5
San Francisco
6°3’N; 75°4’O
1200
bh-T
Bs, Ra
1
7
La María
6°5’N; 75°5’O
900
bh-T
Bs, Ra
2
16
El T ablazo
6°1’N; 75°6’O
700
bh-T
Bpi, Bs, Ra
4
32
El Prodigio
6°7’N; 74°45’O
470
bh-T
Bpi, Bs, Ra
1
6
Las Confusas
6°4’N; 74°42’O
320
bh-T
Bp, Bpi, Bs
4
30
Playa Rosa
6°2’N; 74°40’O
360
bh-T
Bpi, Bs, Ra
2
13
Puerto Perales
6°0’N; 74°39’O
200
bh-T
Bs, Ra
4
30
Las Mercedes
5°56’N; 74°45’O
350
bh-T
Bs, Ra
3
27
Río Claro
5°58’N; 74°48’O
400
bh-T
Bpi, Bs, Ra
2
15
La Soledad
5°45’N; 75°15’O
1200
bp-PM
Bs, Ra
1
5
El Arenal
5°43’N; 75°10’O
1000
bh-T
Bpi, Bs, Ra
2
14
Granada
San Luis
PuertoT riunfo
Sonsón
Playa Rica
5°41’N; 75°9’O
950
bh-T
Bp, Bpi, Bs
3
24
Argelia
San Pablo
5°40’ N; 75°0’O
800
bh-T
Bpi, Bs, Ra
2
16
Nariño
Samaná
5°32’ N; 75°7’O
800
bh-T
Bpi, Bs, Ra
1
5
95
719
Total
Convenciones: Z.V: Zona de vida; G: Grupos observados; N° ind: individuos observados; bh-T : Bosque húmedo tropical; bp-MB:
Bosque pluvial montano bajo; bp-PM: Bosque pluvial premontano; bh-PM: Bosque húmedo premontano; Bp: Bosque primario;
Bpi: Bosque primario intervenido; Bs: Bosque secundario; Ra: Rastrojo alto.
Neotropical Primates 9(3), December 2001
109
Las Juntas por la quebrada La Trinidad) municipio de Amalfi
(veredas La Vetilla, Los Toros, rodeando la cuenca del Río
Tinitá); municipio de San Carlos sector de Samaná (veredas
Miraflores, El Prado y San José); Municipio de San Rafael
(vereda Jaguas); Municipio de San Luis (Las Confusas). Las
características que presentan estos bosques son el tamaño, la
vegetación, la oferta de alimento y refugios y corredores que
comunican con otros fragmentos facilitando el intercambio
de individuos entre poblaciones.
En las diferentes subregiones donde se detectó la presencia de
S. leucopus se presentan diferentes actividades de explotación
a saber:
José Bernardo Barreiro Luna
Figura 1. Saguinus leucopus (tití gris).
alturas entre 3 y 6 m. Finalmente el matorral alto tiene una
altura entre 1.5 y 7 m y sus copas se proyectan cubriendo el
60% del sustrato. En el trabajo de campo se pudo observar
algunas plantas utilizadas por S. leucopus para alimento
(Tabla, 2).
Saguinus leucopus se observó utilizando diferentes tipos de
hábitats, con preferencia por los bosques primarios, primarios
poco intervenidos y secundarios de sucesión tardía. En
estos hábitats, de denso follaje y oquedades en los troncos,
encuentra alimento, buen refugio de sus predadores naturales
y sitios de anidación y descanso. También se lo observó
utilizando los bosques secundarios muy intervenidos y
rastrojos altos para alimentarse y para desplazarse a otros sitios
o parches de bosque más densos donde se establecía o buscaba
alimento. Se pudo observar un grupo conformado por siete
individuos en un palo de naranjo consumiendo dicho fruto
(vereda Cocalito) en un bosque muy intervenido.
En varias ocasiones se observó que para desplazarse de un
parche a otro el tití gris tenía que atravesar potreros, poniendo
en más riesgo su existencia. En una ocasión se pudo ver un
perro cazando y dándole muerte a un ejemplar ya que eran
presa fácil en el suelo (El Cedro, quebrada Santa Barbara).
Esto hace pensar en la necesidad de recuperación de franjas
de potreros y zonas boscosas degradadas para adecuarlas
como corredores naturales y sitios de alimento y paso a otros
parches más densos.
Los bosques primarios y primarios intervenidos cubren áreas
considerables en los municipios de Anorí (sector de Liberia y
Subregión del Bajo Cauca : Hasta el año 1964 la región del
Bajo Cauca fue zona de reserva forestal y estaba cubierta casi
en su totalidad por bosques primarios, pero por solicitud
del INCORA (Instituto Colombiano de Reforma Agraria)
y en virtud de la Ley 019 de 1964 el sector desde el Río
Nechí hasta el Río Cauca fue declarado área de colonización,
dejando áreas pequeñas como reserva en los municipios
de Nechí, El Bagre y Zaragoza. En 1973 gran parte de
la vegetación fue destruida y adecuadas las tierras para
ganadería. La ganadería fue reemplazada por la minería,
resultando en la destrucción de los potreros, principalmente
por la minería de aluvión mecanizada en tierra y agua. A la
fecha, esta subregión solo presenta unos pocos remanentes de
bosque.
Subregión del Nordeste: En el municipio de Anorí, sector de
Liberia, se practica la minería de aluvión mecanizada; es
preocupante el futuro de estos bosques ya que la región es
altamente minera y la penetración a esta zona boscosa es
inminente. En Santiago, la actividad consiste en cultivos,
y ganado, así como la extracción y extracción de madera.
Las Juntas presenta un bosque bien conservado, con poca
actividad de extracción y pocas áreas para ganadería. En el
municipio de Amalfi se practica la minería mecanizada y
de veta. En la vereda Arenas Blancas hay gran explotación
maderera. En la vereda los Toros se practica minería y
ganadería intensiva. En la vereda La Vetilla se presenta
explotación minera y en la vereda El Jardín explotación
maderera. En los municipios de Santo Domingo y San
Roque, se presentan áreas de ganadería y cultivo, los bosques
mejor conservados en San Roque están ubicados en las
márgenes del río Nús.
Subregión del Norte: En el Municipio de Yarumal, vereda
El Cedro, los bosques se encuentran en la margen derecha
e izquierda de la quebrada Santa Bárbara; esta zona se
caracteriza por la dominancia de potreros para ganadería y
agricultura, y en el futuro serán inundados por un proyecto
hidroeléctrico.
Subregión del Magdalena Medio: El Municipio de Puerto
Triunfo, con la apertura de la autopista Medellín-Bogotá,
ha sido muy intervenido, especialmente para extracción de
madera. Puerto Perales presenta explotación petrolera, los
bosques están conservados y cuidados, pero se consideran
110
Neotropical Primates 9(3), December 2001
T abla 2. Plantas visitadas y partes consumidas por Saguinus leucopus.
Familia
Especie
N. Vulgar
Consumen
Anacardiaceae
Anacardium excelsum
Spondias mombin
Mangifera indica
Tapirira guianensis
Aspidosperma dugondi
Bombacopsis aquinata
Ceiba pentandra
Ochroma lagopus
Bursera simaruba
Protium nodulosum
Brownea macrophylla
Sterculia apetala
Laetia procera
Uribea tamarindoides
Inga spectabilis
Inga sp.
Inga sp. 1.
Bellucia axinanthera
Ficus americana
Ficus insipida
Psidium guajava
Myrcia sp.
Eugenia sp.
Bactris minor
Pouteria multiflora
Caracoli
Jobo
Mango
Fresno
Carreto
Ceiba
Ceiba
Balso
Almácigo
Anime
Arizal
Piñón
Saino
T amarindo de mico
Guaimaro
Guamo de monte
Guamo bejuco
Guayabo de monte
Suán
Higuerón
Guayaba
Arrayán
Arrayán
Corozo de lata
Caimito castaño
F, Ht, Yf, P
H, F(c p)
F(c p)
Fruto entero
Frutos tiernos
Hojas
Hojas tiernas
Fruto entero
F, Yf, P
F (pulpa)
Hojas, Flores
Hojas, Flores
F, Fl, H
F(arilos)
Hojas, Flores
Fruto(pulpa)
Fruto(pulpa)
Fruto entero
Hojas, Flores
Frutos, Flores
Fruto entero
Fruto entero
Fruto entero
F(c p)
Fruto (pulpa)
Apocynaceae
Bombacaceae
Burseraceae
Caesalpinicidea
Esterculiaceae
Flacourtiaceae
Leguminosae
Mimosoideae
Melastomataceae
Moraceae
Myrtaceae
Palmae
Sapotaceae
Convenciones: F: fruto entero; Ht: hojas tiernas; Yf: yemas foliares; P: peciolos; H: hojas; F(cp): del fruto consumen la cascara y pulpa;
Fl: flor.
islas ya que están bordeados por potreros extensivos para
ganadería. En Las Mercedes el bosque lo tienen protegido y
lo conservan como protector de la microcuenca El Corozal.
En la vereda Río Claro varios de los bosques son protegidos
y cuidados por sus propietarios; en áreas aledañas a estos
bosques se presenta extracción de madera y explotación de
minas karsticas (mármoles y calizas).
Subregión del Oriente: Se caracteriza principalmente por la
extracción de madera. En Sonsón, vereda La Soledad, hay
destrucción de los bosques y se hacen cultivos de café, caña
y extracción de madera para cocina. Las veredas El Arenal y
Playa Rica presentan poca ganadería, se queman parches de
bosque para cultivo de maíz y caña. El sector de La Danta es
protegido y se presenta poca extracción de madera, aunque
se observan pequeños áreas para ganado. Municipio de San
Carlos, veredas El Prado, Miraflores y San José presentan gran
explotación maderera y potreros ganaderos. En el municipio
de San Luis se presenta gran explotación maderera.
Es preocupante el futuro de S. leucopus, ya que el área de su
distribución está siendo alterada y fragmentada a un ritmo
acelerado. Estos hábitats naturales han sido fuertemente
afectados por la actividad humana, ya que ofrecen
condiciones para la explotación maderera, expansión
de tierras para cultivos y ganadería, apertura de vías,
explotación minera y construcción de embalses. La situación
se agrava por no existir un control en el manejo y uso de la
tierra ni áreas de reserva para la protección y conservación
de la especie.
La fragmentación de los bosques tendrá consecuencias
drásticas sobre la distribución de esta especie ya que
puede resultar en extinciones locales. La degradación y
fragmentación de los ecosistemas están creando “islas” de
áreas naturales en las que las poblaciones se están aislando
de sus congéneres de otras partes. En parches de bosque
suficientemente grandes se puede mantener poblaciones con
una tasa baja de extinción; pero cuando los parches son muy
pequeños y aislados, estos mantienen poblaciones pequeñas,
decrece la tasa de colonización y de intercambio genético por
lo que la extinción puede llegar a ser alta.
Conectar habitats fragmentados sería una de las soluciones
a corto plazo, lo cual reduciría las posibilidades de extinción
por efecto del aislamiento, por lo que se. Se propondrían
corredores de hábitat (Corredor a Escala de Mosaico de
Paisaje) que conectarían hábitats aislados y promoverían
procesos de movimiento y colonización entre fragmentos,
permitiendo un flujo de genes entre diferentes grupos y
poblaciones. Estos corredores deben ser amplios y grandes
para facilitar el movimiento de manera estacional o cotidiana.
Los corredores conectarían parches separados a través de
largas franjas de bosque, como bosque ribereño a lo largo
de ríos, quebradas y riachuelos o hábitats de montañas. Para
establecer los corredores se deben tener en cuenta factores
111
Neotropical Primates 9(3), December 2001
adicionales como la estructura del hábitat, la existencia de
árboles con huecos para resguardo y forrajeo.
Es urgente que las corporaciones y entidades encargadas
creen áreas de reserva para la protección y conservación de
la especie. Son varios los bosques que pueden ser protegidos
para asegurar la supervivencia de esta especie, ya que existen
áreas extensas de bosque primario, primario poco intervenido,
bosques secundarios de sucesión media y tardía, entre los
cuales están los de Anorí, Liberia, Samaná, San Carlos, San
Luis, Sonsón y Amalfi.
Carlos A. Cuartas-Calle, Depto. de Biologia, Universidad
de Antioquia, A.A.1226, Medellin, Colombia.
howler monkeys, Alouatta fusca , observed during a study
of their behaviour and ecology carried out at the Intervales
State Park, São Paulo, from November, 1998 to October,
1999 (Steinmetz, 2000).
T he Intervales State Park projects 49,888 ha of Atlantic
rain forest in the state of São Paulo, Brazil (24°12’–24°25’S,
48°03’– 48°30’W). T he climate there is temperate, with an
annual precipitation above 1.000 mm and no dry season. T he
average temperature is 18°C in the coldest month and 22°C
in the hottest month (Petroni, 2000). During the year of
study (November 98 to October 99) the average temperature
was 16.2°C and the total precipitation was 1.707,82 mm
(data collected in the Intervales State Park) (Fig. 1).
Referencias
DRINKING BY H OWLER MONKEYS ( ALOUATTA FUSCA)
AND ITS SEASONALITY AT THE INTERVALES STATE
PARK, SÃO PAULO, BRAZIL
Sandra Steinmetz
Introduction
Drinking is only infrequently observed in howler monkeys
(Bicca-Marques, 1992; Bonvicino, 1988; Carpenter, 1934;
Glander, 1975, 1978; Moynihan, 1976; Terborgh, 1983)
and it is argued that their diet provides the majority of fluids
they need (Glander, 1978). In this note I report on the
occurrence of drinking in a population of southern brown
Precipitation
Temperature
25
20
15
10
5
0
400
Precipitation
(mm)
Cuervo, D. A., Hernández-Camacho, J. y Cadena, A.
1986. Lista actualizada de los mamíferos de Colombia.
Anotaciones sobre su distribución. Caldasia 15(71–75):
472–501.
Emmons, L. H. y Feer, F. 1998. Neotropical Rainforest
Mammals, Second Edition. A Field Guide. University of
Chicago Press, Chicago.
Eisenberg, J. F. 1989. Mammals of the Neotropics the Northern
Neotropics, Volume 1. Panamá, Colombia, Venezuela, Guyana,
Suriname, French Guiana . T he University of Chicago Press.
Chicago and London.
Hernández-Camacho, J. y Cooper, R. 1976. T he nonhuman primates of Colombia. In: Neotropical Primates:
Field Studies and Conservation, R. W. T horington, Jr. y
P. G. Heltne (eds.), pp.35– 69. National Academy of
Sciences, Washington, DC.
Hernández-Camacho, J. y Defler, T. 1983. Algunos aspectos
de la conservación de primates no humanos en Colombia.
In: La Primatología en Latinoamérica, C. Saavedra, R. A.
Mittermeier y I. B. Santos (eds.), pp.67–97. World Wildlife
Fund, Washington, DC.
Vargas, T. N. y Solano, C. L. 1996. Evaluación del estado
de dos poblaciones de Saguinus leucopus para determinar
áreas potenciales de conservación en un sector del valle
del Magdalena Medio, Colombia. Neotrop. Primates 4(1):
13 –15.
300
200
100
0
N D J F M A M J
J A S O
Months
Figure 1. Monthly average temperature and cumulative precipitation
registered at Intervales State Park, São Paulo, November and
December of 1998 and January to October of 1999.
Methods
T he activity budget and diet of a group of six individuals,
composed of two adult males, one juvenile male, one female
and one infant, were registered by monthly scan sampling
from November, 1998 to October, 1999. Direct observations
of the group totalled 918:30 hours or 92 days, of which
65 were full days. All observations of the howlers drinking
water were noted. To verify differences between the light
rainy season (April to August) and the heavy rainy season
(September to March), the monthly percentages were
compared using the Mann-Whitney “U” test. T he Spearman
coefficient was used for the correlations and significance was
set at the 0.05 level.
Results and Discussion
Drinking was observed 79 times (Table 1). In all instances the
howlers drank water accumulated in epiphytic bromeliads.
T hey were seen drinking more often in the lighter rainy
season (Mann-Whitney ‘U’ = 35.000; p = 0.0025) (Table
1). Occurrences of drinking were negatively correlated with
precipitation and temperature (r = -0.642; p = 0.0244
and r = -0.6103; p = 0.0351, respectively). Drinking was
positively correlated with the consumption of old leaves, and
they drank less often when more fruit was eaten (Pearson
correlation, r = 0.7231; p = 0.0079, r = -0.6208; p = 0.0312,
respectively) (Figs. 2 and 3).
112
Neotropical Primates 9(3), December 2001
T able 1 . T otal number of observations, mean of observations per
month and standard deviation (SD ) of drinking of howler
monkeys, Alouatta fusca , in two seasons, and throughout the
study (November 1998 to October 1999) at the Intervales State
Park, São Paulo.
Season
Number of
observations
Mean
SD
69
10
79
13.80
1.43
6.58
9.36
1.13
8.55
Less rainy
Most rainy
T otal
Number of observations
30
25
20
15
10
5
0
N
D
J
F
M
A
M
J
J
A
S
O
Months
Figure 2. Monthly variation of the number of observations of
drinking behaviour in howler monkeys, Alouatta fusca , between
November 1998 and October 1999, at Intervales State Park, São
Paulo.
Old leaves
Fruits
% of Diet
80
60
40
20
0
N
D
J
F
M
A
M
J
J
A
S
O
Months
Figure 3. Monthly percentile of old leaves and fruits in the diet
of howler monkeys, Alouatta fusca , between November 1998 and
October 1999, at Intervales State Park, São Paulo.
Glander (1978) also found a seasonal pattern in drinking
behaviour correlated with the consumption of old leaves.
Besides a reduced availability of water, old leaves have more
secondary compounds that, after the detoxification process,
produce metabolites that require water for their elimination
(Glander, 1978). At Intervales, the howlers have no difficulty
in finding water because of the abundance of bromeliads and
the absence of a defined dry season. Drinking seems to be
related to the kind of food consumed: fruits have more water
and less secondary compounds than old leaves. However, in
Alegrete, Rio Grande do Sul State, Brazil, a place with drastic
dry seasons, Bicca-Marques (1992) noted that howlers
consumed more water in the rainy season, and that drinking
behaviour was not related to diet.
Sandra Steinmetz, Departamento de Zoologia, Instituto
de Biociências, Universidade de São Paulo, Cidade
Universitária, 05508-900 São Paulo, São Paulo, Brazil.
Address for correspondence: Rua Marie Satzke 172, 04664-150
São Paulo, São Paulo, Brazil, e-mail: <steinmet@usp.br> or
<sandra@ambientalconsulting.com>.
References
Bicca-Marques, J. C. 1992. Drinking behavior in the
black howler monkey (A. caraya ). Folia Primatol. 58(2):
107–111.
Bonvicino, C. R. 1988. Observações sobre a ecologia e o
comportamento de Alouatta belzebul (Primates: Cebidae)
na Mata Atlântica. Dissertação de Mestrado, Universidade
Federal da Paraíba, João Pessoa.
Carpenter, C. R. 1934. A field study of behavior and
social relations of howling monkeys (Alouatta palliata ).
In: Naturalistic Behavior of Nonhuman Primates, C. R.
Carpenter (ed.), pp.3–92. Pennsylvania State Press, PA.
Glander, K. E. 1975. Habitat description and resource
utilization: A preliminary report on mantled howling
monkey ecology. In: Socioecology and Psychology of Primates,
R. Tuttle (ed.), pp.37–57. T he Hague, Mouton.
Glander, K. E. 1978. Howling monkey feeding behavior
and plant secondary compounds: A study of strategies.
In: The Ecology of Arboreal Folivores, G. G. Montgomery
(ed.), pp.561–574. Smithsonian Institution Press,
Washington, DC.
Moynihan, M. 1976. The New World Primates.
Princeton University Press, Princeton.
Petroni, L. M. 2000. Caracterização da área de uso
e dieta do mono carvoeiro (Brachyteles arachnoides,
Cebidae-Primates) na Mata Atlântica, Serra de
Paranapiacaba, SP. Tese de Doutorado, Universidade
de São Paulo, São Paulo.
Steinmetz, S. 2000. Ecologia e o comportamento do
bugio (Alouatta fusca clamitans, Atelidae - Primates)
no Parque Estadual Intervales – SP. Dissertação de
Mestrado, Universidade de São Paulo, São Paulo.
Terborgh, J. 1983. Five New World Primates: A Study
in Comparative Ecology. Princeton University Press,
Princeton, NJ.
USO DE P LANTAS C OMO ALIMENTO POR MONOS
AULLADORES, ALOUATTA PALLIATA, EN EL PARQUE
YUMKÁ, TABASCO, MÉXICO
Yasminda García del Valle
David Muñoz
Miguel Magaña-Alejandro
Alejandro Estrada
Berenice Franco
Introducción
El estado de Tabasco en el sur de México resguarda
poblaciones representantes de las tres especies de primates
que existen en México: Alouatta palliata, A. pigra y Ateles
geoffroyi (Smith; 1970, Horwich and Johnson 1986;
Rylands et al., 1995). Tabasco es el único estado de México,
113
Neotropical Primates 9(3), December 2001
y la única zona de la región Mesoamericana, en donde
podemos encontrar representantes de las tres especies de
primates y resguarda la zona de transición entre A. palliata
y A. pigra y en algunas localidades las dos especies son
simpátricas (Smith, 1970). Cerca del 60% de la superficie
del estado estaba originalmente cubierta por selvas, pero
como resultado de la actividad humana en Tabasco, cerca
del 80% de esta vegetación ha desaparecido a una tasa de
600 km2 ó más al año, siendo las tierras bajas en donde ha
ocurrido la mayor transformación de la selva a pastizales y
otros agrosistemas (Masera, 1996 México, SEMARNAP,
1999, INEGI, 1996).
Aunado a la desaparición de las selvas en Tabasco, hay una
falta de información acerca de la distribución geográfica
actual y tamaño de las poblaciones de las tres especies de
primates. Igualmente faltante son datos sobre su historia
natural, ecología, conducta y estado de conservación. Entre
estos estudios, aquellos relacionados a la ecología alimentaria
de los aulladores aportan información fundamental para
determinar los recursos que son capaces de utilizar estos
primates como fuente de alimento. Tales datos son
importantes no sólo como aspectos de la historia natural de
las especies, pero también como indicadores de los conjuntos
de plantas presentes en las selvas que son aprovechables
por los primates. La ausencia de datos básicos acerca de las
preferencias alimentarias de A. palliata en Tabasco y como
varían estas en el tiempo dificulta el llevar a cabo proyectos
de conservación y manejo de las poblaciones remanentes en
el estado.
Con el objeto de contribuir a este vacío de información, en
este trabajo reportamos los resultados de un estudio parcial
sobre el uso de plantas como alimento por una tropa de
monos aulladores (Alouatta palliata ) en el Parque Yumká
localizado en la parte central de Tabasco. Un trabajo anterior
reporta datos sobre el tamaño y aspectos demográficos de la
población de monos aulladores en este sitio (Estrada et al.,
2001).
Métodos
Sitio de estudio
El Parque Yumká se localiza a 17°45’’ y 18°00’’N, 92°45’’ y
93°00’’W y a 15 km de la ciudad de Villahermosa, la capital
del estado. Yumká es un parque público que comprende una
superficie de 101 ha, de las cuales, 33 ha presentan selva alta
perennifolia, 47 ha son sabanas y el resto lo conforma un
lago (Fig. 1). La altura sobre el nivel del mar es de 15 m. El
clima es cálido-húmedo con una precipitación media anual
de 2159 mm y una temperatura media anual de 29.4°C.
Fig. 1. Localización del Parque Yumká en la parte central del estado
de Tabasco (punto negro en el mapa del sur de México). Las líneas
paralelas y solida son una carretera pavimentada y otra de terracería.
Las líneas delgadas son veredas en el área de selva del Parque. El área
sombreada en la parte infeior de la figura es parte de un lago.
Observaciones de los monos aulladores
Las observaciones del comportamiento de alimentación de
los aulladores se llevaron a cabo durante siete días de cada
mes entre Noviembre 2000 y Abril 2001. El método de
muestreo empleado en las observaciones fue el de animal
focal (Altmann, 1974). El tiempo de duración de la muestra
focal para cada sujeto fue de una hora, registrando el tiempo
dedicado al consumo de hojas (jóvenes y maduras), de
frutos (jóvenes y maduros), de flores, de pecíolos, de epifitas,
de hemiparásitas y de bejucos. Los árboles utilizados por
los aulladores fueron marcados, medidos (altura máxima y
diámetro a la altura del pecho) y identificados a nivel de
especie. Debido a que los datos para los meses de Diciembre
y Enero fueron escasos, ambos meses se combinaron como
un solo periodo.
La diversidad dietética mensual se expresó con el índice de
diversidad de Shannon (H´) y el índice de Sorencen fue
calculado para expresar la similitud intermensual en el uso
de especies en la dieta de los aulladores. La dispersión en el
espacio de los árboles que fueron fuentes de alimento para los
aulladores se determino por medio de la ubicación de estos
en un mapa a escala. En este mapa, el área de selva se dividió
en sectores de 1.0 ha en tamaño cada uno, resultando en
un total de 33 sectores más 14 sectores adicionales, ya que
en algunos casos los aulladores salieron del área de selva y
utilizaron arboles fuera de la propiedad del Parque. El patrón
de dispersión espacial de los árboles usados por los aulladores
como fuente de alimento se determinó por medio del calculo
del índice de dispersión de Morisita (Franco, et al.1995). Este
permitió discernir si la distribución espacial de los árboles
utilizados por la tropa era al azar, uniforme o agregada.
Sujetos de estudio
Nuestro estudio se basó en observaciones del comportamiento
alimentario de una de las cuatro tropas de monos aulladores
que existen en el Parque (Estrada et al 2001). Esta tropa
estaba formada por 28 individuos: cinco macho adultos,
once hembras adultas, cinco juveniles, cuatro infantes y tres
individuos cuyo sexo no pudo ser determinado.
Resultados
Esfuerzo de muestreo
Durante el periodo de muestreo (Noviembre 2000 –Abril
2001) se completaron mensualmente un promedio de 7.0
+ 2.1 días de observación de la conducta de los aulladores y
114
Neotropical Primates 9(3), December 2001
acumulamos 727 muestras focales en 302 hrs de registro. El
promedio mensual fue de 43 hrs de observación.
Recursos utilizados
de alimento (rs = 0.76, P < 0.002) y una correlación positiva
se encontró entre el tiempo de alimentación y el número de
árboles usados por especie (rs = 0.78, P < 0.005).
Los aulladores utilizaron 21 especies de plantas (13 familias
botánicas) como fuente de alimento. De estas, 19 especies
estuvieron representadas por 113 árboles, una especie más
estuvo representada por una planta epifita y otra más por un
bejuco (Tabla 1). Los árboles utilizados por los aulladores
presentaron una altura promedio de 18 m (rango = 5 - 24
m) y un d.a.p. promedio de 0.50 + 0.40 m (rango 0.1 - 1.8
m) y se encontró una correlación positiva entre el d.a.p. y la
altura de los árboles utilizados por los aulladores (rs = 0.82, p
<0.001).
Tres familias botánicas contribuyeron al 75% del tiempo
de alimentación registrado. La familia Moraceae con dos
especies de plantas contribuyó al 32% del tiempo alimenticio.
Mientras que la Fabaceae con seis especies de plantas aportó
un 24% del tiempo de alimentación (Tabla 1). El 19%
de tiempo alimenticio fue aportado por dos especies de
la familia Caesalpiniaceae. Una sola especies de la Araceae
contribuyó al 8% del tiempo de alimentación. El restante
25% lo aportaron especies en las otras 11 familias botánicas
(Tabla 1).
Tres especies de árboles, (Brosimun alicastrum, Cynometra
retusa y B. terrabanum) contribuyeron al 51% del tiempo de
alimentación y al 49 % de los árboles utilizados como fuente
de alimento (Tabla 1). Tres especies arbóreas adicionales
(Gliricidia sepium, Sabal mauritiformis y Lysiloma bahamensis)
contribuyeron a un 25% más del tiempo de alimentación y
contribuyeron al 29% de los árboles utilizados. El resto de
las especies registradas contribuyeron al 24% restante del
tiempo de alimentación y al 22% de los árboles usados
(Tabla 1). El tiempo de alimentación se encontró asociado
positivamente con el número de especies usadas como fuente
Selectividad de las partes de las plantas utilizadas como
alimento
El 72% del tiempo de alimentación registrado fue utilizado
por los aulladores en el consumo de hojas. De este, el 38%
y 34% fue invertido en el consumo de hojas jóvenes y hojas
maduras respectivamente y los frutos maduros aportaron el
10% y los jóvenes el 4%. El consumo de flores contribuyó
al 13% del tiempo de alimentación. La mayor diversidad
de especies se encontró en el consumo de hojas maduras
(17 especies) y de hojas jóvenes (12 especies), mientras que
T abla 1 . Especies de plantas utilizadas por los monos aulladores del Parque Yumká, T abasco, México, como fuente de alimento (Nov
2000 – Abril 2001). Se muestra el porciento de tiempo de alimentación que los aulladores pasaron alimentándose de cada parte de la
planta. Las especies están listadas de acuerdo al número de individuos utilizados por los aulladores. Las letras entre paréntesis indican la
familia botánica: M Moraceae, C Caesalpiniaceae, F Fabaceae, A Araceae, R Rutaceae, B Boraginaceae, S Sapindaceae, M Meliaceae,
Si Simarubaceae, Bo Bombacaceae, Bu Burseraceae, U Ulmaceae y Fl Flacourtiaceae. Be bejuco, E epífita.
Hojas
jóvenes
Hojas
maduras
Frutos
jóvenes
Brosimum alicastrum (M)
23
20.9
53.0
Brosimum terrabanum (M)
15
9.3
46.0
Cynometra retusa (C)
31
14.6
Gliricidia sepium (F)
1
5.9
Especie
Frutos
maduros
Flores
Número de
individuos
5
20
18
15.0
18
59
Sabal mauritiformis (A)
85.0
Lysiloma bahamensis (F)
1
Zanthoxylum microcarpum (R)
6
0.4
Cordia stellifera (B)
1
2.9
Piscidia communis (F)
5
3.9
17
9
27
7
5
3
7
3
Enterolobium cyclocarpum (F)
4.7
2
Gliricidia sp. (F)
5.3
2
14.7
2
Paullinia pinnata (S) Be
8
Ampelocera hottlei (U)
1.1
Bursera simaruba (Bu)
1.5
Casearia bartlettii ((Fl)
0.2
Ceiba pentandra (Bo)
1.0
Dialium guianense (C)
2
Guarea chichon (M)
4
Picramnia antidesma (Si)
3
1.0
1
1
1
2
1
1
11.0
1
1
Platymiscium yucatanensis (F)
2.5
1
Syngonium podophyllum (A) E
0.1
1
115
Neotropical Primates 9(3), December 2001
Dos especies de plantas fueron utilizadas por los aulladores
como fuente de frutos jóvenes. De estas, B. alicastrum
contribuyó al 54% del tiempo de alimentación y
B. terrabanum al 46% (Tabla 1). En el caso de frutos maduros
los aulladores usaron dos especies: S. mauritiformis y C. retusa ,
pertenecientes a las familias Araceae y Caesalpiniaceae. Estas
especies aportaron el 85% y 14% del tiempo de alimentación,
respectivamente (Tabla 1). Cinco especies de árboles fueron
usadas como fuentes de flores, G. sepium, L. bahamensis,
Piscidia communis, B. alicastrum y Ceiba pentandra. De estas,
G. sepium fue la más importante, aportando el 60% del
tiempo total registrado en el consumo de flores (Tabla 1). El
aporte de otras cuatro especies fue 27% L. bahamensis, 7%
P. communis, 5% B. alicatrum y 2% C. pentandra .
Variación mensual en la dieta de los aulladores
El 19% de las especies de plantas usadas como fuente
de alimento se registró en Noviembre, primer mes de
observaciones. La aparición de especies nuevas en la dieta
de los aulladores en los meses posteriores, presentó dos
incrementos significativos en Dic/Ene con el 33% de las
especies (n = 7) y otro en Febrero con el 38% (n = 8).
Después de Febrero, los aulladores sólo añadieron una nueva
especie de planta a su dieta en el mes de Marzo y otra en
Abril. El índice promedio mensual de diversidad dietética
fue de H´= 1.59 + 0.53, pero este varió de mes a mes,
presentando sus valores más altos en el mes de Febrero y
los más bajos en el mes de Noviembre (Fig. 2). El índice
promedio de similitud intermensual (índice de Sorensen
IS) a nivel de especie fue de IS = 0.49 + 0.07. Este varió
de 0.42 entre Noviembre y Diciembre-Enero a 0.59 entre
Diciembre-Enero y Febrero (Fig. 2).
El consumo de hojas y frutos fue variable durante los
meses que duró el estudio, presentándose una marcada
estacionalidad en el consumo de flores, frutos y también de
Indice de H´ Shannon
Los aulladores utilizaron 12 especies de plantas como
fuentes de hojas jóvenes, pero dos de ellas, B. alicastrum y
B. terrabanum, contribuyeron al 38% del tiempo registrado
para alimentación en hojas jóvenes, otro 31% fue aportado
por C. retusa (Tabla 1). El tiempo empleado por los aulladores
en el consumo de hojas jóvenes se encontró asociado
positivamente con el número de árboles usados por especie,
(rs = 0.82, P < 0.008). En el caso de las hojas maduras
los aulladores utilizaron 17 especies. De estas B. alicastrum
y B. terrabanum contribuyeron con un 30% del tiempo
de alimentación. Las especies C. retusa y Paullinia pinnata
contribuyeron, cada con una, con un 15% del tiempo de
alimentación y la especie Guarea chichon contribuyó con
un 11% del tiempo alimenticio (Tabla 1). El 29% restante
del tiempo registrado en alimentación de hojas maduras se
distribuyó en nueve especies. El tiempo empleado por los
aulladores en el consumo de hojas maduras se encontró
asociado positivamente con el número de árboles usados por
especie (rs = 0.50, P < 0.02).
3
0,7
2,5
0,6
0,5
2
0,4
1,5
0,3
1
Indice de diversidad de Shannon
0,5
Indice de similitud de Sorensen
0
0,2
0,1
0
Nov
Dic-Ene
Feb
Mar
Indice de Similitud Sorensen
el número de especies utilizadas por los aulladores para
consumo de frutos y flores varió de 2 a 5 especies (Tabla 1).
Abr
Meses
Fig. 2. Diversidad mensual (índice de Shannon H´) y el índice de
similitud intermensual (Índice de Sorensen) en el uso de especies
de plantas usadas por los aulladores como fuente de alimento en el
Parque Yumká (Noviembre 2000–Abril 2001).
hojas jóvenes y maduras (Fig. 3). El consumo de flores fue
importante en los meses de Noviembre a Febrero, mientras
que el consumo de frutos maduros se presentó en todos los
meses del periodo de estudio. El consumo de hojas jóvenes
se concentró entre los meses de Febrero y Abril y este fue
precedido por una concentración en el consumo de hojas
maduras (Fig. 3).
Dispersión espacial de los recursos
Los aulladores usaron 19 de los 47 sectores de 1.0 ha
en tamaño cada uno en que fue dividido el área selvática
del Parque Yumká ó un 40% del espacio disponible. En
estos sectores se encontraron dispersos los árboles que los
aulladores usaron como fuente de alimento. Las especies
B. terrabanum, B. alicastrum, C. retusa y S. mauritiformis
contribuyeron al 64% de los árboles usados. Especies como
L. bahamensis, G. sepium, Dialium guianensis, P. comunis,
Zantoxilum microcarpus, Gliricidia sp., Ampelocera hottlei y
Picramia antidesma aportaron el 28% de los árboles usados.
El 8% restante estuvo representado por especies como
Bursera simaruba, Casearia bartleti, C. pentandra, Cordia
stellifera, Enterolobium microcarpus, G. chichon y Platymicium
yucatenensis.
Fig. 3. Variación mensual en el porcentaje del tiempo de
alimentación dedicado por los aulladores al consumo de diferentes
partes de la planta en el Parque Yumká (Noviembre 2000-Abril
2001). Note la estacionalidad en el consumo de flores, mientras
el consumo de hojas jóvenes estuvo concentrado entre Febrero y
Abril.
116
Los valores del índice de Morisita derivados del calculo del
patrón de dispersión espacial de los árboles usados por los
aulladores como fuente de alimento fueron > 1.0 en cuatro
calculos cubriendo sectores diferentes dentro de su área de
suministro (IdA = 1.35, IdB = 1.59, IdC = 1.02, IdD = 1.13),
lo que indica que los recursos utilizados por los aulladores
presentaron un patrón agregado en el espacio (Muñoz, 2001).
La distancia promedio recorrida por día por los aulladores en
la búsqueda del alimento fue de 125.8 + 95.0 m y la distancia
promedio recorrida por mes fue de 652 + 429 m, pero esta
varió de 229 m en Enero a 1243 m en Febrero.
Discusión
Nuestros resultos indicaron que el uso de árboles en el entorno
en el que existen los aulladores del Parque Yumká estuvo
directamente asociado a la utilización de estos como fuente
de alimento. Estos árboles que tienden a ser relativamente
grandes en tamaño y les sirven también como substrato físico,
representaron a cerca de 21 especies que les sirvieron como
fuente de alimento. Entre estas predominó la utilización de
especies pertenecientes a las familias Moraceae, Fabaceae y
Caesalpiniceae. Especies en estas familias han sido reportadas
como parte importante en la dieta de monos aulladores en
otras localidades en México como en Los Tuxtlas en Veracruz
(Estrada, 1984; Estrada et al., 1999; Juan et al., 1999) y
en Centro y Sud América, como en Belice (Silver et al.,
1998), Finca la Pacifica, Costa Rica (Glander, 1975), Isla de
Barro Colorado, Panamá (Milton, 1980) y Finca Meremberg,
Colombia ( Gaulin y Gaulin, 1982).
Como un dato sobresaliente fue la importancia de la palma
Sabal mauritiformis (Araceae) que sirvió de suministro de
frutos maduros a los aulladores durante cuatro de los cinco
meses de duración del estudio. Esta palma es la segunda
especie arbórea mas importante en el sitio presentándose
en densidades de 26 ind/ha (Jiménez, 1987). Es probable
que debido a la predominancia de esta especie y de aquellas
del genero Brosimum, los aulladores cuentan con una fuente
adecuada y más ó menos constante de alimento en forma
de hojas y de frutos a través del año. La asociación existente
entre el porciento de tiempo de alimentación y el número
de árboles usados por especie sugiere que los aulladores
persistentemente están buscando árboles de estas especies en
su área de suministro.
Se ha sugerido que debido a la consistencia con que son
usadas las especies de la familia Moraceae como fuente de
hojas y frutos por monos aulladores, existe una tendencia en
él genero Alouatta hacia la especialización en el uso de especies
de esta familia (Milton, 1980; Estrada y Coates Estrada,
1995). La predominancia y consistencia en el uso (árboles
y tiempo de alimentación) de las especies B. alicastrum y
B. terrabanum de la Moraceae por el grupo de aulladores en
el Parque Yumká es consistente con esta observación. El uso
predominante de las Moráceas también ha sido asociado a la
alta densidad que caracteriza a las especies de esta familia en
hábitats con elementos de vegetación primaria y secundaria
(Julliot y Sabatier, 1993). Por ejemplo, en el Parque Yumká
Neotropical Primates 9(3), December 2001
la densidad estimada de B. alicastrum es de 15 ind/ha, lo que
acoplado al aporte de su área basal, la coloca entre las cuatro
especies arbóreas más dominantes en este sitio (Jiménez,
1987).
El género Alouatta ha sido clasificado como folívoro-frugívoro
(Crockett y Einsenberg 1987), dependiendo del hábitat que
ocupen. En el Parque Yumká, durante el periodo de estudio
los aulladores fueron más folívoros que frugívoros ya que
pasaron el 76% del tiempo de alimentación consumiendo
hojas. Las altas tasas de consumo de hojas observadas en
el Yumká son consistentes con aquellas reportadas para él
genero Alouatta en otras localidades (Glander, 1975; Milton,
1980; Gaulin y Gaulin, 1982; Estrada, 1984, 1988; Julio
y Sabatier, 1993; Galetti et al., 1994; Bicca-Marques et al.,
1994; Silver et al., 1998, Juan et al., 1999).
Se ha reportado que en la dieta de los monos aulladores
predomina el consumo de hojas jóvenes (Braza et al.,
1983; Estrada, 1984; Glander, 1975; Julliot y Sabatier,
1993; Milton, 1980; Silver et al., 1998; Juan et al., 1999),
preferencia atribuida a una alta concentración de proteína
(33% más que las hojas maduras), altos contenidos de
nutrientes digeribles y menor contenido (36% menos que las
hojas maduras) de fibra que en las hojas maduras (Estrada,
1984; Glander, 1975; Milton, 1978, 1980). Las hojas
maduras, en contraste, contienen niveles altos de compuestos
secundarios (taninos, alcaloides, fenoles, etc.) y de fibra
(celulosa, hemicelulosa y lignina) (Glander, 1982; Hladik,
1978; Milton, 1978, 1979).
En general, estas observaciones son consistentes con los datos
obtenidos en el Parque Yumká, en donde los aulladores
mostraron una marcada preferencia por las hojas jóvenes
cuando estas estuvieron disponibles (Marzo-Abril). En los
otros meses, predominó el uso de hojas maduras, lo que
indica una cierta estacionalidad en la disponibilidad de hojas
jóvenes. Debido a la estacionalidad en la disponibilidad de
hoja jóvenes, los aulladores consumieron hojas maduras en
una mayor proporción en esos meses en que las hojas jóvenes
fueron escasas, pero el número de especies utilizadas fue
mayor, invirtiendo más tiempo y recorriendo más distancias
en su búsqueda (Muñoz, 2001). Los comportamientos arriba
indicados se dieron a pesar de la mayor predecibilidad de
las hojas maduras en la selva, lo que sugiere la necesidad
que tienen los aulladores de balancear su dieta y minimizar
la ingestión de fibra y compuestos tóxicos (Glander, 1975;
Milton, 1977, 1979, 1980; Gaulin y Gaulin, 1982; Braza et
al., 1983: Estrada, 1984, Estrada et al., 1999).
A pesar de la estacionalidad en la producción de frutos en
el sitio, el comportamiento asincrónico y el largo periodo de
frutación en la población de Sabal mauritiformis, permitió
que los aulladores consumieran frutos en todos los meses
que duró el periodo de estudio. Especies como B alicastrum,
B. terrabanum, Cynometra retusa y Ampelocera hotleii
presentaron frutos durante dos de los cinco meses, pero la
dependencia de los aulladores de los frutos de S. mauritiformis
es enfatizada por el dato de que el 63% del tiempo registrado
117
Neotropical Primates 9(3), December 2001
en el consumo de frutos por los aulladores, se registró en
esta especie. Es probable que la fuerte dominancia de esta
especie en la comunidad vegetal selvática del Yumká ha sido
un aspecto favorable para el sostenimiento de la población
de aulladores en este sitio. Otras especies importante en la
dieta de los aulladores fueron aquellas que les sirvieron como
fuente de flores, reforzando así la ingestión de proteína. Estas
especies, G. sepium, L. bahamensis, P. comunis, B. alicastrum
y C. pentandra, fueron utilizadas brevemente (1–2 meses)
enfatizando la marcada estacionalidad en la disponibilidad
de las flores consumidas por los aulladores.
Las variaciones mensuales observadas en la diversidad dietética
(indicado por H´) de los aulladores, atestigua a las variaciones
estaciónales en la disponibilidad de hojas, frutos y flores
discutidas arriba, pero resalta el hecho de que el mes en que
fue mayor el consumo de hojas maduras tiene el índice de
diversidad más alto (H´ 2.45 versus el promedio mensual
H´ 1.59). Esto sugiere que cuando escasea el alimento de
mayor calidad (hojas jóvenes, frutos maduros y flores) los
aulladores están forzados a alimentarse de hojas maduras,
incrementando el número de especies y individuos de los
cuales cosechan estas partes de las plantas. Esto último debido,
posiblemente, al mayor contenido de fibra y compuestos
secundarios en estas partes de las plantas (Estrada, 1984). Así,
los monos aulladores logran adaptarse a las limitaciones de su
flexibilidad digestiva por medio de respuestas conductuales en
el tiempo y espacio que les permiten enfrentarse a variaciones
en el comportamiento fenológico y propiedades químicas
del alimento, logrando optimizar la ingestión de nutrientes
y minimizando la ingestión de fibra y compuestos tóxicos
(Milton, 1980; Estrada, 1984).
Se ha descrito que las distancias que recorren los aulladores
a través de su área de suministro puede ser un buen
indicador de la dispersión espacial y temporal de los recursos
alimenticios (Estrada, 1984, Estrada, 1999). Los árboles de
las especies usadas por los aulladores del Parque Yumká como
fuente de alimento presentaron un patrón de dispersión
espacial agregado, indicando una alta dispersión en el espacio
de los recursos preferidos. Los aulladores respondieron a estos
aspectos de sus recursos viajando distancias variables cada
día, que fueron de 190 m a 380 m. Estos recorridos los
llevaron a distintas secciones dentro de su área de suministro.
Durante el periodo de estudio la tropa estudiada utilizó un
40% de la superficie selvática disponible o 19 ha, pero este
uso varió mensualmente de 6 a 18 ha. Es claro que los monos
aulladores no utilizaron de modo uniforme el área selvática
disponible, algo que estuvo fuertemente condicionado por
el patrón agregado de las fuentes de alimento, especialmente
de aquellas especies arbóreas que tuvieron una marcada
presencia en su dieta, como fue el caso de S. mauritiformis,
C. retusa, B. alicastrum y B. terrabanum.
Aun cuando la presencia de otras tropas puede influir también
en las variaciones observadas en el uso del espacio, nuestros
datos sugieren que es muy probable que los comportamientos
observados fueron respuestas a aspectos de los recursos
alimenticios como su dispersión en el espacio y tiempo y su
densidad y dominancia relativa. Estas respuestas están dadas
por la necesidad de los aulladores de balancear y diversificar
su dieta con la meta de optimizar su estrategia de forrajeo.
La importancia del estudio de la pequeña población de
monos aulladores en el Parque Yumká radica en la necesidad
de documentar, por un lado, aspectos de la ecología y historia
natural para las especies primates del estado de Tabasco. Por
otro lado, estos estudios son importantes para comprender
la flexibilidad adaptativa de miembros del género Alouatta
a la fragmentación, aislamiento y reducción en área de sus
hábitats. Los monos aulladores del Parque Yumká han tenido
éxito en esta dirección y una buena prueba de ellos es la
persistencia y crecimiento de la población en una pequeña
área de selva por ya cerca de cinco décadas (Estrada et al.,
2001). Por consiguiente, el estudio del comportamiento de
los aulladores y la caracterización de los rasgos del entorno
ecológico en el que existen nos permitirá comprender la
manera en que se adaptan a la disponibilidad de los recursos,
al espacio disponible y al crecimiento demográfico. Esta
información nos puede dar las herramientas metodológicas,
teóricas y empíricas para crear modelos de manejo que
promuevan la conservación de poblaciones aisladas de estos
primates en otras localid del estado de Tabasco y en el
Neotrópico.
Agradecimientos
Se agradece el apoyo del Lincoln Zoo Scott Neotropic Fund
y de la Universidad Nacional Autónoma de México. Se
agradece también la autorización de los Directores del Parque
Yumká para llevar a cabo estos trabajos y el apoyo logístico
aportado por la administración y empleados del Parque.
Yasminda García del Valle, División de Ciencias Biológicas,
Universidad Juárez Autónoma de Tabasco, Villahermosa,
Tabasco, México, e-mail: <monayasmi@primatesmx.com>,
David Muñoz, División de Ciencias Biológicas, Universidad
Juárez Autónoma de Tabasco, Villahermosa, Tabasco, México,
e-mail: <aullador@primatesmx.com>, Miguel MagañaAlejandro, División de Ciencias Biológicas, Universidad
Juárez Autónoma de Tabasco, Villahermosa, Tabasco, México.
Alejandro Estrada, Estación de Biología Los Tuxtlas,
IB-UNAM, Apartado 176, San Andrés Tuxtla, Veracruz,
México, e-mail: <aestrada@primatesmx.com>, y Berenice
Franco, División de Ciencias Biológicas, Universidad Juárez
Autónoma de Tabasco, Villahermosa, Tabasco, México,
e-mail: <berefranco@primatesmx.com>.
Referencias
Rylands, A., Mittermeier, R. A. y Rodríguez-Luna, E. 1995.
A species list for the New World primates (Platyrrhini):
Distribution by country, endemism, and conservation
status according to the Mace-Lande system. Neotrop.
Primates 3(suppl.): 114–164.
Altmann, J. 1974. Observational study of behavior: Sampling
methods. Behavior 49:227–267.
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Bicca-Marques, J. C. y Calegaro-Marques, C. 1994. Activity
budget and diet of Alouatta caraya : An age-sex analysis.
Folia Primatol. 63: 216 –220.
Braza, F., Álvarez, F. y T. Azcarate. 1983. Feeding habits of
the red howler monkeys (Alouatta seniculus) in the Llanos
of Venezuela. Mammalia 47: 205–214.
Crockett, C. M. y Eisenberg I. F. 1987. Howlers: Variation
in group size and demography. En: Primate Societies, B. B.
Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wranham y T.
T. Struhsaker (eds), pp.54 – 68. T he University of Chicago
Press, Chicago.
Estrada A. 1984. Resource use by howler monkeys (Alouatta
palliata ) in the rain forest of Los Tuxtlas, Veracruz, México.
Int. J. Primatol. 5: 105–131.
Estrada, A. y Coates-Estrada R. 1995. La contracción y
fragmentación de las selvas y las poblaciones de primates
silvestres: El caso de Los Tuxtlas, Veracruz. En: Estudios
Primatologicos en México. Vol. II, E. Rodríguez-Luna, L.
Cortes Ortiz y J. Martínez Contreras (eds.), pp.25–29.
Biblioteca Universidad Veracruzana, Xalapa, Veracruz,
México.
Estrada, A., Juan Solano, S., Ortiz Martines, T. y CoatesEstrada, R. 1999. Feeding and general activity patterns
of a howler monkey (Alouatta palliata ) troop living in a
forest fragment at Los Tuxtlas, Mexico. Am. J. Primatol. 48:
167–183.
Estrada, A., García, Y., Muñoz, D., y Franco, B. 2001. Survey
of the population of howler monkeys (Alouatta palliata ) at
Yumká Park in Tabasco, México. Neotrop. Primates 9(1):
12–15.
Franco, L. J., De la Cruz, A. G., Cruz, G. A., Rocha, R. A.,
Navarrete, S. N., Flores, M. G., Kato, M. G., Sánchez, C.
S., Abarca, A. L. G. y Bedia, S. C. M. 1989. Manual de
Ecología . Editorial Trillas, Mexico.
Galetti, M., Pedroni, F. y Morellato L. P. C. 1994. Diet of the
brown howler monkey Alouatta fusca in a forest fragment
in southeastern Brazil. Mammalia . 58: 111–118
Gaulin, S. J. C. y Gaulin C. K. 1982. Behavioral ecology of
Alouatta seniculus in Andean cloud forest. Int. J. Primatol.
3: 1–32.
Glander, K. E. 1975. Habitat description and resource
utilization: An ecological view of social organization in
mantled howler monkeys. En: Socioecology and Psychology
of Primates, R. H. Tuttle (ed.), pp.37–57. T he Hague,
Mouton.
Glander, K. E. 1982. T he impact of plant secondary
compounds on primate feeding behavior. Yearb. Phys.
Anthropol. 25: 1–18.
Hladik, C. M. 1978. Adaptive strategies of primates in
relation to leaf-eating. En: The Ecology of Arboreal Folivores,
G. G. Montgomery (ed.), pp.373–395. Smithsonian
Institution Press, Washington, DC.
Horwich, R. H. y Johnson, R. D. 1986. Geographical
distribution of black howler (Alouatta pigra ) in Central
America. Primates 27: 53–62.
Jiménez, P. J. 1987. Estudio preliminar de la estructura
arbórea de dos relictos de Selva Mediana en Tabasco.
Tesis profesional. Colegio superior de agricultura Tropical.
H. Cárdenas, Tabasco, México.
Neotropical Primates 9(3), December 2001
Juan, S., Ortiz-Martínez, T. J., Estrada, A. y Coates-Estrada,
R. 1999. Uso de plantas como alimento por Alouatta
palliata en un fragmento de selva en los Tuxtlas, México.
Neotrop. Primates. 7: 8–11.
Julliot, C. y Sabatier, D. 1993. Diet of the red howler
monkeys (Alouatta seniculus) in French Guiana. Int. J.
Primatol. 14: 527–549.
Masera, O. R. 1996. Deforestación y degradación forestal en
México. Documento de Trabajo. Grupo interdisciplinario de
Trabajo de Tecnología Rural Apropiada 19: 1–15.
Milton, K. 1977. T he foraging strategy of the howler monkey
in the tropical forest of Barro Colorado Island, Panama,
Ph. D dissertation, New York University.
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the mantled howler monkey (Alouatta palliata ). En: The
Ecology of the Arboreal Folivores, G. G. Montgomery (ed.),
pp.535–549. Smithsonian Institution Press, Washington,
DC.
Milton, K. 1979. Factors influencing leaf choice by howler
monkeys: A test of some hypotheses of food selection by
generalist herbivores. Amer. Nat. 114: 362–378.
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A Study in Primate Economics. Columbia University Press,
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Muñoz, D. 2001. Estudio preliminar del patrón general
de actividades de monos aulladores (Alouatta palliata ) en
semilibertad en el parque Yumká, Tabasco, México. Tesis
Licenciatura. Universidad Juárez Autónoma de Tabasco,
Villahermosa Tabasco, México.
SEMARNAP Webpage. 1999. <www.semarnap.gob.mx>.
Silver, S. C., Ostro, L. E. T., Yeager, C. P. y Hoorwich,
R. 1998. Feeding Ecology of the black howler monkey
(Alouatta pigra ) in northern Belize. Am. J. Primatol.
45: 263–279.
Smith, J. D. 1970. T he systematic status of the black
howler monkeys, Alouatta pigra Lawrence. J. Mammal.
51: 358–369.
ALOUATTA GUARIBA CLAMITANS CABRERA, 1940:
A NEW SOUTHERN L IMIT FOR THE SPECIES AND FOR
NEOTROPICAL PRIMATES
Rodrigo C. Printes
Marcus V. A. Liesenfeld
Leandro Jerusalinsky
Introduction
T he state of Rio Grande do Sul in Brazil has a rich
biodiversity due to its geographic location and landscape.
T hirty-five percent of the Brazilian mammals, 141 species
in 34 families, have been recorded for the state (Silva, 1994).
Most of them occur in the Atlantic forest which extends
from Rio Grande do Norte in the northeast of Brazil. In Rio
Grande do Sul, this forest extends from the municipality of
Torres to the Rio Maquiné in the northeast of the state, and
marks the southern limit for most tropical plants (Reitz et al.,
1988). Few tropical forest plant species reach the region of
119
Neotropical Primates 9(3), December 2001
Porto Alegre or the Rio Jacuí. Forest fragments are found on
the quaternary wet plains, and on the foothills of mountains
(up to 900 m, in the region called Serra Geral).
Once an area was sufficiently explored and there were no
new indications of the occurrence of howler monkeys, the
expedition moved north.
T he genus Alouatta Lacèpéde, 1799 is the most widely
distributed of Neotropical primates (Neville et al., 1988).
T heir northern limit is in the Yucatán Peninsula, Mexico
(20°N) (Smith, 1970) and their southern limit, as defined
until now, was the Rio Jacuí (30°S), Rio Grande do Sul,
Brazil (Hirsch et al., 1991). It was Cabrera (1940) who
suspected that the southern brown howler, Alouatta guariba
clamitans, may occur south of the Rio Jacuí, but no concrete
evidence was available. Here we report on five expeditions to
the region in order to define more exactly the southernmost
limits to its range.
In the localities where the occurrence of A. guariba clamitans
was verified, we carried out a quick survey of the vegetation
using a 50 m transect with one sample point every 2 m.
Trees closest to the transect, in any direction, with a 7 cm
or greater circumference at breast height were identified.
Tree heights and their distance from the transect were also
recorded (Filgueiras et al., 1994).
Methods
Five expeditions were carried out between December 1998
and September 2000. Our fieldwork began in the forests
along the Rios Camaquã and Piratini; along the middle
and southern portions of the south-eastern mountain ranges,
respectively, 30–31°S, where the forests and original natural
vegetation are relatively well conserved. Further south the
forests give way to the grassland and bushy savannas of the
Rio Grande do Sul Shield (Rambo, 1956; Fernandes, 1998).
Geographic co-ordinates were taken using a GPS (Garmin®
models 1 and 2).
Police stations and local people (mainly hunters and
fishermen) were contacted in the different localities to obtain
information on the possible occurrence of howlers. To avoid
false positive identifications of howlers, we asked questions
about the mammal fauna in general. Photographs were also
used to confirm howler monkey identification.
Positive information was selected for field verification
according to the location of the area indicated (latitude, if
near to forest, rivers or mountains), when the animals were
seen, the number of animals reported for each area, and a
general feeling for the veracity of the information from the
behaviour patterns of the primates described by the observer.
Results
T he 11 localities surveyed are shown in Table 1 and Figure
1. T here was no evidence of A. guariba clamitans in the Rio
Piratini basin, but they were found at two sites along the Rio
Camaquã, south of the Rio Jacuí.
1) Cristal, municipality of Cristal, Rio Camaquã (31°00’S,
52°04’W), locality 1 (Fig. 1 and Table 1). All reports on the
occurrence of A. guariba clamitans in upstream sites given
by the local population were confirmed. T he forests become
progressively more fragmented inland, due to agriculture
(beans and corn). Along the Rio Camaquã, however, there
were good stretches of relatively continuous forest. We visited
a farm (5 km from the town of Cristal), where farmers
had reported the presence of at least three howler groups.
T his was confirmed by new and old faeces collected on
31 December 1998, and we eventually saw the monkeys
on 5 March 1999.
T he forest was between 16 and 18 m tall. “Angicovermelho” (Parapiptadenia rigida - Mimosaceae) was the
predominant tree. Other common species found under the
canopy were: “camboatá” (Cupania vernalis and Matayba
elaegnoides - Sapindaceae), “açoita-cavalo” (Luehea divaricata
- Tiliaceae), and “batinga” (Eugenia rostrifolia - Myrtaceae).
Eugenia hiemalis and Eugenia uniflora were common in the
understorey. Considering the size of the Parapiptadenia
rigida and Luehea divaricata trees, and judging from
information obtained from local people, the forest is
T able 1 . Localities visited during the “Southern Limit Expedition”, their respective co-ordinates, survey results (occurrence or
otherwise) and time spent in each site. See Figure 1.
Locality
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
Cristal
Cascavel
Canta Galo
T uruçu
T orrinhas
Hulha Negra
Canguçu
7 o Distrito de Pelotas
Candiota
Pedro Osório
F. Capão Redondo
* non consecutive days
River Basin
Camaquã
Camaquã
Camaquã
T uruçu
Jaguarão
Jaguarão
Pelotas
Pelotas
Jaguarão
Piratini
Piratini
Coordinates
º
31 00’S;
31 º 05’S;
31 º 10’S;
31 º 21’S;
31 º 22’S;
31 º 24’S;
31 º 24’S;
31 º 26’S;
31 º 38’S;
31 º 52’S;
31 º 57’S;
º
52 04’W
52 º 17’W
52 º 19’W
52 º 28’W
53 º 33’W
53 º 21’W
52 º 40’W
52 º 27’W
53 º 44’W
52 º 46’W
52 º 33’W
Occurrence
T ime (days)
Yes
No
Yes
No
No
No
No
No
No
No
No
4*
1
6*
1
1
1
4*
1
1
1
2
120
Neotropical Primates 9(3), December 2001
Figure 1. Localities visited during the “Southern Limit Expedition” (the old limit for A. guariba clamitans is shaded dark; the new limit is
lighter): (1) Cristal, 31°00’S; 52°04’W; (2) Cascavel, 31°05’S; 52°17’W; (3) Canta Galo, 31°10’S; 52°19’W; (4) Turuçu, 31°21’S; 52°28’W;
(5) Torrinhas, 31°22’S; 53°33’W; (6) Hulha Negra, 31°24’S; 53°21’W; (7) Canguçu, 31°24’S; 52°40’W; (8) 7 o Distrito de Pelotas, 31°26’S;
52°27’W; (9) Candiota, 31°38’S; 53°44’W; (10) Pedro Osório, 31°52’S; 52°46’W; (11) Faz. Capão Redondo, 31°57’S; 52°33’W.
relatively undisturbed and well conserved. T he entire area
is occasionally inundated, and forests along the banks of
the Rio Camaquã are seasonally covered by water. Other
mammals recorded for this site were: paca (Agouti paca ),
raccoon (Procyon cancrivorus), deer (Mazama sp.), ninebanded armadillo (Dasypus novemcinctus), and jaguarundi
(Herpailurus jagouaroundi).
2) Canta Galo, municipality of São Lourenço, Rio Camaquã
basin (31°10’S, 52°19’W), Locality 3 (Fig. 1 and Table
1). Local people reported the occurrence of A. guariba
clamitans on the opposite bank of the Rio Camaquã to
Cristal. According to the reports, the howlers could be seen
there only during the summer, when the grapes are ripening,
which the howlers feed on. Old howler excrement was found
in a forest patch on a farm 8 km away from Canta Galo, on
2 February 2000.
T he forest was humid, 40 ha in size, and surrounded by
corn crops. “Batinga” (Eugenia rostrifolia ) was the most
common tree in the canopy, and its fruits, probably eaten
by the howlers, also mature during the summer (usually
in February). Some of the trees reach 16 m in height. T he
understorey was well shaded, and the most common species
found were Sorocea bonplandii (Moraceae) and Trichilia
claussenii (Meliaceae).
Discussion
Being sub-tropical, the extreme south of Brazil is marked
by distinct seasonal patterns of spring, summer, autumn and
winter, and forests are semi-deciduous. T his seasonality, and
even the occasional occurrence of snow, probably limits the
occurrence of primates to only the larger monkeys, Cebus
and Alouatta . T he Rio Camaquã basin marks the transition
between the Atlantic Forest and the Pampas (Rambo, 1956)
with a gradual loss of forest and a reduced tree diversity,
which makes even folivory a difficult diet to maintain.
T he Rio Jacuí was considered to be the southern limit for
Alouatta guariba clamitans until 1991 (Hirsch et al., 1991).
However, the results presented here show that this species
occurs on both margins of the Rios Jacuí and Camaquã (200
km south of the Rio Jacuí). It is probable that the howlers
of the Rio Camaquã have to move long distances during
times of flooding, and to exploit perhaps relatively few key
resources, such as cultivated grapes and the fruits of Eugenia
rostrifolia .
121
Neotropical Primates 9(3), December 2001
Villalba et al. (1995) indicated the possible natural occurrence
of Alouatta caraya in northern Uruguay (31°00’S, 56°00’W)
which, although not yet confirmed, is just a little north of the
localities we have identified on the Rio Camaquã. T he most
southerly record for this species is the town of Canta Galo
(31°10’S, 52°19’W), in the municipality of São Lourenço do
Sul, Rio Grande do Sul, Brazil. T his locality is also the new
southern limit for all Neotropical primates.
We conclude that the key factors determining the
distributional limits of primates in the south of South
America are: 1) T he seasonal inundation of rivers in the
Camaquã basin; 2) the reduction in tree species diversity;
3) the gradual predominance of deciduous trees; and 4) the
low temperatures during winter.
Rambo, B. 1956. A Fisionomia do Rio Grande do Sul. 3rd
edition. Ed. UNISINOS, São Leopoldo. 472pp.
Reitz, R., Klein, R. M. and Reis, A. 1988. Projeto Madeira
do Rio Grande do Sul. Companhia Rio-grandense de Artes
Gráficas, Porto Alegre. 525pp.
Smith, J. D. 1970. T he systematic status of the black
howler monkey, Alouatta pigra Lawrence. J. Mammal. 51:
358–369.
Silva, F. 1994. Mamíferos Silvestres do Rio Grande do Sul.
2nd edition. Fundação Zoobotânica do Rio Grande do Sul,
Porto Alegre.
Villalba, J. S., Prigioni, C. M. and Sappa, A. C. 1995. Sobre
la posible presencia de Alouatta caraya en Uruguay. Neotrop.
Primates 3(4): 173 –174.
Acknowledgments
T he authors would like to thank the Military Police of the
state of Rio Grande do Sul; our fellow researchers André
Hirsch, Anthony B. Rylands, Andrea Lamberts, Denise A.
Rosário, David Buss, Gerson Buss, Helena Romanowski,
Laís F. Moraes, Liane B. Printes, Luiz Felipe Kunz Jr., Paulo
Oliveira, Shaula M. V. Sampaio, T hales Freitas, and Yanina
M. S. Dalessandro; as well as the photographer Adriano
Becker. T hanks also to all the local people who collaborated
with the interviews, especially to Ademar Brodt, Antônio
Gomes, Anita B. Madrid, Guilherme Brodt, Jair S. da Costa,
João C. de Souza, Lucas Brodt, Otto Leichtnow, Zelomar
Krolow and Zeno Koltz.
Rodrigo C. Printes, Marcus V. A. Liesenfeld, and Leandro
Jerusalinsky, Programa Macacos Urbanos, Departamento
de Zoologia, Universidade Federal do Rio Grande do Sul,
Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, Rio
Grande do Sul, Brasil. E-mail of first author: <cambara@
smam.prefpoa.com.br>.
References
Fernandes, A. 1998. Fitogeografia Brasileira . Editora Multigraf.
Fortaleza. 340pp.
Filgueiras, T. S., Brochado, A. L., Nogueira, P. E. and Guala
II, G. T. 1994. Caminhamento: Um método expedito
para levantamentos florísticos qualitativos. Cadernos de
Geociências, 12: 24 – 43.
Hirsch, A., Landau, E. C., Tedeschi, A. C. de M. and
Meneghetti, J. O. 1991. Estudo comparativo das espécies
do gênero Alouatta Lacèpéde, 1799 (Plathyrrhini, Atelidae)
e sua distribuição geográfica na América do Sul. In: A
Primatologia no Brasil - 3 , A. B. Rylands and A. T. Bernardes
(eds.), pp.239–262. Sociedade Brasileira de Primatologia,
Fundação Biodiversitas, Belo Horizonte.
Neville, M. K., Glander, K. E., Braza, F. and Rylands,
A. B. 1988. T he howling monkeys, genus Alouatta . In:
Ecology and Behavior of Neotropical Primates, Vol. 2 , R. A.
Mittermeier, A. B. Rylands, A. F. Coimbra-Filho and G. A.
B. da Fonseca (eds.), pp.349– 453. World Wildlife Fund,
Washington, DC.
TWO TAXONOMIES OF THE NEW WORLD PRIMATES
– A C OMPARISON OF RYLANDS ET AL. (2000) AND
GROVES (2001)
Anthony B. Rylands
Two listings of the New World Primates were published
recently. T he first by Rylands et al. (2000) arose from a
review of the species and subspecies during the workshop
“Primate Taxonomy for the New Millennium”, organized
by the IUCN/SSC Primate Specialist Group (PSG) at the
Disney Institute, Orlando, Florida, in February 2000. T he
second was published by Colin P. Groves of the Australian
National University, Canberra, in his book Primate Taxonomy,
published in April 2001 by the Smithsonian Institution
Press, Washington, DC. Rylands et al. listed 110 species and
205 species and subspecies of New World primates. Groves
also listed 110 species, but only 177 species and subspecies.
In this note, I point out and comment on the (minor)
differences between these listings, the most significant
of which is in the names used for the families and
subfamilies. Rylands et al. opted for five families, using the
traditional names, as follows: Callitrichidae (the marmosets
and tamarins), Cebidae (capuchin monkeys and squirrel
monkeys), Aotidae (night monkeys), Pitheciidae (sakis,
uakaris and titi monkeys) and Atelidae (howling monkeys,
spider monkeys, muriquis, and woolly monkeys). Groves
followed a very similar arrangement, but defined the Cebidae
differently, with three subfamilies: the marmosets and
tamarins, the squirrel monkeys, and the capuchin monkeys
(as proposed by Rosenberger in 1981). However, regarding
the correct names of the family-groups, Groves, with the
International Code of Zoological Nomenclature (2000) in hand,
winkled out some synonyms and has suggested changes in
some of the family and subfamily names (Table 1).
T he first is his argument that the correct family-group
name for the marmosets and tamarins is not Callitrichidae
T homas, 1903, but Hapalidae Gray 1821 (Hapalinae as
a subfamily of the Cebidae). I quote his reasoning here
verbatim (pp.126–127):
122
Neotropical Primates 9(3), December 2001
T able 1. Families and subfamilies of Platyrrhini according to
Groves (2001).
Family/Subfamily
Cebidae Bonaparte, 1831
Hapalinae Gray, 1825
Chrysotrichinae Cabrera, 1900
Cebinae Bonaparte, 1831
Nyctipithecidae Gray, 1870
Pitheciidae Mivart, 1865
Pitheciinae Mivart, 1865
Callicebinae Pocock, 1925
Atelidae Gray, 1825
Atelinae Gray, 1825
Mycetinae Gray, 1825
Genera
Cebuella, Mico, Callithrix,
Callimico, Leontopithecus,
Saguinus
Saimiri
Cebus
Aotus
Pithecia, Cacajao,
Chiropotes
Callicebus
Ateles, Lagothrix, Oreonax,
Brachyteles
Alouatta
“Callitrichinae T homas, 1903, is a synonym. T here are two
reasons why the name Callitrichinae (and its coordinate
Callitrichidae for those wishing to retain family-level status
for the marmosets and tamarins) cannot be used.
First: Priority in the family-group is accorded not to the
type genus but to the family-group name itself. T he earliest
family-group name given to marmosets is Harpalidae [sic] by
Gray (1821), who misread Hapale Illiger, 1811, as Harpale.
T he current (fourth) edition of the International Code of
Zoological Nomenclature (2000) states in Article 40:
(a) After 1960 . When, after 1960, the generic name on
which a valid family-group is based on is rejected as a junior
synonym, that family-group name is to be replaced unless
the conditions of Subsection (i) apply.
(i) If the senior generic synonymy is itself the basis
of a family-group name, or if a reclassification also
involves other family group names, the Principle
of Priority applies to all the family group names
concerned.
(b) Before 1961 . If a family group name has been replaced
before 1961 because of such synonymy, and the replacement
name has one general acceptance, it is to be maintained.
In this case T homas (1903) discovered that the generic name
Callithrix Erxleben, 1777, referred to marmosets, not to titis
as had been previously assumed, and took three actions: 1) he
replaced the commonly used name Hapale Illiger, 1811, with
Callithrix, 2) he replaced the family name Hapalidae with
Callithricidae (recte Callitrichidae), and 3) he gave the titis
a new generic name Callicebus. T he first and third of these
actions were justified; the second, admittedly retroactively,
was not. But the Code must be followed. T he provisions
of article 40(b) apply: the family-group name was replaced
before 1961, but the replacement name cannot be said
to have “won general acceptance,” by virtue especially
of the continued use of Hapalidae in W. C. O. Hill’s
influential monograph series Primate: Comparative Anatomy
and Taxonomy.
Second: Because the name Callithrix was long used,
incorrectly, for the titis (as just discussed) family group
names for the marmoset/tamarin group were understandably
based on what was thought to be the correct name. Gray
(1821) misread the name as Callitrix and based the family
name Callitricidae on it. T his might, at a pinch, be taken
as effectively a different name, but the same cannot be said
of Callitrichina Gray, 1825 (during the intervening four
years, he had corrected his misspelling). T his means that
Callitrichinae/-idae T homas 1903, for the marmosets and
tamarins is preoccupied by the same name of Gray, 1825,
for the titis.
T he first point is difficult, but arguable. T he second
point is fundamental, not arguable. T he correct name
for the subfamily containing marmosets is therefore not
Callitrichinae T homas, 1903, as listed by Simpson (1945, as
Callithricidae) or Napier and Napier (1967), or Hershkovitz
(1977).”
Groves also argued that: the subfamily name of the squirrel
monkeys, Saimiriinae Miller, 1924 (used by Hershkovitz,
1977) is a synonym of Chrysotrichinae Cabrera, 1900
(p.156); the family-group name Aotidae/Aotinae Poche, 1908
(used by Hershkovitz, 1977 and Hill, 1960) is a synonym
of Nyctipithecidae Gray, 1870; and that the subfamily name
Alouattinae Elliot, 1904 (used by Hershkovitz, 1977 and
Hill, 1960) is a synonym of Mycetinae Gray, 1825. Groves
attributes the authorship of the family-group name Cebidae
to Bonaparte, 1831. T he name was assigned to Swainson,
1835, by Hill (1960), but Groves argued that Bonaparte
clearly intended the name Cebina to be a family-group
suffix and is therefore the original author. Table 1 shows the
families/subfamily arrangement according to Groves (2001).
Regarding the list of species, those in the Callitrichidae/
Hapalinae, are identical except for the addition of three
marmosets by Rylands et al.: Mico saterei (Silva, Jr. and
Noronha, 1998), and Mico manicorensis and Mico acariensis,
both described (under the genus Callithrix) by Van Roosmalen
et al. (2000), the descriptions of which had not been
published when Groves’ book was in press. Groves gave
subgeneric classifications to the marmosets, subgenus Mico
Lesson, 1840, for the Amazonian marmosets, and Callithrix
Erxleben, 1777, for the “Jacchus” group marmosets of eastern
and south-eastern Brazil. Rylands et al. went the whole hog in
assigning all the Amazonian marmosets to the genus Mico.
T he genus Cebus presents some discrepancies in the
continued listing of numerous, often poorly defined,
subspecies by Rylands et al. In his research, however, Groves
whittled them down considerably. C. capucinus limitaneus
Hollister, 1914, C. capucinus imitator Thomas, 1903, and
C. capucinus curtus Bangs, 1905, listed by Rylands et al.,
are considered synonyms by Groves. T hey were listed by
Hershkovitz (1949) who, as pointed out by Groves, even
then doubted their validity, and Hernández-Camacho
and Cooper (1976) also found that the pelage characters
123
Neotropical Primates 9(3), December 2001
used to distinguish them were too variable to allow for the
recognition of distinct subspecific forms.
Rylands et al. continued to follow Hershkovitz (1949) in
listing 11 poorly defined subspecies of Cebus albifrons, while
Groves reduced the number to six: C. albifrons albifrons
(Humboldt, 1812); C. albifrons unicolor Spix, 1823; C.
albifrons cuscinus T homas, 1901, C. albifrons trinitatis Von
Pusch, 1941, C. albifrons aequatorialis Allen, 1914, and C.
albifrons versicolor Pucheran, 1845 (see Table 2). Rylands et
al. did not list C. albifrons unicolor on the advice of T homas
Defler, whose investigations had led him to argue cogently
that it is a synonym of C. albifrons albifrons (see Defler and
Hernández-Camacho, in press). Rylands et al. also maintained
T able 2. A summary of the taxonomic differences between the listings of the Platyrrhini by Rylands et al. (2000) and Groves (2001).
Rylands et al. (2000)
Groves (2001)
Mico saterei (Silva, Jr. & Noronha, 1998)
Mentioned (p.131), but description not published when Groves (2001)
was in press.
Mico manicorensis (Van Roosmalen, Van Roosmalen,
Mittermeier & Rylands, 2000)
Mico acariensis (Van Roosmalen, Van Roosmalen,
Mittermeier & Rylands, 2000)
Cebus capucinus capucinus (Linnaeus, 1758)
Cebus capucinus limitaneus Hollister, 1914
Cebus capucinus imitator Thomas, 1903
Cebus capucinus curtus Bangs, 1905
Synonym of C. albifrons albifrons (Humboldt, 1812)
(see Defler et al., in press)
Cebus albifrons cesarae Hershkovitz, 1949
Cebus albifrons leucocephalus Gray, 1865
Cebus albifrons yuracus Hershkovitz, 1949
Cebus albifrons adustus Hershkovitz, 1949
Cebus albifrons malitiosus Elliot, 1909
Cebus olivaceus olivaceus Schomburgk, 1848
Cebus olivaceus apiculatus Hershkovitz, 1949
Cebus olivaceus brunneus Allen, 1914
Cebus olivaceus castaneus I. Geoffroy, 1851
Cebus olivaceus kaapori Queiroz, 1992
Saimiri boliviensis pluvialis Lönnberg, 1940
Saimiri boliviensis jaburuensis Lönnberg, 1940
Pithecia monachus napensis Lönnberg, 1938
Callicebus personatus (É. Geoffroy, 1812)
Callicebus nigrifrons (Spix, 1823)
Callicebus melanochir (Wied-Neuwied, 1820)
Callicebus barbarabrownae Hershkovitz, 1990
Alouatta palliata palliata (Gray, 1849)
Alouatta palliata mexicana (Merriam 1902)
Alouatta palliata aequatorialis (Festa, 1903)
Alouatta coibensis coibensis Thomas, 1902
Alouatta coibensis trabeata Lawrence, 1933
Alouatta seniculus ssp. (formerly straminea ; see Rylands
and Brandon-Jones, 1998)
Alouatta seniculus amazonica Lönnberg, 1941
Alouatta seniculus puruensis Lönnberg, 1941
Alouatta seniculus insulanus Elliot, 1910
Alouatta belzebul belzebul (Linnaeus, 1766)
Alouatta belzebul discolor (Spix, 1823)
Alouatta belzebul ululata Elliot, 1912
Ateles hybridus hybridus (I. Geoffroy, 1829)
Ateles hybridus brunneus Gray, 1872
Ateles geoffroyi fusciceps Gray, 1866
Ateles geoffroyi rufiventris Allen, 1914
Ateles geoffroyi panamensis Kellogg & Goldman, 1944
Ateles geoffroyi azuerensis (Bole, 1937)
Ateles geoffroyi frontatus (Gray, 1842)
Description not published when Groves (2001) was in press.
Description not published when Groves (2001) was in press.
Cebus capucinus monotypic
Synonym of Cebus capucinus
Synonym of Cebus capucinus
Synonym of Cebus capucinus
Cebus albifrons unicolor Spix, 1823
Synonym of Cebus albifrons versicolor Pucheran, 1845
Synonym of Cebus albifrons versicolor Pucheran, 1845
Synonym of Cebus albifrons cuscinus T homas, 1901
Synonym of Cebus albifrons versicolor Pucheran, 1845
Synonym of Cebus albifrons versicolor Pucheran, 1845
Cebus olivaceus monotypic
Synonym of Cebus olivaceus
Synonym of Cebus olivaceus
Synonym of Cebus olivaceus
Listed as Cebus kaapori
Synonym of Saimiri boliviensis boliviensis (I. Geoffroy & de Blainville, 1834)
Synonym of Saimiri boliviensis boliviensis (I. Geoffroy & de Blainville, 1834)
Not listed
Callicebus personatus with four subspecies
Subspecies of Callicebus personatus
Subspecies of Callicebus personatus
Subspecies of Callicebus personatus
Alouatta palliata monotypic
Synonym of Alouatta palliata
Synonym of Alouatta palliata
Alouatta coibensis monotypic
Synonym of Alouatta coibensis
Alouatta macconnelli Elliot, 1910
Synonym of Alouatta seniculus juara Elliot 1910
Synonym of Alouatta seniculus juara Elliot 1910
Synonym of Alouatta macconnelli
Alouatta belzebul monotypic
Synonym of Alouatta belzebul
Synonym of Alouatta belzebul
Ateles hybridus monotypic
Synonym of Ateles hybridus
Listed as Ateles fusciceps fusciceps Gray, 1866
Listed as Ateles fusciceps rufiventris Allen, 1914
Synonym of Ateles geoffroyi ornatus Gray, 1870
Synonym of Ateles geoffroyi ornatus Gray, 1870
Synonym of Ateles geoffroyi geoffroyi Kuhl, 1820
124
the subspecies of Cebus olivaceus recognized by Hershkovitz
(1949) under the species name of nigrivittatus Wagner, 1848
(see Rylands, 1999). Groves placed them all as synonyms of
C. olivaceus. Rylands et al. listed the form kaapori Queiroz,
1992, as a subspecies of C. olivaceus, whereas Groves (2001)
maintained it as a distinct species as described by the author.
Rylands et al. adopted Groves’ taxonomy for the tufted
capuchin monkeys of the Cebus apella group.
T he taxonomies of Saimiri are the same except that Rylands
et al. listed the two forms, pluvialis Lönnberg, 1940 and
jaburuensis Lönnberg, 1940, mentioned in a footnote by
Hershkovitz (1987). Groves listed them both as synonyms of
S. boliviensis boliviensis.
Rylands et al. followed Groves on the taxonomy of the
Pitheciidae except in giving all the Atlantic forest titis
the status of species, as recommended by Kobayashi and
Langguth (1999) in their description of Callicebus coimbrai.
Rylands et al. also listed a third subspecies of Pithecia
monachus. Based on his examination of specimens in the
British Museum (Natural History), Peter Grubb argued that
P. monachus napensis Lönnberg, 1938, is a distinct and valid
subspecies (pers. comm., February, 2000).
T he final two genera which present discrepancies are Alouatta
and Ateles. Groves did not recognize the subspecies of Alouatta
palliata , A. coibensis and A. belzebul listed by Rylands et al.
(see Table 2). Whereas Rylands et al., were not prepared
to designate a subspecific name to the Guianan red howler
(see Rylands and Brandon-Jones, 1998), Groves listed it
as Alouatta macconnelli Elliot 1910. Groves synonymized
Alouatta seniculus amazonica Lönnberg, 1941 and Alouatta
seniculus puruensis Lönnberg, 1941, with Alouatta seniculus
juara Elliot 1910, and the Trinidad howling monkey, Alouatta
seniculus insulanus Elliot, 1910 with A. macconnelli.
Rylands et al. followed Collins and Dubach (2000) in placing
the brown-headed spider monkey, and the Colombian black
spider monkey, as subspecies of A. geoffroyi: A. geoffroyi
fusciceps Gray, 1866 and A. geoffroyi rufiventris Allen, 1914,
respectively, whereas Groves maintained them as subspecies of
A. fusciceps. Groves did not recognize Ateles hybridus brunneus
Gray, 1872, and also synonymized Ateles geoffroyi panamensis
Kellogg and Goldman, 1944 and Ateles geoffroyi azuerensis
(Bole, 1937) with Ateles geoffroyi ornatus Gray, 1870. Lastly,
he considered Ateles geoffroyi frontatus (Gray, 1842) to be a
synonym of Ateles geoffroyi geoffroyi Kuhl, 1820.
Anthony B. Rylands, Center for Applied Biodiversity
Science, Conservation International, 1919 M Street NW,
Washington, DC 20036, USA. E-mail: <a.rylands@
conservation.org>.
References
Collins, A. C. and Dubach, J. 2000. Phylogenetic relationships
of spider monkeys (Ateles) based on mitochondrial DNA
variation. Int. J. Primatol. 21(3): 381– 420.
Neotropical Primates 9(3), December 2001
Defler, T. R. and Hernández-Camacho, J. I. In press. T he true
identity and characteristics of Simia albifrons Humboldt,
1812: Description of neotype. Neotrop. Primates.
Groves, C. P. 2001. Primate Taxonomy. Smithsonian
Institution Press, Washington, DC.
Hernández-Camacho, J. and Cooper, R. W. 1976. The nonhuman primates of Colombia. In: Neotropical Primates: Field
Studies and Conservation, R. W. Thorington Jr. and P. G.
Heltne (eds.), pp.35– 69. National Academy of Sciences,
Washington, DC.
Hershkovitz, P. 1949. Mammals of northern Colombia.
Preliminary report No. 4: Monkeys (Primates), with
taxonomic revisions of some forms. Proc. U. S. Nat. Mus.
98: 323– 427.
Hershkovitz, P. 1977. Living New World Monkeys (Platyrrhini)
with an Introduction to Primates, Vol. 1 . Chicago University
Press, Chicago.
Hershkovitz, P. 1987. Uacaries, New World monkeys of
the genus Cacajao (Cebidae, Platyrrhini): A preliminary
taxonomic review with the description of a new subspecies.
Am. J. Primatol. 12: 1–53.
Hill, W. C. O. 1957. Primates. Comparative Anatomy
and Taxonomy III. Pithecoidea Platyrrhini (Families
Hapalidae and Callimiconidae). Edinburgh University Press,
Edinburgh.
Hill, W. C. O. 1960. Primates. Comparative Anatomy and
Taxonomy IV. Cebidae Part A. Edinburgh University Press,
Edinburgh.
Hill, W. C. O. 1962. Primates. Comparative Anatomy and
Taxonomy V. Cebidae Part B. Edinburgh University Press,
Edinburgh.
Kobayashi, S. and Langguth, A. 1999. A new species of
titi monkey, Callicebus T homas, from north-eastern Brazil
(Primates, Cebidae). Rev. Bras. Zool. 16(2): 531–551.
Rosenberger, A. L. 1981. Systematics: the higher taxa.
In: Ecology and Behavior of Neotropical Primates, Vol. 1,
A. F. Coimbra-Filho and R. A. Mittermeier (eds.), pp.9–27.
Academia Brasileira de Ciências, Rio de Janeiro.
Rylands, A. B. 1999. T he name of the weeper or wedgecapped capuchin in the Guianas. Neotrop. Primates 7(3):
89–91.
Rylands, A. B. and Brandon-Jones, D. 1998. T he scientific
nomenclature of the red howlers from the northeastern
Amazon in Brazil, Venezuela and the Guianas. Int. J.
Primatol. 19(5): 879–905.
Rylands, A. B., Schneider, H., Langguth, A., Mittermeier,
R. A., Groves, C. P. and Rodríguez-Luna, E. 2000. An
assessment of the diversity of New World primates. Neotrop.
Primates 8(2): 61–93.
Silva Jr., J. S. and Noronha, M. de A. 1998. On a new species
of bare-eared marmoset, genus Callithrix Erxleben, 1777,
from central Amazonia, Brazil (Primates: Callitrichidae).
Goeldiana Zoologia (21): 1–28.
Van Roosmalen, M. G. M., Van Roosmalen, T., Mittermeier,
R. A. and Rylands, A. B. 2000. Two new species of
marmoset, genus Callithrix Erxleben, 1777 (Callitrichidae,
Primates), from the Tapajós/Madeira interfluvium, south
central Amazonia, Brazil. Neotrop. Primates 8(1): 2–18.
Neotropical Primates 9(3), December 2001
NEWS
JORGE IGNACIO H ERNÁNDEZ-CAMACHO
J ANUARY 17, 1935 - SEPTEMBER 15, 2001
Jorge
Ignacio
HernándezCamacho, “Mono Hernández,”
was a remarkable naturalist. His
complete dedication and his
genius allowed him to maintain
an encyclopedic knowledge of
many aspects of the paleontology,
taxonomy, ecology, and distributions of the Colombian
fauna and flora. He was a mentor
for an entire generation of
Colombian biologists, not to mention the many foreigners
who profited from information that he would always most
willingly provide.
I first heard of Mono in 1975 when Heliodoro Sánchez, then
of Parques Nacionales-INDERENA, suggested that I write
to him about a project I was proposing in the Serranía La
Macarena to study woolly monkeys. I was still finishing my
Ph.D. I knew nothing about woolly monkeys, and even
less about Colombia, but I did know what I was going
to do with the rest of my life, that is, dedicate myself to
the tropical forest and its conservation. Jorge Hernández,
evidently understanding the passion I must have put into
the letter, answered me in a typewritten three-page missive.
I was not disappointed. T he letter was a tour de force of
the status of the woolly monkey in Colombia up to that
point, filled with detailed facts of their natural history, and
providing such an extraordinary amount of information that
I was completely astonished that he should have taken so
much time to answer me in such depth. I began planning a
move to Colombia, using Mono’s advice to get in touch with
the local Peace Corps program, through another Colombian
biologist, Ernesto Barriga, in charge at the time.
Because Jorge was advisor to so many people, he was not easy
to pin down to a meeting in Bogotá, and my first attempts
involved days of waiting outside his office. In those days he
was head of terrestrial fauna at INDERENA, a government
natural resource agency that he had helped to organize and
which was the precursor to the present day Ministry of the
Environment. His days were always filled with people asking
his opinion, his advice, his help, and a young foreigner had to
wait. But our first meetings were like his letters, only better as
they ranged through many themes with inevitable taxonomic
stops along the way. Unfortunately American universities
prepare students very poorly in taxonomy, and in my early
Colombian days it was wholly alien to my interests. It must
have been difficult for him to talk to me about Colombian
geography, the basis for grasping the details of primate
distributions, since I knew so little then. I found that I
was ignorant of much, but Mono’s extraordinary patience
125
and personal diplomacy meant that my understanding of the
many taxonomic problems grew painlessly, not only in my
area of primatology, but for other groups as well, and I began
to grasp the complexity of Colombian geography and species’
distributions, and the reasons why Colombia is considered
truly a “megadiverse” country. One of his insistent lessons was
that the study of Neotropical taxonomy was essential to our
understanding of the full extent of Neotropical biodiversity.
While helping me to prepare for my first field experience,
Jorge Hernández was gently educating this new Ph.D. who
knew essentially nothing about Colombia and very little
about Colombian monkeys.
Usually a late office meeting with him ended with the
invitation “Vamos a tomar un traguito” (“let’s go have a little
drink”) and we would put our coats on and walk up to
one of his favorite watering holes to continue a conversation
that easily might have begun 2–3 hours before. In those
years, Mono’s “after hours” spot was just a block up from
INDERENA, beside 26th Avenue, but after the place became
known to so many, I think he decided to change it a bit
to the north to the now (among the Mono’s friends and
admirers) famous Casa Mendoza, his informal Bogotá office
into the night. T hese meetings inevitably went on until
midnight when the place would attempt to close, not easy
for the owners, since their best client often ignored their
admonitions and continued to hold forth on some biological
topic that had been chosen for the night. T he extended
conversations about the Colombian biota were usually in
the form of a monologue from Jorge, which in later years
I finally learned to write down, encouraged by him; since
normal person that I am, I could not hope to remember the
rich detail that he provided. T his was the “University of the
Mono” and this was where I continued my education, right
up until he left us.
In later years he preferred to come to my Bogotá apartment
for our meetings, but by then they required many books and
references and, at least talking about primates, I possessed
many of them. Always the meetings involved the ubiquitous
rum and coca-cola and voluminous clouds of cigarette smoke,
for Jorge was a chain smoker until the day he died, and a
meeting with the Mono would always last 4 – 6 hours. So
you had to have stamina. I usually did. You had to accept
the smoke and the late hours, and you had to drink rum
and coca-cola, because drinking beer that long just doesn’t
work! T here were times in our relationship when I could not
accept these terms, but I always weakened. T he truth was, if
I wanted to enjoy his company I must also survive the smoke
and the booze.
Well, I learned to like the booze. I also got to the point where
it was worthwhile for Jorge to collaborate on some primate
papers, far too few for the time that we knew each other,
but by then I was spending most of my time in remote
corners of eastern Colombia and could not stay extended
periods in the city. A few years back, however, I realized that
I must concentrate on producing a few papers which we
had discussed, for his health was not so good, with so many
126
Neotropical Primates 9(3), December 2001
years of smoky meetings with Colombians and foreigners
and friends and I realized that he would probably not be with
us for too much longer. I am particularly relieved that we
both insisted on these projects, as they came to fruition just
before he left us and will form part of his legacy.
But research and writing papers were only a small part
of this great gentleman’s repertoire. T he present form and
content of Colombian National Parks is especially due
to his efforts. T he complexity and comprehensiveness of
Colombian environmental legislation is in great part due
to him. T he university degrees of many, many Colombians
have been successfully completed due to his often profound
intellectual support. T he acceptance of the CIT ES treaty and
Colombia’s international contribution during the early years
is mostly due to his efforts.
His inspiration touched many others besides myself. He was
one of the small circle of Colombian friends that I knew I
would lose touch with if I were to accept a tempting offer
in 1983 from Russell Mittermeier to work on Brachyteles in
Brazil. Even then, a consideration of what his professional
influence had meant to me was enough to make me realize
that I would continue to invest my future in this tragic yet
biologically fantastic country, Colombia. I owe him much,
both professionally and personally. I shall miss him dearly.
Thomas Defler, Instituto Amazónico de Investigaciones,
Universidad Nacional de Colombia, Apartado Aéreo 215,
Leticia (Amazonas), Colombia.
JORGE IGNACIO H ERNÁNDEZ-CAMACHO
E NERO 17
DE
1935 - SEPTIEMBRE 15
DE
concerning the cotton-top tamarin, Saguinus oedipus, endemic
to the country.
Characterizing his contributions to primatology would be
incomplete without mentioning his role as maestro and
guide for innumerable Colombians and foreigners dedicated
to primates. His enormous knowledge and his holistic vision
of conservation problems were part of the justification for
pre-selection of the geographic areas which make up what is
today the national system of natural parks in Colombia.
It has been frequently recognized that his awesome capacity
to accumulate information and to comparatively analyze
it, helped to form the pillars of Colombian environmental
institutions. Also, it is important to recognize that the origins
of the legal structures and laws which are in force today and
the solidity of the National Code for Natural and Renewable
Resources and the Environment, including its various legal
decrees, are due to his genius and to his broad vision
and knowledge of national and international environmental
problems.
But more than all this, Jorge Ignacio Hernández-Camacho
leaves us a legacy of professional honesty, personal decency
and love for nature which few people have left in this world. It
is certain that we have undoubtedly lost the “last Neotropical
naturalist” as he was once called by Phillip Hershkovitz,
but his recommendations, formed in the context of his
cultural heritage, his goodness and great selflessness, should
be examples to follow in order to secure a future for our
natural heritage.
José Vicente Rodríguez-Mahecha, Conservation International, Carrera 13 # 71-41, Bogotá, Colombia.
2001
In memoriam
Jorge Ignacio Hernández-Camacho, affectionately known as
“el Mono”, was the true “Father of Colombian Primatology”,
since it was under his leadership and advice that the first
studies were begun, and under his supervision and inspiration
that so many were carried out in subsequent years. His
first publication concerning this group of mammals was the
discovery of Goeldi’s monkey, Callimico, in Colombia in
1966, but his most important and basic contribution was his
classic review of the status and distribution of Colombian
primates: J. Hernández Camacho and R. W. Cooper 1976.
The nonhuman primates of Colombia, in Neotropical Primates:
Field Studies and Conservation, R. W. Thorington, Jr. and P.
G. Heltne (eds.), pp.35– 69, National Academy of Sciences,
Washington, DC. During his life he was always interested in all
aspects relating to primatology, as much in terms of taxonomy
and systematics as from the viewpoint of the conservation and
sustainable-use of the rich Colombian primate fauna. A theme
of particular interest to him was biomedical research. I had the
opportunity to share his passion and co-author several papers
in various projects which we advanced together, especially
C ONSERVATION
INTERNATIONAL’S
AWARDED BRAZIL’S H IGHEST H ONOR
PRESIDENT
In recognition of his years of
conservation work in Brazil, CI
President Russell Mittermeier
was awarded the National
Order of the Southern Cross by
the Brazilian government. Dr.
Mittermeier received the award
on August 29 at the Brazilian
Ambassador’s residence in
Washington, DC. T he National
Order of the Southern Cross
was created in 1922 to recognize the merits of individuals
who have helped to strengthen Brazil’s relations with the
international community. T he award is the highest given to
a foreign national for service in Brazil.
For the past three decades, Mittermeier has been a leader
in promoting biodiversity conservation in Brazil and has
conducted numerous studies on primates and other fauna in
127
Neotropical Primates 9(3), December 2001
the country. During his time with the World Wildlife Fund
(1978–1989), he played a key role in putting Brazil’s Atlantic
Forest, one of the planet’s highest-priority hotspots, on the
international conservation agenda. He became well-known
throughout the country after, with Adelmar Coimbra-Filho
(then of the Rio de Janeiro Primate Center), successfully
mobilizing international support for the endangered lion
tamarins, and with Célio Valle (then Professor of Zoology
at the Federal University of Minas Gerais), creating similar
national and international attention for the muriquis;
campaigns that sparked a newfound pride in the country’s
native animals. Mittermeier was also instrumental in the
creation of Conservation International-Brazil, which has
since become one of the country’s leading conservation
advocates.
Patrick Johnston, Conservation International, 1919 M St.
NW, Suite 600, Washington, DC 20036, USA. E-mail:
<p.johnston@conservation.org>.
PRÊMIO VON MARTIUS 2001 C ONCEDIDO
INSTITUTO F LORESTAL DE SÃO PAULO
AO
O Instituto Florestal de São Paulo teve o trabalho
“Geoprocessamento no Levantamento da Vegetação e no
Suporte às Unidades de Conservação” premiado pela
Câmara de Comércio e Indústria Brasil-Alemanha, na
categoria Tecnologia do Prêmio Ambiental von Martius-2001,
patrocinado pelas empresas Henkel S/A, Deutsche Bank e
TetraPak S/A. Concorreram ao referido prêmio 191 trabalhos,
sendo que foram premiados nove; três para cada uma das
categorias (humanidade, natureza e tecnologia). O trabalho
conduzido pelo Instituto Florestal relata as ações referentes
ao Levantamento da Vegetação Natural, com abrangência
estadual e aquelas referentes à estruturação de base digital
das Unidades de Conservação. São parceiros deste trabalho
a Universidade de Campinas (UNICAMP) e a Escola
Superior de Agricultura “Luiz de Queiróz” da Universidade
de São Paulo (USP), Piracicaba. Na parte referente ao
reflorestamento, houve envolvimento das empresas do setor
de celulose, papel e chapas, com participação direta da
Sociedade Brasileira de Silvicultura (SBS). Fonte: Instituto
Florestal, 10 August 2001.
E COLOGÍA AUSTRAL
Ecología Austral is the scientific journal of the Argentine
Ecological Society. It publishes original scientific articles on
any area of the environmental sciences. Articles may be (1)
Original research: results of field, experimental or theoretical
research, (2) Reviews: papers reviewing the present knowledge
of a topic, and (3) Short communications: short papers
reporting on a minor work representing an improvement in
general knowledge or a methodological development. Articles
are peer reviewed by at least two referees. Manuscripts are
accepted in Spanish, English or Portuguese. T he Editor-inChief is seeking the help of reviewers in any of the three
languages of the journal. To this end, a data base is being
developed (about 120 reviewers already entered), in order to
have a wide range of expertise available, and also to avoid
requesting reviews from the same expert too frequently.
For those interested in volunteering for the peer review
process please send a message to: Dr. Jorge Rabinovich,
Editor, Ecología Austral, e-mail: <ecol_aus@netverk.com.ar>.
From: NeoCons, 1(2), April 2001, Neotropical Conservation
Biology Bulletin: http://www.conservationbiology.org/SCB/
Publications/NeoCons/>.
Q UATORZE RESERVAS PARTICULARES (RPPNS) NOVAS
BRASIL
NO
O presidente do Instituto Brasileiro do Meio Ambiente
e dos Recursos Naturais Renováveis (Ibama), Hamilton
Casara, assinou portarias no dia 16 de outubro de 2001,
reconhecendo mais 14 propriedades privadas como Reservas
Particulares do Patrimônio Natural (RPPNs), em nove
estados: São Paulo, Rio de Janeiro, Ceará, Rondônia, Bahia,
Maranhão, Santa Catarina, Minas Gerais, e Mato Grosso do
Sul. Ao transformar suas terras em RPPNs os proprietários
terão vários benefícios: incentivos fiscais e assessoria técnica do
Ibama, podendo utilizá-las apenas para projetos ambientais,
como ecoturismo e educação ambiental, desde que não
alterem sua biodiversidade original.
Com estas, são 353 RPPNs no Brasil, protegendo
380.660,327 ha dos principais biomas. A maior, protege
87 mil hectares do Pantanal em Mato Grosso; e, a menor,
apenas 1 ha de cerrado, no Distrito Federal. As savanas da
região Centro-Oeste são as mais bem protegidas por RPPNs:
são 64, cobrindo 215,385 ha; 33 protegem 120,274 ha de
Floresta Amazônica, na região Norte; 82 estão no nordeste
protegendo 88,657 ha de Caatinga; 117 ficam no Sudeste
protegendo 39,280 ha de Mata Atlântica e da Zona Costeira;
e, 44 estão no sul protegendo 15,614 ha de Mata Atlântica,
de Campos Sulinos, e, de Costa.
A maior das novas RPPNs é em Rondônia: O Parque Natural
Leonildo Ferreira, com 981 ha de Floresta Amazônica
no município de Pimenta Bueno. A menor é o Parque
Arqueológico da Serra do Santo Antonio, com apenas 9 ha
de Mata Atlântica no município de Andrelândia. A segunda
maior, é em Mato Grosso do Sul. A Fazenda Floresta Negra
protegerá 971 ha de Floresta Amazônica no município de
Sete Quedas. As cinco novas RPPNs reconhecidas em São
Paulo protegerão 803,63 ha de Mata Atlântica. Incluem:
Palmira, com 242 ha no município de Serra Azul; Meambros
II, com 145,20 ha, e Meambros III, com 72,60 ha, no
município de Ibiúna; Fazenda Serrinha, com 117,30 ha, no
município de Bragança Paulista; e, Meambros, com 11,30 ha
no município de Ibiúna. Por ordem de abrangência, o Ibama
reconheceu como RRPNs: no Ceará (duas) totalizando
128
Neotropical Primates 9(3), December 2001
704,17 ha de Caatinga: Monte Alegre, com 263,17 ha
no município de Quixeramobim, com 441 ha; em Santa
Catarina, a Chácar Edith, com 415,79 ha de Mata Atlântica,
no município de Brusque; no Rio de Janeiro, a Reserva
Ecológica Floresta Alta, com 380,90 ha de Mata Atlântica
no município de Silva Jardim; no Maranhão, no município
de Rosário, protegerá 349 ha de Floresta Amazônica; na
Bahia, Pedra do Sabiá, com 22 ha de Mata Atlântica no
município de Itacaré; e, em Minas Gerais, a Reserva tem
apenas 9 ha de Mata Atlântica e de Cerrado no município
de Andrelândia.
Para obter o reconhecimento do Ibama como RPPN o
proprietário precisa provar que o imóvel é importante para a
conservação da biodiversidade de determinado bioma (flora
e fauna), e/ou possui belezas cênicas. Criado em 1990, o
programa RPPN é importante para a conservação da natureza
porque: contribui para uma rápida ampliação das áreas
protegidas do país; atua como zonas tampão no entorno dos
parque e reservas, formando corredores ecológicos; apresenta
índices altamente positivos na relação custo/benefício; é
facilmente regulamentada; permite a participação da iniciativa
privada no esforço nacional de conservação; e, contribui para
a conservação da biodiversidade dos biomas brasileiros.
Como benefícios, os proprietários de RPPNs asseguram:
preservação do direito de propriedade; isenção do Imposto
sobre a Propriedade Territorial Rural (IT R) transformada
em RRPN; prioridades nas análises dos projetos pelo
Fundo Nacional do Meio Ambiente e na concessão de
crédito agrícola junto às instituições oficiais; permissão para
implantar atividades de recreação, lazer, educação ambiental,
pesquisa, cultura, e ecoturismo na área reconhecida pelo
Ibama; e, cooperação com entidades privadas e públicas na
proteção da RPPN.
D EVELOPMENTS
PROSPECTS
IN
PRIMATOLOGY: PROGRESS
AND
Kluwer Academic/Plenum Publishers is pleased to introduce
Developments in Primatology: Progress and Prospects (formerly
Advances in Primatology), a new series under the direction
of the Editor-in-Chief of the International Journal of
Primatology: Dr. Russell H. Tuttle, University of Chicago,
Chicago, Illinois.
T his peer-reviewed book series will meld the facts of
organic diversity with the continuity of the evolutionary
process. T he volumes in this series will exemplify the
diversity of theoretical perspectives and methodological
approaches currently employed by primatologists and
physical anthropologists. Specific coverage includes: primate
behavior in natural habitats and captive settings; primate
ecology and conservation; functional morphology and
developmental biology of primates; primate systematics;
genetic and phenotypic differences among living primates;
and paleoprimatology.
Volume authors will be invited to participate based on their
expertise in a given area and overall approval by the series
editor. Volume authors and editors will receive generous
royalties, complimentary copies and full marketing and
editorial support. Contributors will receive complimentary
copies as opposed to royalties. All manuscripts will be “typeset
from disk” for the convenience of the author/editor. Volumes
will be approximately 300 printed pages (all page lengths are
negotiable) in a 6 1/2 x 9 7/8 format. For further information
on how to contribute an authored or edited volume to this
series please contact Andrea Macaluso at (212) 620-8007 or
via e-mail at <amacaluso@wkap.com>.
Russell H. Tuttle, Department of Anthropology, T he
University of Chicago, 1126 East 59th Street, Chicago,
Illinois 60637, USA.
RPPN FELICIANO MIGUEL ABDALA - A PROTECTED
AREA FOR THE NORTHERN MURIQUI
T he Atlantic Forest region of Brazil is one of the richest
and most diverse forest systems in the world; it is also
one of the most threatened, ranking among the five top
biodiversity hotspots on Earth. Although it once covered
some 1.2 million km², it has been reduced to about 7% of
its original extent. Needless to say, many of the animals and
plants living in this region are severely threatened, and a large
number are now at risk of extinction.
Primates have long been the most important symbols for the
Atlantic Forest, and their situation is indicative of what is
happening to the region as a whole. Some 24 species and
subspecies are found in the Atlantic Forest, many of them are
now considered endangered or critically endangered. One,
the northern muriqui, Brachyteles hypoxanthus, the largest
mammal endemic to Brazil and a species of great charm and
appeal, ranks high on the list of most endangered primates,
and has become a flagship species of enormous importance
to Brazil. Only about 300 individuals remain in the wild,
and half of those occur in a single forest, in the region of
Caratinga, in the state of Minas Gerais.
Like the northern muriquis, Caratinga is very special.
T he area had been effectively protected by its owner, the
late Senhor Feliciano Miguel Abdala, since the 1950’s. A
successful coffee farmer, Sr. Feliciano set aside about 2200
acres of relatively untouched Atlantic rainforest at the Montes
Claros farm in the mountainous reaches of the state of Minas
Gerais in southeastern Brazil to provide a sanctuary for the
fauna and flora - for no other reason than that he thought
it was a good idea and the right thing to do. Abdala was
especially fond of the muriqui. For more than five decades,
he protected the forest at Caratinga, while his neighbors
dismissed him as a quack for “squandering” good farmland.
When Abdala reluctantly allowed researchers to study his
farm, Brazilian conservation pioneer, Alvaro Aguirre, visited
129
Neotropical Primates 9(3), December 2001
the site during a region-wide survey in the late 1960’s,
introducing Caratinga’s forest to the scientific community.
However, it received little attention, buried as it was in a list
of several areas still believed to harbor muriquis at the time.
By the mid-1970’s, the situation of the Atlantic Forest had
deteriorated to such an extent that the muriqui was thought
to be extinct in the state.
In 1976, the Caratinga population was rediscovered by
Professor Célio Valle of the Federal University of Minas
Gerais. T he first ever field study of Brachyteles in the wild,
was carried out there in 1977, by the Japanese primatologist
Akisato Nishimura. In late 1979, Russell Mittermeier, Célio
Valle and Adelmar F. Coimbra Filho, the pioneer of Brazilian
primatology, visited Caratinga while surveying for primates
in the protected areas of the Atlantic Forest. T here, they
found muriquis, as well as healthy populations of three
other primate species: the brown howler monkey (Alouatta
guariba ), the tufted capuchin (Cebus nigritus), and the buffheaded marmoset (Callithrix flaviceps) never recorded in
Minas Gerais prior to this visit. Indeed, after a decade of
primate survey work that ended in the late 1980’s, Caratinga
was seen as one of the single most important sites for primate
conservation in the entire Atlantic Forest and was made the
focus of an education campaign for Atlantic Forest primates,
using the muriqui as the obvious flagship species. Brazilian
and foreign researchers were enlisted to come and work at
Caratinga, in an attempt to stimulate further research on its
unique primate community.
Karen Strier began her groundbreaking muriqui research in
1982, and her 20-year study has now become one of the
classics of primatology. Many other researchers have also
worked there, including leaders in Brazilian conservation,
such as Gustavo Fonseca and Sérgio Mendes. T hese studies
convinced Abdala of the scientific importance of Caratinga,
and his mistrust gave way to enthusiastic support. He
responded by creating a field laboratory which, in 1983,
became the Biological Research Station at Caratinga. Since
then the Caratinga Biological Station has proven to be one
of the most productive sites for primate research in all South
America, resulting in more than 50 scientific publications
by national and international researchers. In addition, a
small-scale visitor program has been introduced, encouraging
ecotourism, and a small tree nursery has been established
for the purposes of reforestation and habitat enrichment. An
environmental education and awareness program has also
been started.
For the past 18 years, Eduardo Marcelino Veado, current
director of tha Caratinga Biological Station and VicePresident of the local NGO, Associação Pró-Estação Biológica
de Caratinga, has managed these activities at the Station. He
has been working closely with the Abdala family to ensure
permanent protection of the Montes Claros Farm. After Sr.
Abdala’s death last year (June 1, 2000), his family decided
to follow his wishes for continued protection of the forest,
and agreed to the creation of an official private reserve
under Brazilian law, to help preserve the muriquis, together
with the black-capped capuchin, brown howler monkey and
buffy-headed marmoset, the latter two currently listed by the
IUCN as Vulnerable and Endangered, respectively. Caratinga
is also home to a diverse fauna, including approximately 217
species of birds, 45 species of mammals and 16 species of
amphibians.
On the 3 rd September, 2001, the President of the Brazilian
Institute for the Environment (Instituto Brasileiro do Meio
Ambiente e dos Recursos Naturais Renováveis - IBAMA) of
the Ministry of the Environment, signed Decree 116/2001
declaring the Fazenda Montes Claros forests a Private Natural
Heritage Reserve (Reserva Particular de Patrimônio Natural
- RPPN). T he private reserve, with 957 ha (or 2,365 acres
- equivalent to three times the size of New York’s Central
Park), has been named “RPPN Feliciano Miguel Abdala”, in
tribute to the man who, nearly 60 years ago, decided to save
this valuable legacy of our forest heritage.
On September 24, 2001, during a party in the town of
Caratinga to celebrate the creation of the Reserve, Federal
authorities presented the town with the Zero issue of a
Federal Lottery ticket bearing the Muriqui as its symbol. T he
lottery ticket illustrated with the muriqui reached all corners
of Brazil.
Maria Inês Castro, Brazil Regional Program, Conservation
International, 1919 M Street NW, Suite 600, Washington,
DC 20036, USA. E-mail: <i.castro@conservation.org>.
VERSION 2.0
AVAILABLE
OF
RAMAS RED L IST SOFTWARE
Version 2.0 of the RAMAS® software used for assessing the
conservation status of species for possible inclusion in the
IUCN Red List of T hreatened Species, is now available. T he
software incorporates the revised Red List Categories (2000)
(see below). To purchase a copy, please contact Isabelle
Weber, IUCN/SSC, Rue Mauverney 28 CH-1196 Gland,
Switzerland, Fax: +41-22-9990015; e-mail: <isc@iucn.org>
or Applied Biomathematics, 100 North Country Road,
Setauket, NY 11733, USA, Fax: +1 516-751-3435. Singleuser and site-licensed copies of the software are priced
US$295 and US$445 respectively. From: IUCN Species
Survival Commission (SSC) E-Bulletin - May 2001. Anna
Knee, Communications Officer SSC/IUCN.
REVISED RED L IST C RITERIA
T he new improved categories and criteria used for listing
plants and animals on the IUCN Red List of T hreatened
Species are now available after a four-year review which
was called for by IUCN members. T he review, coordinated
by SSC, involving broad consultation with users and
organizations from around the world, has produced a clearer,
130
Neotropical Primates 9(3), December 2001
more open, and easy-to-use system for assessing species.
With particular attention paid to marine species, harvested
species, and population fluctuations, the review has refined
the effectiveness of the Red List categories and criteria
as indicators of extinction risk. See <http://www.iucn.org/
themes/ssc/redlists/RLcategories2000.html> for more details.
From: IUCN Species Survival Commission (SSC) E-Bulletin
- March 2001. Anna Knee, Communications Officer SSC/
IUCN.
A CD-ROM OF W ILDLIFE SOUNDS IN THE ATLANTIC
FOREST
With support from the Margot Marsh Biodiversity
Foundation and Conservation International, the Caratinga
Biological Station produced 3,000 CDs (from EarthEar) with
the soundscapes of the Fazenda Montes Claros forest, now
the “RPPN Feliciano Miguel Abdala” in Minas Gerais, Brazil.
T he "Caratinga" CD, produced pro-bono by Douglas Quin,
presents a day in Brazil's disappearing Atlantic rainforest,
starting with a stream and birds in the early morning,
followed by the sounds of howler (Alouatta guariba ) and
capuchin monkeys (Cebus nigritus). Marmosets, Callithrix
flaviceps, call after their midday rest, and muriquis, Brachyteles
hypoxanthus - stars of this CD - are recorded calling, moving
and feeding in trees near the biological station. T he day
proceeds with an afternoon storm and closes with the sound
of frogs in the forest. T he CD includes a 20-page booklet,
beautifully illustrated by Stephen Nash (State University
of New York – Stony Brook). with detailed track notes
and essays in English and Portuguese. It will be used
to promote the conservation of Caratinga’s forest at various
levels, from raising awareness in Caratinga schools and
other local community organizations, to introducing these
remarkable soundscapes to the general public in Brazil
and worldwide. Proceeds from the sale of the CD go to
support the conservation efforts of the Biological Station at
Caratinga. See http://www.dqmedia.com/caratinga/booklet
.pdf;
<http://www.dqmedia.com/caratinga/traycard.pdf>;
<http://www.dqmedia.com/caratinga/cd.pdf>.
Maria Inês Castro, Brazil Regional Program, Conservation
International, 1919 M Street NW, Suite 600, Washington,
DC 20036, USA. E-mail: <i.castro@conservation.org>.
PRIMATE L IT NOW AVAILABLE
FOR
SEARCHING
T he Wisconsin Regional Primate Research Center is pleased
to announce that PrimateLit, the primary database for
searching the literature of primatology, is now available in
a new web format. T he database includes over 170,000
citations and covers the literature from 1940 to date. Indexed
by the Primate Information Center in Seattle and managed
by the Wisconsin Regional Primate Research Center in
Madison, PrimateLit is being released in “test” mode. We
would very much appreciate feedback from members of
Primate-Science - comments and suggestions on how it can
be modified and improved to meet your needs. Current
Primate References, formerly a print only publication, has
been recreated in the web environment to afford access to the
most recent literature. In this release the default is set at six
months. We will be gradually phasing in 1, 2 and 3 month
options.
T he National Center for Research Resources is supporting
this service - without fees or passwords - for everyone in the
international scientific community who needs access to the
nonhuman primate research literature. Future enhancements
in development include: tailored display and print options;
enhanced navigational features and search functions; and
access to the PrimateLit T hesaurus of index terms.
Special thanks go to Nolan Pope, Sue Dentinger, Mark
Foster and Rose Smith of the University of WisconsinMadison Libraries who have worked with Jackie Pritchard
and Chico Otsuka-Gooding of the Primate Information
Center to oversee the migration of PrimateLit to Madison
and to deal with the countless details that attend remounting
a large database. Please take a critical look - we need
your feedback. Send your comments to me or Jackie
Pritchard, PIC Manager, e-mail: <plj@u.washington.edu>.
Supported through NCRR Grant RR15311, Coordinated
Information Services to Support Primate Research. URL:
<http://primatelit.library.wisc.edu/>.
Larry Jacobsen, Director, WRPRC Library and Information
Service, Wisconsin Regional Primate Research Center,
University of Wisconsin-Madison, 1220 Capitol Court,
Madison, WI 53715-1299, USA. E-mail:<jacobsen@
primate.wisc.edu>.
PRESIDENTE
DA
INTERNACIONAL
SPVS
GANHA
PRÊMIO
O presidente da SPVS - Sociedade de
Pesquisa em Vida Selvagem, Clóvis Ricardo
Schrappe Borges, recebeu o prêmio 2001
World Climate Technology and Leadership Award, que é
concedido anualmente pela AIE - Agência Internacional de
Energia através do programa ITC - Iniciativa pela Tecnologia
Climática, para indivíduos e organizações que alcançaram
avanços no uso de tecnologias que não sejam nocivas ao clima.
A SPVS tem sede em Curitiba, Paraná, e atua na proteção
de florestas brasileiras. A organização é pioneira em projetos
de seqüestro de carbono no país, através do programa de
Ação Contra o Aquecimento Global, que pretende retirar da
atmosfera, em 40 anos, 2,5 milhões de toneladas de carbono,
através de reflorestamento e desenvolvimento sustentado
no litoral do Paraná. Muito importante, também têm sido
as ações da SPVS em favor da preservação das florestas e
manguezais da região de Guaraqueçaba, cubrindo a área onde
ocorre o mico-leão-de-cara-preta, Leontopithecus caissara . A
131
Neotropical Primates 9(3), December 2001
cerimônia ocorreu no dia 6 de novembro no Marrocos,
durante a VII Conferência das Partes da Convenção-Quadro
da Nações Unidas sobre Mudança do Clima (COP-7),
principal fórum da ONU sobre mudança climática.
PRIMATE B EHAVIOR
POSITION AVAILABLE
AND
E COLOGY FIELD C OURSE
El Zota Biological Field Station is offering a field course
in primate behavior and ecology taught at a new field site
in northeastern Costa Rica. T he Field Station is home to
howler monkeys, capuchins, and spider monkeys, as well as
endangered fauna such as jaguars and tapir. Students attend
nightly lectures, learn various methods of field techniques
used for the study of primate behavior and ecology, and
conduct their own research project on one of the three
primate species at El Zota.
T his course is included in the curriculum at Iowa State
University and is listed as Anthropology 445/545. Students
receive 4 credits for the course, but arrangements can be
made to receive 6 credits with the addition of 2 credits
of independent study. T his would entail the inclusion of
additional library research and writing as well as other
requirements. Students are not required to enroll at Iowa
State University in order to take the course. Students should
have had a college-level course in basic Biology, Ecology, or
Anthropology and require a health check-up and medical
insurance before they are accepted into the course.
T he cost of the course is approximately $1350. Support
provided for internship/volunteer positions (travel, meals,
lodging): A limited number of internships are available, but
students are required to be enrolled at an El Zota course in
order to be eligible. T he Course will be taught from July 15
through August 11, 2002. Application Deadline: April 2002.
Other courses, such as Tropical Herpetology are also taught
at El Zota and students are also given the option of traveling
to other areas of Costa Rica during a short mid-course trip.
El Zota is sponsored by the non-profit organization DANTA:
Association for Conservation of the Tropics, which organizes
and accounts for course fees students pay to the station.
For further information contact: Jill D. Pruetz, Department
of Anthropology, Iowa State University, Ames, IA 50011,
USA, Tel: (515) 294-5150, e-mail: <pruetz@iastate.edu>.
FUNDACIÓN E COLOMBIA
Colombia is rich in plant and animal species, a number
of which are smuggled illegally out of the country every
day. Some zoos in Colombia serve as quarantine and
holding stations for wildlife confiscated by the environmental
authorities but, due to the high number of seizures,
programs and centers for rehabilitation, reproduction and
reintroduction are needed. Fundación Ecolombia is a private
non-profit institution created in 1999 to promote sustainable
economic alternatives to illegal wildlife traffic of fauna and
flora, specifically for the communities that live off this
activity. Its goals also include, promoting and managing
rehabilitation and reproduction centers for native wildlife
particularly for those species at risk of extinction and
promoting educational programs that prevent the hunting,
capture and trade of wildlife.
Fundación Ecolombia has recently leased 83 ha from the
government to establish a Rehabilitation Center. Dry forest
covers 46 ha, and the rest is cattle pasture which is currently
being restored with native species, permitting the natural
regeneration of the area. Eventually a further 100 ha adjacent
to the land will be integrated into the program. T he project
is located in the town of La Pintada, an area heavily hunted
in the past. Current projects include: T he rehabilitation and
reintroduction of confiscated primates presently caged in
the Santa Fé Zoo, 25 red howlers (Alouatta seniculus), 12
black spider monkeys (Ateles fusciceps) and 18 cotton-top
tamarins (Saguinus oedipus); development of captive breeding
programs for the blue-billed curassow (Crax alberti) and the
green macaw (Ara militaris), for later reintroduction in their
original habitats; development of conservation and population
studies for the white-footed tamarin (Saguinus leucopus); and
implementation of handicraft and environmental education
programs in communities neighboring the conservation
area.
For more information contact: Fundación Ecolombia,
A.A. 75972, Medellin, Colombia, Tel: 57 4 281 40
97, e-mail: <contacto@fundacionecolombia.org>. Website:
<www.fundacionecolombia.org>.
MASTERS C OURSE
IN
PRIMATE C ONSERVATION
T he Oxford Brookes University in Oxford, United Kingdom,
is offering a masters course in primate conservation aimed
at providing a high quality research qualification relevant to
the careers of anthropologists, conservation biologists and
educators. T he course term is from October 2002–September
2003. Each student will be encouraged to build on their
own strengths and interests through a choice of a practical
assignment and co-authorship of a relevant chapter of the
house journal. Eight major themes are covered in the course:
primate diversity and biogeography, socio-political aspects
of conservation, environmental education, molecular and
population genetics, fieldwork training and methods, captive
management, museum studies, habitat protection and the
future of rainforests. Qualifications include: Honors degree
in anthropology, biology or acceptable related discipline.
Undergraduate students will be considered if they can
demonstrate ability to work at an advanced level. Costs
for the course: £7350 for full time overseas students,
£2988 for full time EU students and £1494 for part time
132
Neotropical Primates 9(3), December 2001
EU students. T he application deadline is May 31, 2002.
Applications are available at: <www.brooks.ac.uk/courses/
pgcourses/application/down.html>. For further information
contact: Simon Bearder, School of Social Sciences and
Law, Gypsy Lane Campus, Oxford, United Kingdom OX3
OBP, Tel: 01865 483 760, Fax: 01865 483 937, e-mail:
<skbearder@brooks.ac.uk>.
PRIMAT E SOCIET IES
AMERICAN SOCIETY OF PRIMATOLOGISTS 25 TH ANNUAL
MEETING
T he ASP will host its 25 th annual meeting, 1– 4 June, 2002,
in Oklahoma City, OK. T he meeting will be co-hosted by the
University of Oklahoma and the Oklahoma City Zoo. Prior
to the ASP meeting, the zoo will host meetings of several
of the American Zoological Association’s Primate Taxon
Advisory Groups (TAGs), and the Bushmeat Crisis Task
Force will conduct a special primate bushmeat awareness
session. A schedule of events includes: 28–31 May, Prosimian,
New World Monkey and Old World Monkey TAG meetings;
1 June (am), Bushmeat Crisis Task Force Presentation; 1 June
(pm), ASP welcome reception; 2– 4 June, American Society
of Primatologists’ general sessions and poster presentations;
4 June (pm), ASP closing banquet; 5– 6 June, ASP Education
Committee’s teachers workshop.
For program committee contact: Tammie Bettinger, Chair,
ASP Program Committee, Zoo Atlanta, 800 Cherokee
Avenue SE, Atlanta, Georgia 30315, USA, e-mail:
<tbettinger@zooatlanta.org>. For local arrangements contact:
Janette Wallis, Department of Psychiatry and Behavioral
Sciences, University of Oklahoma, HSC, P.O. Box 26901,
Oklahoma City, OK, 73190, USA, e-mail: <janettewallis@ouhsc.edu>.
2002 ASP CALL FOR AWARD NOMINATIONS
GRANT APPLICATIONS
AND
T he American Society of Primatologists is now seeking
nominations for Conservation Awards and Grants to
recognize colleagues and students working on conservation
related issues. T he awards and grants include: Subscription
Award, Conservation Award and Conservation Small Grants.
All nominations must be submitted by 19 April, 2002 to:
the ASP Conservation Committee Chair: Randall C. Kyes,
Regional Primate Research Center, University of Washington,
Box 357330, Seattle, WA 98195, USA.
T he Subscription Award gives the American Journal of
Primatology to individuals in habitat countries, usually for
a five-year period. Preference is given to those who will
make the journal available for other students or colleagues
to use. Recipients are requested to submit a brief report
every two years summarizing their use of the journal. A
nominating letter should describe the nominee’s credentials,
his/her primate related activities, and should explain why the
nominee deserves to receive priority consideration.
T he Conservation Award provides $750 of financial support
to students from habitat countries that demonstrate potential
for making significant and continuing contributions to
primate conservation. Eligible candidates include students,
researchers and educators from habitat countries who have
not been out of university for more than five years.
Nominators should provide the name, title and full mailing
address of the nominee, along with a statement about
the nominee’s qualifications and a copy of the nominee’s
curriculum vitae. Supporting letters from other colleagues
may be included.
Conservation Small Grants are solicited for conservation
research or related projects, including conservation education.
Small grants are given in amounts up to $1500. Grant
applications can be obtained from the ASP Conservation
Committee Chair Randall C. Kyes, Regional Primate
Research Center, University of Washington, Box 357330,
Seattle, WA 98195, USA, or from the ASP web site at:
<www.asp.org>. Recipients of grants must submit a brief
single-spaced 1-page report for publication in the ASP
Bulletin within six months of completion of the project.
AMERICAN SOCIETY OF PRIMATOLOGISTS’ B OOK
SERIES, SPECIAL TOPICS IN PRIMATOLOG Y
Volume 2 in the American Society of Primatologists’
book series, Special Topics in Primatology, Editor Janette
Wallis, has been published. The Care and Management of
Captive Chimpanzees was edited by Linda Brent, 2001.
ISBN 0-9658301-1-X (paperback). Price: $25.00 + shipping
(US$4.00, outside of US - $9.00, priority mail). T he
publication is a valuable resource for zoos, laboratories and
sanctuaries. It covers topics such as health care, contraceptives,
regulations, training, and forming and managing social
groups. Chapters include: Foreword - F. B. M. de Waal;
Preface - L. Brent; A brief history of captive chimpanzees
in the United States - L. Brent; What does a chimpanzee
need? Using behavior to guide the care and management of
captive populations – J. D. E. Pruetz & W. C. McGrew;
Chimpanzee facility design – J. C. Coe, R. Fulk & L. Brent;
Chimpanzee medicine and health care program - D. R.
Lee & F. A. Guhad; Reproductive management of captive
chimpanzees: Contraceptive decisions – T. L. Bettinger &
K. E. DeMatteo; Behavior and environmental enrichment
of individually housed chimpanzees – L. Brent; Captive
chimpanzee social group formation - J. Fritz & S. Howell;
Social management of captive chimpanzees – M. A.
Bloomsmith & K. C. Baker; Training and cooperative
behaviors and enrichment - G. Laule & M. Whittaker;
133
Neotropical Primates 9(3), December 2001
How much will it cost to keep our chimpanzees?- B. Dyke;
Laws, policies, and guidelines on the care and use of
captive chimpanzees in the United States – S. W. Blangero &
J. L. Vandeberg. Available from: Steve Schapiro, ASP
Treasurer, American Society of Primatologists, UT MD
Anderson Science Park, Rt 2, Box 151-B1 Bastrop, T X
78602, USA, Tel: (512)-321-3991, Fax: (512)-332-5208,
e-mail: <schapir@mdanderson.org>. Payment must be in US
funds and checks should be made payable to “American
Society of Primatologists”. All profits from the sale of the
book will go to the American Society of Primatologists’
Conservation Fund.
ASP CALL
FOR
AWARD NOMINATIONS
T he awards and recognition committee of the American
Society of Primatologists encourages members to nominate
fellow primatologists for T he Distinguished Service Award
and T he Senior Research Award. Nominations must be
received by 15 March, 2002. For further information
please see the ASP web site: <http://www.asp.org/awards> or
contact: Gabriele R. Lubach, Chair, Awards and Recognition
Committee, Harlow Primate Laboratory, University of
Wisconsin, 22 North Charter St., Madison, WI 52715,
USA, Tel: (608) 263-3533, Fax: (608) 262-6020, e-mail:
<lubach@primate.wisc.edu>.
ASP E DUCATION C OMMITTEE H ONORS STUDENTS
At the 2001 American Society
of Primatologists meeting held in
Savannah, Georgia, the Education
Committee honored three student
presentations. T his year a team of
judges including, Siân Evans, Sue
Howell, Nancy Klepper-Kilgore,
Lynne Miller, Leanne Nash, Jaine
Perlman and Coleen Schaffner,
Corina Ross
reviewed 22 papers and 17 posters.
T he three winning presentations
were: Outstanding Paper Presentation: A concept of value in
brown capuchin monkeys (Cebus
apella ), by Sarah Brosan and
Frans de Waal; Outstanding Poster
Presentation: Genetic mosaics
across tissues in callitrichids
(Callithrix kuhlii, black-tufted ear
marmosets), by Corina Ross,
G. Orti and J. A. French; and
Honorable Mention for an
Sarah Brosnan
Outstanding Presentation: Immigration patterns and group stability in wild golden-headed
lion tamarins in southern Bahia, Brazil, by Becky Raboy and
James Dietz. Congratulations to the winners!
RECENT PUBLICAT IONS
NOVA REVISTA CIENTÍFICA DA UNIVERSIDADE
FEDERAL DE MINAS GERAIS, B ELO H ORIZONTE ,
BRASIL
A Lundiana está sendo relançada, não como uma revista de
zoologia, mas como uma revista de Biodiversidade, propondose a publicar artigos nas áreas de Biogeografia, Conservação,
Ecologia, Evolução e Taxonomia, com ênfase na biota
neotropical. O Comitê para Coleções Taxonômicas (CCT )
do Instituto de Ciências Biológicas (ICB) da Universidade
Federal de Minas Gerais (UFMG) está resgatando a revista,
originalmente uma publicação do Departamento de Zoologia
do ICB-UFMG, e que teve apenas dois números editados,
no início da década de 1980. A revista deverá ser publicada
semestralmente (janeiro e julho). O primeiro número dessa
nova fâse da revista será publicado em janeiro de 2002, e o
proximo em julho de 2002. Instruções para os autores podem
ser encontradas no sítio <www.icb.ufmg.br/~lundiana>.
A revista tem como editores os professores Alan L. de
Melo (Departamento de Parasitologia - Editor-chefe), Jaime
A. Bertoluci (Departamento de Zoologia - editor de área,
Zoologia), Julio A. Lombardi (Departamento de Botânica,
editor de área, Botânica) e Carlos A. Rosa (Departamento
de Microbiologia - editor de área, Microbiologia). O CCT
está empenhado em produzir uma revista de alta qualidade
científica e gráfica, e pede a colaboração de toda a comunidade
científica através da submissão de manuscritos e divulgação
da revista junto aos pares de outras instituições. Os artigos
deverão ser preferencialmente em inglês, mas, no primeiro
momento, serão aceitos, também, artigos em português e
espanhol.
Eneida Eskinazi Sant´Anna, Assessora para Projetos,
Comitê para Coleções Taxonômicas (CCT ), Instituto
de Ciências Biológicas, Universidade Federal de Minas
Gerais Avenida Antônio Carlos 6627, Caixa Postal 486,
31270-901 Belo Horizonte, Minas Gerais, Brazil. E-mail:
<cct@mono.icb.ufmg.br>.
T HE FUTURE
OF
EVOLUTION
Volume 98 of 8 May 2001 of the Proceedings of the National
Academy of Sciences includes a series of papers presented
at a National Academy of Sciences Colloquium - “T he
Future of Evolution” held 16–20 March, 2000 at the Arnold
and Mabel Beckman Center in Irvine California. It was
organized by Norman Myers, of Green College, Oxford
University, who with Andrew Knoll (Harvard University)
wrote the first, overview paper on the effect of the extinction
crisis on the future of the evolution of the planet’s biota.
Myers and Knoll give an eloquent and dramatic summary
of the biotic crisis that they, and the other authors, argue
cogently will disrupt and deplete certain basic processes
134
of evolution, with consequences likely to persist for millions
of years. T he “first order effects” include 1) a major
extinction of species estimated to remove one-third to
two-thirds of all species; 2) a mega-mass extinction of
populations; 3) alien invasions and mixings of biota; 4)
progressive depletion and homogenization with potential
threshold effects on ecosystems; 5) general biotic
impoverishment and a decline in global biomass; and 6)
gross reduction and virtual elimination of entire sectors
of some biomes, notably tropical forests, coral reefs and
wetlands which have served as centers for diversification in
the past. Further evolutionary effects they discuss include:
1) fragmentation of species ranges with disruption of gene
flow; 2) decline in effective population sizes with depletion
in gene reservoirs; and 3) biotic interchanges introducing
species and even entire biotas into new areas, with multiple
founder effects and novel competitive and other ecological
interactions. T he consequences they consider include an
outburst of speciation, proliferation of opportunistic species
(“pest and weed” ecology), depletion of evolutionary
powerhouses; decline in biodisparity (the biota’s manifest
morphological and physiological variety), an end to
speciation in large vertebrates, and emergent, difficult to
predict novelties.
Papers: T he biotic crisis and the future of evolution –
N. Myers & A. H. Knoll, pp.5389-5392; Lessons from the
past: Evolutionary impacts of mass extinction – D. Jablonski,
pp.5393-5398; Lessons from the past: Biotic recoveries from
mass extinctions – D. H. Erwin, pp.5399–5403; Loss of
speciation rate will impoverish future diversity – M. L.
Rosenzweig, pp.5404–5410; What was natural in the coastal
oceans? – J. B. C. Jackson, pp.5411–5418; T he future
of coral reefs – N. Knowlton, pp.5419–5425; Disrupting
evolutionary processes: T he effect of habitat fragmentation
on collared lizards in the Missouri Ozarks – A. R. Templeton,
R. J. Robertson, J. Brisson, & J. Strasburg, pp.5426–5432;
Human-caused environmental change: Impacts on plant
diversity and evolution – D. Tilman & C. Lehman,
pp.5433–5440; Plant biology in the future - F. A. Bazzaz,
pp.5441–5445; T he evolutionary impact of invasive species
- H. A. Mooney & E. E. Cleland, pp.5446–5451; Rapid
plant diversification: Planning for an evolutionary future R. M. Cowling & R. L. Pressey, pp.5452–5457; Humanmodified ecosystems and future evolution – D. Western,
pp.5458–5465; T he current biodiversity extinction event:
Scenarios for mitigation and recovery – M. J. Novacek &
E. E. Cleland, pp.5466–5470; Decline of biomes and biotas
and the future of evolution – D. S. Woodruff, pp.5471–5476;
Intervening in evolution: Ethics and actions – P. R. Ehrlich,
pp.5477–5480.
Papers from the National Academy of Sciences Colloquium
on T he Future of Evolution are available for download
at
<http://www.pnas.org/content/vol98/issue10/>.
For
subscription information see: <http://www.pnas.org/
subscriptions/> or contact: the PNAS Circulation Office
USA phone: 1-202-334-2672, fax 1-202-334-2738 or e-mail:
subspnas@nas.edu.
Neotropical Primates 9(3), December 2001
SPECIAL ISSUE
OF
TREE - SPECIATION
A special issue of Trends in Ecology and Evolution, Vol. 16(7),
July 2001, Editor Catriona J. MacCallum, is dedicated to
“Speciation”. T he Guest Editor was Nicholas J. Barton,
Institute of Cell, Animal and Population Biology of the
University of Edinburgh, UK. T he special issue aims to review
recent developments and to bring together all aspects of
speciation, from genetics through ecology to palaeontology.
Of particular interest for conservation is the first article
by Jody Hey, Rutgers University, NJ, who discusses the
confusion about exactly what a species is, arising from
conflict between intuitive classification and the complex
and continuous process of evolution. In his Introduction
(p.325), Barton rationalizes some of the subsequent series
of articles in the form of questions: “Why should there be
distinct ‘species’ at all rather than a continuous intergradation
of interbreeding organisms that reflects the continuity of
evolution (Turelli et al.)? Is the distribution of species’
abundance determined primarily by the distribution of
ecological niches, or does it also depend on how species form
(Godfray & Lawton)? To what extent does genetic exchange
impede divergence? In the extreme, can a single population
split into two species without any spatial separation at
all (Turelli et al., Via, and Riesenberg)? What processes
drive divergence - random drift, natural selection, or sexual
selection (Panhuis et al. and Schluter)? What kinds of genetic
differences distinguish species, and what do these tell us
about the process of divergence (Turelli et al. and Orr).”
Further aspects treated include the role of selection as a
cause of divergence (Panhuis et al. and Schluter), the use of
molecular markers (Orr), the use of phylogenies for rigorous
comparative tests and inferences about the evolutionary
process (Barraclough & Nee), the use of “gene trees” to
measure evolutionary processes of selection, migration and
drift that are involved in speciation (Nichols), and how
palaeontology has allowed clear hypotheses about the relation
between speciation and morphological evolution (Benton &
Pearson).
Papers: T he mind of the species problem - J. Hey, pp.326–329;
T heory and Speciation - M. Turelli, N. H. Barton & J. A.
Coyne, pp.330–343; T he genetics of species differences H. A. Orr, pp.343–350; Chromosomal rearrangements and
speciation - L. H. Riesenberg, pp.351–358; Gene trees and
species trees are not the same - R. Nichols, pp.358–364;
Sexual selection and speciation - T. M. Panhuis, R. Butlin,
M. Zuk & T. Treganza, pp.364–371; Ecology and the origin
of species - D. Schluter, pp.372–380; Sympatric speciation in
animals: T he ugly duckling grows up - S. Via, pp.381–390;
Phylogenetics and speciation - T. G. Barraclough & S. Nee,
pp.391–399; Scale and species numbers - H. C. J. Godfray
& J. H. Lawton, pp.400– 404; Speciation in the fossil record
- M. J. Benton & P. N. Pearson, pp.405– 411. T here is also
a pertinent review of Frogs, Flies and Dandelions: The Making
of Species by Menno Schilthuizen, Oxford University Press,
Oxford, 2001, along with a glossary of speciation.
Neotropical Primates 9(3), December 2001
T HE RED L IST CATEGORIES AND C RITERIA BOOKLET
T he Red List Categories and Criteria booklet (in English,
French and Spanish) is now available on the SSC website in
pdf: <http://www.iucn.org/themes/ssc/redlists/RLcategories
2000.html>. T his is the only version that should be used
and distributed. T he previous version in Word had an error
in the citation. T he correct citation is: IUCN. (2001).
IUCN Red List Categories and Criteria: Version 3.1 . IUCN
Species Survival Commission. IUCN, Gland, Switzerland
and Cambridge, UK. ii+30 pp.
B OOKS
A Primatologia no Brasil – 7 , edited by Carmen Alonso
and Alfredo Langguth, 2000, 360pp. Editora Universitária,
Universidade Federal da Paraíba, Sociedade Brasileira de
Primatologia, João Pessoa, Paraíba. Anais do VIII Congresso
Brasileiro de Primatologia, João Pessoa, 10–15 de agosto
de 1997. Proceedings of the VIII Brazilian Primatology
Congress. T he publication of this book was supported by
the Margot Marsh Biodiversity Foundation. It contains 23
articles in Portuguese and English on the behavior, ecology
and physiology of Brazilian (and one Colombian) primates.
Contents: Comparação do cuidado de uma prole de gêmeos
com uma prole de filhote único de Callithrix jacchus no
ambiente natural - F. S. Albuquerque, E. Otta & M. de
F. Arruda, pp.11–21; Social interactions in a Callithrix
kuhlii family (Primates: Callitrichidae) in captivity - C.
Alonso, S. Porfírio & A. Langguth, pp.23 –33; Uso do
espaço e comportamento social em sagüis do cerrado
(Callithrix penicillata ) selvagens, no Centro de Primatologia
da Universidade de Brasília - V. Boere, L. Tillman, M. C.
de Resende & C. Tomaz, pp.35– 48; Distribuição diária da
atividade locomotora e da cataçao em uma fêmea reprodutora
de Callithrix jacchus durante a gestação e após o parto C. S. Camillo et al., pp.49– 63; Influência da distribuição
e disponibilidade dos frutos, na dieta e uso do espaço em
sagüi-do-nordeste (Callithrix jacchus) - C. S. S. de Castro, A.
Araújo, C. Alho & M. M. Dias Filho, pp.65–80; Ecologia
alimentar e sazonalidade em primatas neotropicais: Gênero
Saguinus - S. Egler, pp.81–95; A comparative study of hand
preference in three species of the genus Cebus - S. F. Ferrari, T.
W. R. Lobato & M. S. Andrade, pp.97–105; Mães, filhotes
e uma análise dos custos do cuidado parental - R. F. Guerra,
pp.107–149; Aspectos ecológicos e do comportamento de
Alouatta fusca (Geoffroy, 1812) na Estação Ecológica de
Aracuri, RS, Brasil - M. M. de A. Jardim & L. F. B. de
Oliveira, pp.151–169; Behaviour of free-ranging squirrel
monkeys Saimiri sciureus, (Platyrrhini: Cebidae) at the
fazenda Monte Verde, Peixe-Boi, Pará - E. M. Lima, A.
L. C. B. Pina & S. F. Ferrari, pp.171–180; Uso do
espaço por um grupo de Alouatta fusca clamitans em um
fragmento degradado de floresta Atlântica - V. L. A. G.
Limeira, pp.181–196; Evolutionary history of the duplicated
135
gamma hemoglobin genes in New World monkeys (Primates:
Atelinae) – C. M. Meireles, J. Czelusniak, M. P. C. Schneider
& M. Goodman, pp.197–214; Emissão de gritos longos
por grupos de Callicebus nigrifrons e suas reações a playbacks
- F. R. de Melo & S. L. Mendes, pp.215–222; Sex and
age differences in foraging and vigilance behavior of captive
Saguinus midas midas (Primates: Callitrichidae) - A. C. de
A. Moura & C. Alonso, pp.223–238; Influência de filhotes
dependentes no padrão de atividades de um grupo silvestre de
Callithrix jacchus - M. C. L. Nascimento & M. de F. Arruda,
pp.239–246; Percepção de cores em Cebus apella (Primates:
Cebidae) - V. F. Pessoa et al., pp.247–264; Comunicación
vocal y su relación con las actividades, estructura social
y contexto comportamental en Callicebus cupreus ornatus
- M. Porras, pp.265–274; Aspectos de comportamento
social de Saguinus midas midas (Primates: Callitrichidae) em
cativeiro - N. Schiel & A. Souto, pp.275–289; Resultados de
uma pequena expedição primatológica à Amazônia Central
(Primates: Playtrrhini) - J. de S. e Silva Júnior & M. de A.
Noronha, pp.291–304; Consistência no uso das mãos em
atividades forçadas e espontâneas no sagüi, Callithrix jacchus
- M. B. C. de Sousa, N. S. Xavier & H. A. P. Peregrino,
pp.305–317; Influência da variação diurna no sangue e do
estresse na excreção fecal de esteróides em Callithrix jacchus
- M. B. C .de Sousa & T. Ziegler, pp.319–331; Memória
operacional no macaco-prego (Cebus apella ) - C. Tomaz, M.
C. H. Tavares & A. L. R. Caldas, pp.333 –347: A questão do
gênero na produção científica em Primatologia no Brasil - M.
E. Yamamoto & K. S. da Silva Diniz, pp.349–360. Available
from: Alfredo Langguth, Departamento de Sistemática e
Ecologia CCEN, Universidade Federal da Paraíba, 58059-900
João Pessoa, Paraíba, Brazil. E-mail: <alfredo@dse.ufpb.br>.
Biodiversidade na Amazônia Brasileira: Avaliação e Ações
Prioritárias para a Conservação, Uso Sustentável e Repartição de
Benefícios, edited by Adalberto Vérissimo, Adriana Moreira,
Donald Sawyer, Iza dos Santos, Luis Paulo Pinto and João
Paulo Capobianco, 2001, 540pp. In Portuguese. Published
by the Instituto Socioambiental and Estação Liberdade, São
Paulo, Brazil. ISBN 85 7448 052 5 (Estação Liberdade), 85
85994 13 4 (Instituto Socioambiental). T his is a remarkable
compilation of articles, facts, figures and maps on diverse
aspects of the Brazilian Amazon: its biodiversity, socioeconomy, conservation, development, and destruction. T he
first part provides valuable overviews of its biodiversity. Maria
Nazareth F. da Silva et al. give an overview of mammals.
T hey listed 311 mammal species as occurring in the Brazilian
Amazon – 22 marsupials, 11 edentates, 124 bats, 57 primates,
16 carnivores, two cetaceans, one sirenian, 72 rodents and
one rabbit. T his book is the result of the priority setting
workshop, held in Macapá, Amapá, 20–25 September, 1999
- “Projeto Avaliação e Identificação de Ações Prioritárias
para a Conservação, Utilização Sustentável e Repartição dos
Benefícios da Biodiversidade da Amazônia Brasileira”, part
of the activities of the Programa Nacional de Diversidade
Biológica - PRONABIO of the Ministry of the Environment.
Key organizations involved in coordinating the workshop
were: Instituto Socioambiental – ISA (João Paulo Capobianco,
136
Adriano Ramos & Geraldo Andrello), Instituto do Homem
e Meio Ambiente da Amazônia – IMAZON (Adalberto
Veríssimo & Eugênio Arima), Instituto de Pesquisa Ambiental
da Amazônia – IPAM (Adriana Moreira & Paulo Moutinho),
Conservation International do Brasil (Luiz Paulo Pinto &
Roberto Cavalcanti) and Instituto Sociedade, População e
Natureza – ISPN (Donald Sawyer & Maurício Pontes).
Contents: Part 1 - Biodiversidade e funções ecológicas
dos ecossistemas: O peso dos invertebrados na balança
de conservação biológica da Amazonia – W. L. Overal,
pp.50 –59; Componente biota aquática – R. Barthem,
pp.60 –78; Relatório técnico sobre a diversidade de
anfíbios na Amazônia brasileira – C. Azevedo-Ramos &
U. Galatti, pp.79–88; Biodiversidade de répteis do bioma
floresta amazônica e ações prioritárias para sua conservação
– R. C. Vogt, G. M. Moreira & A. C. de O. C. Duarte,
pp.89–96; Biogeografia e conservação de aves na região
amazônica – D. C. Oren, pp.97–109; Biogeografia e
conservação da mastofauna na floresta amazônica brasileira
– M. N. F. da Silva, A. B. Rylands & J. L. Patton, pp.
110 –131; Área botânica – B. W. Nelson & A. A. de Oliveira,
pp.132–176; As funções ecológicas dos ecossistemas florestais:
implicações para a conservação e uso da biodiversidade
amazônica – P. Moutinho & D. Nepstad, pp.177–183.
Part 2 – Sociodiversidade e etnoconhecimento: Populações
tradicionais e conservação ambiental – M. C. da Cunha &
M. W. B. Almeida, pp.184 –193; A sociodiversidade
nativa contemporânea no Brasil e a biodiversidade na
Amazônia – B. Ricardo, pp.194 –204; “Populações
tradicionais” e biodiversidade na Amazônia: levantamento
bibliográfico – A. C. Diegues. G. Andrello & M. Nunes,
pp.205–224; Elementos de discussão sobre a conservação
da agrobiodiversidade: o exemplo da mandioca (Manihot
esculenta Crant) na Amazônia brasileira – L. Emperaire,
pp.225–234; Biodiversidade e conhecimentos tradicionais –
J. Santilli, pp.235–245. Part 3 – Unidades de Conservação
e terra indígenas: Unidades de Conservaão na Amazônia
Legal – F. Ricardo & J. P. R. Capobianco, pp.246–250; Terra
indígenas na Amazônia Legal – F. Ricardo, pp.251–258;
Sobreposições entre Unidades de Conservação (UCs)
federais, estaduais, terra indígenas, terras militares e reservas
garimpeiras na Amazônia Legal – F. Ricardo, pp.259–262;
Representatividade das Unidades de Conservação e terras
indígenas em relação à fitofisionomias da Amazônia Legal
– J. P. R. Capobianco, pp.263–267; Identificação de áreas
prioritárias para a conservação de biodiversidade por meio
de representatividade das Unidades de Conservação e tipos
de vegetação nas ecorregiões da Amazônia brasileira – L. V.
Ferreira, R. Lemos de Sá, R. Buschbacher, G. Batmanian, J.
M. C. da Silva, M. B. Arruda, E. Moretti, L. F. S. N. de
Sá, J. Falcomer & M. I. Bampi – pp.268–286; Incidência
de requerimentos e titulos minerários nas Unidades de
Conservação (UCs) federais e estaduais na Amazônia Legal
– F. Ricardo, pp.287–289; Reservas indígenas de recursos
naturais – M. Santilli, pp.290 –291; Formas de acesso à
terra e a preservação da floresta amazônica: uma análise
jurídica da regularização fundiária das terras dos quilombolas
e seringueiros – J. H. Benatti, pp.292–298; Presenca
humana em Unidade de Conservação: um impasse científico,
Neotropical Primates 9(3), December 2001
jurídico ou político? – J. H. Benatti, pp.299–305. Part 4.
Socieconomia e pressões antrópicas: Diagnóstico demográfico,
socioeconômico e de pressão antrópica na região da Amazônia
Legal – M. P. Monteiro & D. Sawyer, pp.308–320; Eixos
amazônicos de integração e desenvolvimento – obras e
empreendimentos – M. Brito, pp.321–326; O diagnóstico do
uso da terra na Amazônia: exploração madeireira, agricultura
e agropecuária – A. Veríssimo, E. Arima & E. Lima,
pp.327–337; Espécies de árvores potencialmente ameaçadas
pela atividade madeireira na Amazônia – A. Martini, N. de
A. Rosa & C. Uhl, pp.338–347; Oportunidades de negócios
na Amazônia: alternatives sustentáveis – A. Guimarães,
pp.348–351. T he remaining sections include workshop
methodology, texts, maps, tables and details of the base
maps used, the numerous priority area maps for the different
themes, and the final priority areas selected during the
workshop. Available from: Instituto Socioambiental, Av.
Higienópolis 901, 01238-001 São Paulo, São Paulo, Brasil,
Tel: +55 11 3825 5544, Fax: +55 11 3825 7861, e-mail:
<isa@socioambiental.org>. Web site: <www.socioambiental.
org>.
Biology, Medicine, and Surgery of South American Wild
Mammals, edited by Murray E. Fowler and Zalmir S. Cubas,
2001, 536pp. Iowa State University Press, Ames, Iowa.
ISBN 0 8138 2846-5. Price US$89.65. A compilation of
continent specific coverage of amphibians, birds, reptiles and
all South American mammals arranged by order and genus.
Topics include conservation efforts, diseases in free-ranging
populations, and management of animals in captivity. Special
coverage is given to general health topics such as nutrition,
ophthalmology and dentistry. Pages 256 to 278 are dedicated
to the New World primates, with the following contributions:
Biology of the Cebidae - Anthony B. Rylands, pp.256–259;
Biology and conservation of the Callitrichidae – Cláudio
Valladares-Padua, pp.259–261; Nutrition - Roberto da
Rocha e Silva, pp.261–263; Behavior and environmental
enrichment - Vanner Boere, pp.263 –267; Medicine - José
Luiz Catão Dias, pp.267–272; Medicine, selected disorders
- Alcides Pissinatti, pp.272–274; Reproduction - Marcelo A.
de B. V. Guimarães, pp.274 –278. An excellent compendium
and difficult to believe that any zoo or breeding institution
could do without it. Available from: Iowa State University
Press, 212 South State Avenue, Ames, IA 50014, USA, Tel:
800 862 6657, 515 292 0155, Fax: 515-292-3348. Web
site:<www.isupress.com>.
Songs, Roars, and Rituals: Communication in Birds, Mammals,
and Other Animals, by Lesley J. Rogers and Gisela Kaplan,
Harvard University Press 2000. Price: $31.50, ISBN: 0-67400058-7. T he authors have highlighted many of the latest
developments in the study of animal communication,
offering insights on how animals communicate by sight,
sound, smell, touch and electrical signaling. T hey explore
a wide variety of communication patterns and how these
patterns evolved, including an account of the science of
animal communication and modern concepts, controversies
and the evolution of human language and the use of symbolic
language by apes. Available from: Harvard University Press,
137
Neotropical Primates 9(3), December 2001
Customer Service Department, 79 Garden Street, Cambridge,
Massachusetts 02138 USA, Fax: (800) 962-4983, phone:
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Colbert’s Evolution of the Vertebrates: A History of the
Backboned Animals Through Time, Fifth Edition, by Edwin H.
Colbert, Michael Morales and Eli C. Minkoff, WILEY-LISS
2001. Price: $145.00 (hardbound), ISBN: 0-471-38461-5.
A valuable reference for professionals in evolutionary biology
and paleontology, as well as students in those fields. From
the back cover: “Vertebrate evolution is studied through
comparative anatomy and functional morphology of existing
vertebrates as well as fossil records. Since the publication of
the previous edition of Colbert’s Evolution of the Vertebrates:
A History of the Backboned Animals T hrough Time, there
have been significant advances in the knowledge surrounding
backboned animals. T his latest edition of the classic text is
completely revised to offer the most recent discoveries in this
continually evolving field of science. Covering the various
aspects of vertebrate life, from skeletal system to ecology,
behavior, and physiology, the Fifth Edition includes new
sections on conodonts, dinosaurs, primates, and the origin of
birds, and discusses: Analysis of morphological and molecular
data; early diversification of vertebrates; the evolution of
dinosaurs; the origin of mammals; early ruling reptiles;
and basic adaptation of ungulates”. Chapter twenty-three:
Primates and T heir Kin, covers: T he Archonta, Scandentia,
T he Bats, Dermoptera, T he Origin of the Primates, Primate
Characters, A Classification of the Primates, Plesiadapiformes,
Strepsirhini - T he Adapids, Lemurs, and Lorises, Haplorhini,
T he Tarsioids, Platyrrhini - T he New World Monkeys,
Catarrhini - T he Old World Monkeys, Apes, and Humans
and T he Family Hominidae. Available from: John Wiley &
Sons, Inc., Distribution Center, 1 Wiley Drive, Somerset, NJ
08875-1272, phone: (732) 469-4400 or (800) 225-5945,
Fax: (732) 302-2300, e-mail: <bookinfo@wiley.com>.
Animal, The Definitive Visual Guide to the World’s Wildlife,
edited by Don E. Wilson and David Burnie, 2001, 624pp.,
DK Publishing, ISBN: 0-789-47764-5, over 4000 color
photos and color illustrations. Price: £30.00. Researched
by over 70 zoologists and naturalists this book covers
over 2000 mammals, birds, amphibians, reptiles, fish and
invertebrates. Principle consultants include: Juliet CluttonBrock (Mammals) - Dr Francois Vuilleumier (Birds) Richard Rosenblatt (Fish) - Chris Mattison (Reptiles) - Tim
Halliday (Amphibians) - George McGavin (Arthropods) Richard Barnes (Non-Arthropod Invertebrates). Available
from: NHBS Mailorder bookstore, 2-3 Wills Road, Totnes,
Devon, TQ9 5XN, UK, web site: <http://www.nhbs.com>.
NHBS Stock Code: #119919W hardback.
Economics in Nature: Social Dilemmas, Mate Choice and
Biological Markets, edited by Ronald Noe, Jan van Hooff
and Peter Hammerstein, 2001. Published by Cambridge
University Press, ISBN: 0-521-65014-3 (hardbound). Price:
$80.00. From the back cover:
Since the development of game theory, the analysis of animal
behaviour using the theories of economics has become a
growing field of biological research in which models of
games and markets play an important role. Studies of
sexual selection, interspecific mutualism and intraspecific
cooperation show that individuals exchange commodities to
their mutual benefit; the exchange values of commodities are
a source of conflict, and behavioural mechanisms such as
partner choice and contest between competitors determines
the composition of trading pairs or groups. T hese ‘biological
markets’ can be examined to gain a better understanding
of the underlying principles of evolutionary ecology. In
this volume scientists from different disciplines combine
insights from economics, evolutionary biology and the
social sciences to look at comparative aspects of economic
behaviour in humans and other animals. Aimed primarily
at evolutionary biologists and anthropologists, it will also
appeal to psychologists and economists interested in an
evolutionary approach. Available from: Cambridge University
Press, 40 West 20 th St., New York, NY 10011-4211, USA.
Phone: (800)-872-4723, Fax: (800)-914-937-4712, web site:
<www.cambridge.org>.
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Wallander, D. L. 1999. Food sharing and the development
of feeding behavior in Saguinus imperator, the emperor
tamarin (family: Callitrichidae). Diss. Abst. Int. A60(6):
2114.
Neotropical Primates 9(3), December 2001
In: Am. J. Phys. Anthropol. Suppl. 32, 2001.
Barnett, A. A. and Ross, C. 2001. T he predictive value of
metachromism in primate taxonomy: A critical analysis
using Neotropical Cebidae, p.35.
Bezanson, M. F., Garber, P. A. and DeLuycker, A. M. Patterns
of subgrouping and spatial affiliation in a community of
mantled howling monkeys (Alouatta palliata ), pp.39– 40.
Bicca-Marques, J. C. and Garber, P. A. Cognitive ecology
and within-patch foraging decisions in tamarins, p.40.
Campbell, C. J. Copulatory behavior of free-ranging blackhanded spider monkeys (Ateles geoffroyi), p.47.
Clarke, M. R. and Glander, K. E. Presence of mother
and juvenile dispersal in free-ranging howling monkeys
(Alouatta palliata ) in the tropical dry forest of Costa Rica,
p.50.
Cole, T. M., III. Phylogenetic analysis of landmark data and
the evolution of ateline skull form, p.52.
Cunningham, E. P. and Janson, C. H. Effect of small home
range size on use of memory, p.56.
Davis, L. C. and Ford, S. M. Forelimb anatomy and foraging
strategy in Leontopithecus rosalia , p.57.
DeLeon, V. B., Frohlich, B., Garafolo, E. and Ruff,
C. B. Crushing seeds and gouging tress: T he impact on
mandibular and zygomatic arch strengths, p.58.
Difiore, A. Ranging behavior and foraging ecology of lowland
woolly monkeys (Lagothrix lagothrica ), p.59.
Duren, D. L. Metaphyseal angular morphology and primate
locomotion, p.61.
Garber, P. A, and Leigh, S. R. Scaling and size reduction in
tamarins, p.68.
Henry, R. E. and Winkler, L. Foraging, feeding and
defecation site selection as a parasite avoidance strategy of
Alouatta palliata in a dry tropical forest, p.79.
Huntington, C. and Fernandez-Duque, E. Natal dispersal in
the monogamous owl monkey, (Aotus azarai) of Formosa,
Argentina, pp.83–84.
Norconk, M. A. and Conklin-Brittain, N. L. Methods for
assessing nutrient intake in wild primates: Temporal- vs.
weight-based estimates, pp.113–114.
Panger, M., Perry, S., Rose, L., Gros-Louis, J., Vogel, E.,
MacKinnon, K. and Baker, M. Food processing technique
differences across three capuchin (Cebus capucinus)
populations in Costa Rica, p.117.
Pucciarelli, H. M., Mune, M. C., Orden, A. B., Oyhenart,
E. E., Villanueva. M. E., Rodriguez, R. R. and Pons,
E. R. Growth velocity of bone variables and indices in the
squirrel monkey (Saimiri sciureus boliviensis). A longitudinal
experiment, pp.121–122.
Richmond, B. G. and Strait, D. S. Knuckle-walking and the
midcarpal joint, p.126.
Runestad Connour, J. A. and Glander, K. E. Description of
a feral Alouatta palliata population observed during three
decades, pp.128–129.
Suarez, S. A. Quantifying fission-fusion behavior and social
dynamics in free-ranging spider monkeys (Ateles belzebuth
belzebuth), pp.145–146.
Swartz, D. Gradient phenomena in primates and the
intermembral index, p.146
141
Toloczko, D. M. Love potions in primate brains? p.150.
Videan, E. N. Daytime resting-site selection in mantled
howling monkeys (Alouatta palliata ): Relative influences of
feeding and comfort, p.155.
Vinyard, P. S. Variance dimorphism in the postcrania of
hominoids and several monkeys, pp.156 –157.
Walker, S. E. and Ford S. M. Evolution of behavioral and
ecological variables in the Pitheciinae, p.158.
Winkler, L., Zhang, X. and Ferrell, R. Intergroup differences,
troop immigration, and genetic variation in mantled
howling monkeys in Nicaragua, p.166.
Wright, B. W. Fruit tissue toughness as a determinant of
masticatory “robusticity” and food utilization: A study of
primates in central Guyana, p.167.
Wright, K. A. A comparison of the locomotor behavior and
habitat use of Cebus olivaceus and Cebus apella in Guyana,
p.167.
In: Folia Primatologica, 72(3) 2001. Selected abstracts
of the scientific meetings of La Société Francophone de
Primatologie, The Italian Primatological Society and The
German Primate Society.
12 th Annual Meeting of La Société Francophone de Primatologie,
Besancon, September 27–29, 20000
Di Trani, C. M. P. T he primate model in zooanthropology:
Didactic examples at the Mulhouse Zoo, p.117.
Dubreuil, G. and Dormont, D. Prions and non-human
primates, p.119.
Leroy, E., Bilbaut, M., Gautier, Y., Monchatre, R. and Pellier,
A. A successful treatment of a stress-induced behavioural
disorder in Geoffroy’s tufted-ear marmoset, Callithrix
geoffroyi, at the Reserve Africaine de Sigean, pp.122–123 .
14 th Meeting of the Italian Primatological Society, Pisa-Calci,
October 9–11, 2000
Addessi, E. and Visalberghi, E. Social influences on neophobia
in Cebus apella , p.128–129.
Biagini, L., Bogani, P., Ardito, G. and Buiatti, M. Molecular
methods for variability analysis in primates, p.144.
Carosi, M., Ulland, A. E., Gerald, M. S. and Suomi,
S. J. Male-like external genitalia in female tufted capuchins
(Cebus apella ), and the presence of a clitoral bone
(baubellum): A cross-sectional study, p.149.
Carosi, M., Ulland, A. E. and Suomi, S. J. Urine washing
behaviour in tufted capuchin monkeys (Cebus apella ):
Testing a few hypotheses, p.130.
Dal Secco, V. and Visalberghi, E. Male response to female
proceptivity in tufted capuchin monkeys (Cebus apella ),
pp.130 –131.
de Rosa, C., Vitale, A. and Puopolo, M. Puzzle-feeders
as environmental enrichment in common marmosets
(Callithrix jacchus), p.131.
Gueyras, A., Bernarducci, R. and Vitale, A. Environmental
enrichment during separation in captive common
marmosets (Callithrix jacchus): Behavioural and
physiological aspects, pp.151–152.
142
Riviello, M. C. and Wirz, A. Comparative blood values in
several species of New World monkeys, p.152.
Spinozzi, G. and Cacchiarelli, B. Lateral biases for haptic and
visually guided reaching tasks in tufted capuchin monkeys
(Cebus apella ), p.140.
Truppa, V. and Spinozzi, G. Factors affecting manual
laterality in tufted capuchin monkeys (Cebus apella ) for
food reaching tasks, pp.140–141.
Veracini, C., Galleni, L. and Forti, M. T he concept of species
and the foundations of biology, a case study: T he Callithrix
jacchus group, p.148.
Visalberghi, E. and Moltedo, G. Sexual behaviour of tufted
capuchin monkeys (Cebus apella ): What affects the target?
p.134.
Zanzoni, M., Vitale, A. and Chiarotti, F. Social context
affects the emission of food-calls in common marmosets
(Callithrix jacchus), pp.137–138.
7 th Congress of the German Primate Society, Zurich, September
30–October 4, 2001
Anzenberger, G., Münch, M., Moisson, P. and Petit,
T. Intergeneric marmoset hybrids (Cebuella pygmaea x
Callithrix jacchus): An important case study for callitrichid
taxonomy, p.153.
Anzenberger, G. and Pryce, C. R. Field and laboratory
study of callitrichid behavioural biology: Contradictory or
complementary approaches? p.154.
de Oliveira, M. S. Sexual inhibition and inbreeding
avoidance in captive common marmosets (Callithrix
jacchus), pp.174 –175.
Dettling, A. C., Feldon, J. and Pryce, C. R. Repeated parental
separation and long-term biobehavioural development in
the common marmoset (Callithrix jacchus), p.158.
Hammerschmidt, K. and Fichtel, C. ‘Call pitch’ as an
indicator of the intensity of affective states, p.163.
Heistermann, M. and Hodges, J. K. Non-invasive endocrine
assessment: Methods and applications for monitoring
reproductive status and studying physiological mechanisms
underlying primate behaviour, pp.164 –165.
Hemelrijk, C. K. Society, sexual attraction and male
‘tolerance’ to females: An individual-based model, p.165.
Hernandez Salazar, L. T., Rodriguez-Luna, E. and Laska,
M. Sour-taste tolerance in captive spider monkeys, squirrel
monkeys, and pigtail macaques, pp.165–166.
Heymann, E. W. Phenology and the scarcity of folivory in
New World primates, p.166.
Heymann, E. W. T he role of sleeping habits for malaria
infection rates in Amazonian primates, p.167.
Heymann, E. W. T houghts on the future of primate
behavioural ecology, p.167.
Laska, M. Food preferences and nutrient composition in
squirrel monkeys, spider monkeys and pigtail macaques,
pp.170 –171.
Laska, M., Kohlmann, S., Hernandez Salazar, L. T. and
Rodriguez Luna, E. Gustatory responses to polycose in
four species of non-human primates, pp.171–172.
Müller, A. E. and Soligo, C. Why are primates social?
pp.173 –174.
Neotropical Primates 9(3), December 2001
Plesker, R. A. Dipetalonema gracile infection in a squirrel
monkey, p.177.
Seibt, A. and Laska, M. ‘Microsmatic’ primates revisited:
Olfactory sensitivity in squirrel monkeys and pigtail
macaques, p.183.
Sterling, E. J. Conservation of non-human primates: Making
decisions in the face of uncertainty, pp.184–185.
T hiess, A. and Rothe, H. Analysis of socio-dynamic processes
in large families of semi-free living common marmosets
(Callithrix jacchus), pp.186–187.
T homas, R. M. and Curtis, D. J. A novel software application
for the study of photoperiodic cueing mechanisms
underlying circadian and circannual rhythms and lunarperiodic modulations, p.187.
Wiesemüller, B. and Rothe, H. T he problem of small slope
differences in phylogenetic allometry studies, p.192.
Zingg, J. and Martin, R. D. Temporal pattern of exudate
feeding in pygmy marmosets (Cebuella pygmaea ) in Ecuador,
p.193.
In: American Journal of Primatology, 54(Suppl. 1) 2001.
Program and Abstracts of the Twenty-Fourth Annual
Meeting of The American Society of Primatologists,
hosted by Armstrong Atlantic State University, Savannah
Georgia August 8–11, 2001.
Bach, A., Raboy, B. and Dietz, J. M. Birth seasonality in wild
golden-headed lion tamarins (Leontopithecus chrysomelas)
in Una Reserve, Bahia State, Brazil, p.69.
Baker, M. Variation in ranging patterns and habitat use
by capuchin monkeys (Cebus capucinus) in a dry tropical
forest, p.95.
Bales, K., O’Herron, M., Baker, A. and Dietz, J. M. Sources
of variability in number of births in wild golden lion
tamarins, p.76.
Bales, K., French, J. and Dietz, J. Explaining variation
in maternal care in cooperatively breeding golden lion
tamarins, pp.47– 48.
Bider, L. Paternal care in captive white-faced sakis (Pithecia
pithecia ), p.24.
Brosnan, S. and de Waal, F. A concept of value in brown
capuchin monkeys (Cebus apella ), p.51.
Cancino, L., Layne, D. and Tardif, S. D. Preliminary findings
on the relationship between early infant behavior, mother
peripartum behavior and survival in common marmosets
(Callithrix jacchus), p.90.
Clark, M., Arden, D., Epstein, D. and Gilbert, M. Activity
patterns of adult male howling monkeys (Alouatta palliata )
in the dry forest of Costa Rica: Comparison by age, habitat
and social group, p.28.
Cummins-Sebree, S., Fragaszy, D., Johnson-Pynn, J. and
Hirsh, E. A capuchin’s (Cebus apella ) performance in two
and three dimensional mazes, p.57.
Florence, D. Diseases as confounding variables in research:
Symposium, pp.29–30.
Jack, K. and Fedigan, L. Life history of male white-faced
capuchins (Cebus capucinus), Santa Rosa National Park,
Costa Rica, p.50.
143
Neotropical Primates 9(3), December 2001
Janson, C. Field experiments in primate ecology: T he
monkeys are always right, p.107.
Jardim, M. and Setz, E. Group size changes in free-ranging
howler monkeys (Alouatta guariba clamitans) in southern
Brazil, pp.74–75.
Hankerson, S., Short, K., Bachand, K. and Caine, N.
Vigilance as a function of prior exposure to threat in
Geoffroy’s marmosets, Callithrix geoffroyi, p.35.
Landau, K. Evidence for goal directed foraging patterns in the
mantled howler monkey on Ometepe island, Nicaragua,
p.107.
Leighty, K. and Fragaszy, D. Body-tilting during skilled use
of a joystick, p.49.
Masterson, T. Geographic cranial variation among three
subspecies of Cebus apella , pp.46– 47.
McCann, C., Koontz, F., Williams-Guillen, K. and Espinoza,
A. A. Population and habitat assessment of mantled
howling monkeys (Alouatta palliata ) living on coffee
plantations surrounding Mombacho Volcano Nature
Reserve, Nicaragua, p.79.
Miller, L. Bringing primatology into the classroom:
A workshop for K–12 teachers, pp.26 –27.
Miller, L. Is there life after graduate school? A round-table
discussion on putting together grant proposals and applying
for post-docs, p.27.
Miller, L. and Dietz, J. Effects of intrinsic constraints and
seasonality on energy intake and energy expenditure in wild
golden lion tamarins (Leontopithecus rosalia ), pp.75–76.
Miller, L., Savage, A., Mazak, B. and Giraldo, H. Habitat
assessment of the historic home range of cotton-top
tamarins (Saguinus oedipus) using Landsat imagery: Current
status and possible strategies for the future, p.56.
Norconk, M. White-faced saki group dynamics in Lago
Guri, Venezuela: 1990 –2000, p.41.
Pinto, L. and Setz, E. Feeding ecology of Alouatta belzebul in
flood-plain forest of southern Amazon, p.96.
Phillips, K. A. and Shauver, L. M. Reunion displays in tufted
capuchins (Cebus apella ), p.83.
Raboy, B. and Dietz, J. Immigration patterns and group
stability in wild golden-headed lion tamarins in southern
Bahia, Brazil, p.52.
Ross, C., Orit, G. and French, J. A. Genetic mosaics across
tissues in callitrichids (Callithrix kuhlii, black-tufted ear
marmosets), p.55.
Savage, A., Giraldo, H., LaRotta, C., Soto, L. H. and Garcia,
E. F. Conservation education efforts in Colombia: Cottontop tamarins as ambassadors for habitat preservation,
p.57.
Schaffner, C., Aureli, F. and Caine, N. Following the rules:
Why tamarins don’t reconcile, pp.49–50.
Sheeran, L. Ethical issues in primatological research: Captive
settings (workshop), pp.27–28.
Soltis, J., Newman, J. D., Bernhards, D. and Donkin, H.
T he structure and function of the chuck vocalization in
captive squirrel monkeys, p.38.
Suarez, S. Feeding patch choice in free-ranging Ateles
belzebuth belzebuth: Implications for cognitive foraging
skills, p.41.
Urquiza-Haas, T. and Serio-Silva, J. C. Nutritional
composition of Ficus perforata fruit (pulp, seeds and animal
matter), consumed by howler monkeys (Alouatta palliata
mexicana ), pp.105–106.
Weghorst, J. A. Behavioral ecology of the central American
spider monkey (Ateles geoffroyi panamensis) in Costa Rican
wet forest: Pilot study results, p.97.
Ziegler, T. Effective use of fecal and urinary cortisol
measurements for determining health conditions in wild
and captive nonhuman primates, p.44.
MEET INGS
American Society of Primatologists 25th Annual Meeting,
1– 4 June, 2002, Oklahoma City, Oklahoma, USA. For
more information contact: Janette Wallis, Department of
Psychiatry and Behavioral Sciences, University of Oklahoma
Health Sciences Center, P. O. Box 26901, Oklahoma City,
OK 73190. Tel: (405) 627-8820, Fax: (405) 271-3808,
e-mail: <janette-wallis@ouhsc.edu>.
3rd International Canopy Conference, June, 2002, Cairns,
Australia. Sponsored by the Queensland Government of
Australia and the Smithsonian Institution, the conference
theme is “Science, Policy and Utilisation” and is intended
to bring together scientists, environmental managers and
policy makers concerned with the discovery and sustainable
use of forests around the world. Contact: Eileen Domagala,
e-mail <Eileen Domagala@premiers.qld.gov.au> for further
information or look on the web site: <http://www.premiers.
qld.gov.au/whatsnew.htm>.
XV National Congress of The Italian Primatological
Association, 30 May–1 June 2002, Istituto di Psicologia del
CNR Rome. Organized by the Associazione Primatologica
Italiana. Contact: Annarita Wirz, Istituto di Psicologia
del CNR; Via Ulisse Aldovandi 16/B, 00197 Roma,
Italy, Tel: 06-3221252, 3221437, Fax: 06-3217090; e-mail:
<api2002congresso@yahoo.it>. Web site: <http://www.unipv.
it/webbio/api/cong15/15con.htm>.
Encroachment on Wildlife Ecosystems: New and ReEmerging Viral Epidemics, 9–11, June 2002, Artis
Zoological Gardens, Amsterdam, T he Netherlands. T he
meeting focuses on the consequences of altering eco-systems,
alterations that affect an established virus-host balance, with
new and re-emerging diseases as a consequence. Agents
often persist in their natural reservoirs until an ecological
imbalance, such as the destruction of forests, results in
contact with a new and susceptible species. All too frequently
we have witnessed the result as an epidemic with high
morbidity and mortality. Several new and re-emerging viral
epidemics, like West Nile fever, Rift Valley fever, foot-andmouth disease, were witnessed during the last decade and
illustrate the importance and timeliness of this meeting.
144
Reservoirs of viruses in exotic species (such as fruit bats for
Nipah virus) and in aquatic vertebrates (influenza B virus)
were recognized, and their impact on human and animal
health was significant. It is the aim of the organizers to
have experts on wildlife and zoo animal virology discuss
the consequences of trans-species transmission on wildlife,
domestic animals and on the human population. T he meeting
will be an informal opportunity to exchange experience
and expertise in the monitoring, diagnosis, prevention
(including wildlife vaccination) and control of outbreaks.
Contact: Ms. Jeanette Schouw, Department of Virology,
Biomedical Primate Research Centre, PO Box 3306, 2280
GH Rijswijk, T he Netherlands, e-mail: <wildlife@bprc.nl>,
Website: <http://www.wildlife2002.nl>.
16 th Annual Meeting of the Society for Conservation
Biology, 14 –18 July, 2002, Canterbury, England at the
University of Kent’s campus. T he theme of this meeting
will be, People and Conservation and will be co-hosted by
the Durrell Institute of Conservation and Ecology (DICE),
based in the Department of Anthropology at the University
and the British Ecological Society. For more information
contact: Nigel Leader-Williams, SCB2002 Program Chair,
e-mail: <scb2002@ukc.ac.uk> or Andrew Pullin, BES,
e-mail: <a.s.pullin@bham.ac.uk>. Web site: <www.ukc.ac.uk/
anthropology/dice/scb2002/>.
American Veterinary Society of Animal Behavior, 15 July,
2002, Nashville, Tennessee, USA. T his meeting will be held
in conjunction with the annual meeting of the American
Veterinary Medical Association. T he meeting format will
include presentations, question and answer sessions and a
poster session. Deadline for submitting abstracts is December
1, 2001. Authors will be notified by January 15, 2002. For
more information contact: Dr. Margaret Duxbury, 1299
South Shore Drive Amery, WI 54001. Tel: (715) 268-9900,
Fax: (715) 268-2691, e-mail: <mduxburyl@yahoo.com>.
Ecological Society of America 87 th Annual Meeting joint
with the Ecological Society of Mexico, 4 – 8 August, 2002.
Arizona, USA. Details from: ESA, 1707 H St., NW, Suite
400, Washington, DC 20006, USA, Tel: + (202) 833 8773,
Fax: +(202)833 8775, e-mail: <esahq@eas.org>.
XIXth Congress of the International
Primatological Society, 4 –9 August
2002, Beijing, China. Organized by the
Mammalogical Society of China and the
Institute of Zoology, Chinese Academy
of Sciences. T he venue will be the Beijing International
Convention Center, No. 8 Beichen Dong Road, Beijing
100101, China (website <www.bicc.com.cn>). T he theme
of the Congress is “Caring for Primates”, focusing on the
progress and prospects of primatology and the conservation
Neotropical Primates 9(3), December 2001
of non-human-primates. Deadline for symposium and
workshop titles: 31 August, 2001. Deadline for submitting
abstracts is the 31 March, 2002. On-Line registration
will be available after 1 December, 2001. Contact address:
Prof. Fuwen Wei, Secretary General, 19 th Congress of the
International Primatological Society, c/o Institute of Zoology.
Chinese Academy of Sciences, 19 Zhongguancan Lu,
Haidian, Beijing 100080, China, Fax: (86-10) 82627388,
e-mail: <IPS_Beijing@panda.ioz.ac.cn>. Home page: <http:
//www.ips.ioz.ac.cn>.
Xº. Congresso Brasileiro de Primatologia, 26 –30 August
2002, Universidade Federal do Pará, Belém. Hosted by
the Sociedade Brasileira de Primatologia (SBPr). For more
information: Stephen Ferrari, Departamento de Genética,
Universidade Federal do Pará, Campus do Guamá, Caixa
Postal 8607, 66075-150 Belém, Pará, Brazil, e-mail:
<ferrari@ufpa.br>.
Annual Meetings of the IUCN/SSC Conservation
Breeding Specialist Group (CBSG), 10 –13 August, 2002,
T he World Zoo Organization (WZO), 13–17 August
2002, and T he International Association of Zoo Educators
(IZE), 17–22 August, 2002, Hofburg Palace, Redoutensäle,
Vienna. Hosted by the Schoenbrunn Zoo. For more
information: Austropa Interconvention, Conference Office,
Friedrichstrasse 7, A-1010 Vienna, Austria, Fax: +43 1 315
56 50, e-mail: <austropa.congress@verkehrsbuero.at>.
The World Zoo Organization, 13 –17 August, 2002,
Redoutensale, Vienna, Austria. Hosted by the Schoenbrunn
Zoo. For more information contact: Austropa Intercovention,
Conference office, Friedrichstrasse 7, A-1010, Vienna,
Austria. Fax: +43 1 315 56 50, e-mail: <austral.congress@
verkehrsbuero.at>.
The International Association of Zoo Educators, 17–22
August, 2002, Redoutensale, Vienna. Hosted by the
Schoenbrunn Zoo. For more information contact: Austropa
Intercovention, Conference Office, Friedrichstrasse 7, A-1010
Vienna, Austria. Fax: +(43) 1-315-56-50, e-mail:
<austra.congress@verkehrsbuero.at>.
The American Zoo and Aquarium Association (AZA)
Annual Conference, 10 –14 September 2002, Fort Worth
Zoological Park, Fort Worth, Texas. T he conference program
is geared toward the many disciplines in the zoological
profession - directors, animal curators, keepers, society
members, scientists, gift shop merchandisers, and practitioners
in public relations, development, education, and government
affairs will all find something of interest. Most of the AZA
committees and special interests groups meet in conjunction
with the Annual Conference. For more information: <http:/
/www.aza.org/ConfWork/>.
Notes to Contributors
Scope
T he journal/newsletter aims to provide a basis for conservation information relating to the primates of the neotropics. We
welcome texts on any aspect of primate conservation, including
articles, thesis abstracts, news items, recent events, recent publications, primatological society information and suchlike.
photographs, high quality Ýgures, and high quality maps and
tables. Please keep these to a minimum. We stress the importance
of providing maps which are publishable.
News items. Please send us information on projects, field
sites, courses, recent publications, awards, events, activities
of Primate Societies, etc.
References
Examples of house style can be found throughout this journal.
Please refer to these examples when listing references.
Submissions
Please send all English and Portuguese contributions to: Jennifer
Pervola, Conservation International, Center for Applied
Biodiversity Science, 1919 M. St. NW, Suite 600, Washington,
DC 20036, Tel: 202 912-1000, Fax: 202 912-0772, e-mail:
<j.pervola@conservation.org>, and all Spanish contributions
to: Ernesto RodrÌguez-Luna, Instituto de NeuroetologÌa,
Universidad Veracruzana, Apartado Postal 566, Xalapa 91000,
Veracruz, MÈxico. Tel: 281 8-77-30, Fax: 281 8-77-30, 8-63-52,
e-mail: <saraguat@speedy.coacade.uv.mx>
Contributions
Manuscripts can be in English, Spanish or Portuguese,
and should be double-spaced and accompanied by the text
on diskette for PC compatible text-editors (M S-Word,
WordPerfect, Excel, and Access), and/or e-mailed to
<j .pervola@ conservation.org>.(English, Portuguese) or
<saraguat@ speedy.coacade.uv.mx> (Spanish) Hard copies
should be supplied for all Ýgures (illustrations and maps) and
tables. T he full name and address for each author should be
included. Please avoid abbreviations and acronyms without the
name in full. Authors whose Ýrst language is not English, please
have texts carefully reviewed by a native English speaker.
Articles. Each issue of Neotropical Primates will include up to
three full articles, limited to the following topics: Taxonomy,
Systematics, Genetics (when relevant for systematics), Biogeography, Ecology and Conservation. Texts for full articles should
not exceed about 20 pages in length (1.5 spaced, and including the references). Please include an abstract in English, and
(optional) one in Portuguese or Spanish. Tables and illustrations
should be limited to six, excepting only the cases where they are
fundamental for the text (as in species descriptions, for example).
Full articles will be sent out for peer-review.
Short articles. T hese are usually reviewed only by the editors.
A broader range of topics are encouraged, including such as
behavioral research, in the interests of informing on general
research activities which contribute to our understanding of
platyrrhines. We encourage reports on projects and conservation and research programs (who, what, where, when, why etc.)
and most particularly information on geographical distributions,
locality records, and protected areas and the primates which
occur in them. Texts should not exceed 10 pages in length
(1.5 spaced, including the references).
Figures and maps. Articles can include small black-and-white
Journal article
Stallings, J. D. and Mittermeier, R. A. 1983. T he black-tailed
marmoset (Callithrix argentata melanura ) recorded from Paraguay. Am. J. Primatol. 4: 159ñ163.
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(eds.), pp. 23ñ62. Alan R. Liss, New York.
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Napier, P. H. 1976. Catalogue of Primates in the British Museum
(Natural History). Part 1: Families Callitrichidae and Cebidae.
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Wallace, R. B. 1998. T he behavioural ecology of black spider
monkeys in north-eastern Bolivia. Doctoral thesis, University
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O. and Singh, B. 1975. Report on a primate survey in Guyana.
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Washington, DC.
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Neotropical Primates
Journal and Newsletter of the IUCN/SSC Primate Specialist Group
Vol. 9(3), December, 2001
Contents
Short Articles
Body Weights of Adult Female Alouatta palliata in Costa Rica Increase with Age
Evan L. Zucker, Margaret R. Clarke, and Kennneth E. Glander ....................................................................................................................... 93
Variations in Group Size in White-Faced Sakis (Pithecia pithecia): Evidence For Monogamy or Seasonal Congregations?
Shawn M. Lehman, Waldyke Prince, Mireya Mayor ......................................................................................................................................... 96
Diurnal Activity Budgets of Black Spider Monkeys, Ateles chamek, in a Southern Amazonian Tropical Forest
Robert B. Wallace ...................................................................................................................................................................................... 101
Distribución Parcial del Tití Gris (Saguinus leucopus, Callitrichidae) en el Departamento de Antioquia, Colombia
Carlos A. Cuartas-Calle ............................................................................................................................................................................. 107
Drinking by Howler Monkeys (Alouatta fusca) and Its Seasonality at the Intervales State Park, São Paulo, Brazil
Sandra Steinmetz ...................................................................................................................................................................................... 111
Uso de Plantas Como Alimento por Monos Aulladores, Alouatta palliata, en el Parque Yumká, Tabasco, México
Yasminda García del Valle, David Muñoz, Miguel Magaña-Alejandro, Alejandro Estrada, and Berenice Franco ............................................... 112
Alouatta guariba clamitans (Cabrera, 1940): A New Southern Limit for the Species and for Neotropical Primates
Rodrigo C. Printes, Marcus V. A. Liesenfeld, and Leandro Jerusalinsky ........................................................................................................... 118
Two Taxonomies of the New World Primates – A Comparison of Rylands et al. (2000) and Groves (2001)
Anthony B. Rylands ................................................................................................................................................................................... 121
News ....................................................................................................................................................................................................... 125
Primate Societies ..................................................................................................................................................................................... 132
Recent Publications ................................................................................................................................................................................. 133
Meetings ................................................................................................................................................................................................. 143