P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
International Journal of Primatology, Vol. 24, No. 5, October 2003 ( C? 2003)
Demographic Changes over Thirty Years in a Red
Howler Population in Venezuela
R. Rudran1,3 and E. Fernandez-Duque2
Received December 3, 2002; accepted January 2, 2003
During a 30-year span (1969?1999) the annual growth rate of a Venezuelan
red howler (Alouatta seniculus) population fluctuated irregularly, but its size
increased, remained stable for a short while, and finally declined sharply. The
increase took place in three stages, and began as an increase in the size of
established groups. The next two stages of population increase were due to
the formation of new groups and their subsequent increases in size. These
two stages likely occurred because of habitat regeneration, which increased
the areas where newly formed groups could establish home ranges. The pop-
ulation decline of 74% was most likely due to disease. However, new groups
died out more rapidly than established groups, indicating that food shortages,
especially in recently regenerated areas, may also have contributed to the pop-
ulation crash. The food shortages could have been caused by unpredictable
periods of drought, which may explain the irregular size fluctuations of the
study population. Since many howler species show irregular size fluctuations
and sharp declines, their demographic features may reflect adaptations to un-
predictable events like droughts and disease epidemics. On this premise we
explain the preponderance of unimale groups and female-biased birth sex
ratios at low densities and the dispersal of both sexes as adaptations for in-
creasing a population rapidly after a decline. Within the population, mortality
of small juvenile females was higher in multimale than in unimale groups,
though medium juvenile and older immature females were better represented
1Department of Conservation Biology, National Zoological Park, Smithsonian Institution,
Washington, District of Colombia 20008.
2Center for Reproduction of Endangered Species, Zoological Society of San Diego, San Diego,
California.
3To whom correspondence should be addressed; e-mail: rrudran@crc.si.edu.
925
0164-0291/03/1000-0925/0 C? 2003 Plenum Publishing Corporation
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
926 Rudran and Fernandez-Duque
in multimale than in unimale groups. These results may be explained in terms
of group composition and the mating systems in red howlers.
KEY WORDS: density; rate of increase; population size; group composition; age structure;
sex ratios.
INTRODUCTION
The value of conducting long-term field studies to develop a thorough
understanding of primate population dynamics cannot be overemphasized.
Whether the motivation is applied, as when developing Population Viabil-
ity Analysis models for conservation purposes (Caughley, 1994; Cowlishaw
and Dunbar, 2000; Dobson and Lyles, 1989), or theoretical, as when for-
mulating explanations for the evolution of taxon-specific life-history traits
(Charnov and Berrigan, 1993; Ross, 1991), any successful attempt to under-
stand population dynamics will have to be based on studies spanning several
generations. Only then can we expect to determine how population fluctua-
tions affect demographic parameters. Until we know the effect of population
fluctuations and understand the processes driving these changes, we will not
be able to fully explain the observed species-specific life-history strategy as
an adaptive response to the environment.
Given the abundant literature demonstrating that numerous taxa show
regular population fluctuations (Krebs, 1996), it is surprising that this topic
has not received more attention in primate investigations. This lack of atten-
tion may have been due to two reasons. One is the popular misconception
that was recently refuted by Chapman and Peres (2001), that the tropics,
where most primates are found, are relatively stable, especially when com-
pared to temperate areas where population fluctuations have been investi-
gated most extensively (Stenseth, 1999). The other is that few primate field
studies have lasted long enough to cover several generations (Dobson and
Lyles, 1989) or to provide the basic information needed to describe popula-
tion changes in detail.
In the Neotropics, the longest nonhuman primate field studies have
been conducted on howlers (Alouatta spp.). All 6 species of howlers have
been studied for various periods of time (Kinzey, 1997) since the pioneering
work of Carpenter on Alouatta palliata at Barro Colorado Island, Panama?
(Carpenter, 1934). The mantled howler (Alouatta palliata) and the red
howler (A. seniculus) have been the two most intensively studied species with
some of the studies spanning a few decades (Agoramoorthy and Rudran,
1995; Clarke et al., 1986, 1994; Crockett, 1996; Eisenberg, 1979; Estrada,
1982; Estrada et al., 1999; Fedigan et al., 1998; Fedigan and Jack, 2001;
Glander, 1992; Milton, 1996; Neville, 1972; Pope, 1990, 1998, 2000; Rudran,
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 927
1979; Sekulic, 1983). Using these long-term data some authors have hy-
pothesized that their populations may undergo fluctuations (Crockett, 1996;
Crockett and Eisenberg, 1986; Milton, 1982, 1996). We contribute to an eval-
uation of this hypothesis by describing changes in a red howler population
in Venezuela during 30 years.
Between 1969 and 1999 the study population underwent periods of ex-
pansion, stability and decline. We characterize the different stages with data
on the population?s size, density, rate of increase, age structure, sex ratios,
and group size and composition during each stage. The study, which includes
data from approximately 5 generations of howlers, allows us to address the
following questions about population dynamics: Was the rate of popula-
tion increase relatively stable over time? Were population parameters, e.g.,
group size and sex ratios, related to population density? Did sex ratios of the
different age-sex classes change during the population fluctuations in a pre-
dictable manner? Is the population recovering? Are changes in population
parameters related to environmental factors?
METHODS
Study Area and Population
We conducted the study at Hato Masaguaral, a cattle ranch located
in Gua?rico State, Venezuela (8? 34? N, 67? 35? W). Hato Masaguaral?s wild
fauna and flora were protected from fire and deforestation by its strongly
conservation-minded owner, Sr. Tomas Blohm. The ranch included two ma-
jor habitat types; a continuous gallery forest along the river Guarico, and
forest patches?matas?away from the river that were surrounded by sea-
sonally inundated grasslands (Troth, 1979). Red howlers occupied both habi-
tat types, but the census data that we present here were obtained mainly
from the population inhabiting the matas. The mata population has been
studied by numerous researchers: Agoramoorthy and Rudran (1992, 1995),
Crockett (1984, 1985, 1996), Crockett and Pope (1993), Crockett and Rudran
(1987a,b), Eisenberg (1979), Herrick et al. (2000), Neville (1972), Pope (1990,
1992), Rudran (1979), and Sekulic (1982, 1983).
Rainfall in the area is highly seasonal with a discrete wet and dry season
from May to October and November to April, respectively (Crockett and
Rudran, 1987a). The vegetation is semideciduous with many trees and shrubs
losing most of their leaves by the late dry season. The elevation is about 70 m.,
and the monthly average temperatures varied from about 19?22?C minimum
to 33?38?C maximum, with daytime temperatures being generally higher in
the dry season (Troth, 1979).
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
928 Rudran and Fernandez-Duque
Data Collection
Different investigators conducted the censuses; all were trained to clas-
sify individuals into appropriate age categories before they began collect-
ing field data. The training helped to standardize the population structure
data. Moreover, we regularly conducted ear-tagging operations involving
chemical capture of red howlers period (Agoramoorthy and Rudran, 1994;
Thorington et al., 1979, Rudran, unpublished data), in order to facilitate
unambiguous identification of individuals.
Periodic censuses of the study population began in June 1976 and con-
tinued through March 1999. In June and July 1976, and from January 1977 to
October 1978, March 1979 to February 1981 and March 1985 to September
1993 we conducted population censuses more or less each month. From
March 1981 to February 1985 and after September 1993 we usually con-
ducted censuses once per year during the dry season (November?April). We
located the study groups with the help of their loud calls, and if this failed, by
systematically searching different parts of their home ranges. Once located,
we determined group size by counting its members repeatedly until several
consistent totals were obtained. Then we sexed each group member and as-
signed it to an age category via a classification system based on physical and
behavioral characteristics of known-age individuals. We assigned individuals
of both sexes to the infant category if their ages were known or estimated
to be ?10 mo. Females >10 mo are small-, medium-, and large-juveniles
(SJF, MJF, LJF) or subadults (SAF) if their ages are known or estimated to
be >19, 28, 37 and 46 mo, respectively. Similarly, males >10 mo are small-,
medium-, large-juveniles (SJM, MJM, LJM) or subadults (SAM) if their ages
are known or estimated to be <22, 34, 46 and 58 mo, respectively. Females
and males whose ages are known or estimated to be >46 or 58 mo, respec-
tively, are adults. After assigning age categories to individuals, we confirmed
a group?s identity via several features including their size, composition, the
area where they were seen, and any members that were identifiable by natu-
ral markings or ear tags (Agoramoorthy and Rudran, 1994; Thorington et al.,
1979).
We also saw solitary males and females and associations of ?2 indi-
viduals during population censuses. Whenever solitaries and associations
were encountered, we recorded their locations within the study area, size,
composition and individual characteristics. The individuals of an association
either left the area after a while, or stayed together as a social group until
they produced infants. We included the newly formed groups in subsequent
population censuses, which gave rise to a gradual increase in the number of
groups under investigation.
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 929
Data Analysis
Our analysis is based on published and unpublished data
spanning 1969?1999. The published data are derived from Neville (1972,
1976) and Rudran (1979) and cover the period from 1969 to 1978.
The unpublished data included information collected after 1978 by Rudran
in 1979, 1981, 1982, 1984, 1996, 1997 and 1999 and by Rudran and
colleagues: Rumiz (1985?1987), Valderrama (1988), Sestrich (1989),
Agoramoorthy (1990?1992, 1994, 1995) and Kilber (1993) during other
years.
During some population censuses, particularly those conducted on an
annual basis, it was not possible to contact all study groups. In these cases,
we assigned each missing group its average size based on counts during
the previous and the following periods (mo or yr) of contact. Although we
assigned sizes to missing groups we did not attempt to deduce their compo-
sition. Therefore, the groups were excluded from the analysis of population
structure, for which we used only groups whose compositions were actually
verified in the field.
Population size for any given year is the total number of individuals
living in new and established groups during a particular month of that year.
The month of choice was more or less the same during different years (be-
tween December-April) in order to standardize for within-year population
size fluctuations due to demographic events. We computed population den-
sity estimates assuming that the size of the study area is 1.55 km2 (Rudran,
1979).
We computed the annual rate of increase as the ratio of population
size in two successive counts (Caughley, 1977). When two successive counts
were longer or shorter than a year apart (e.g. 1976?1978), we proportion-
ately adjusted the difference between them when calculating the annual rate
of increase. We applied no adjustments for multiple comparisons since all
comparisons are explicitly presented together with the raw data on which
the comparisons were based.
RESULTS
Thirty-five monkeys were marked with ear-tags in 1978, and 149, 5 and
70 individuals were ear-tagged in 1981, 1985 and 1987, respectively. Between
1989?1994 an additional 75 howlers were marked with ear-tags. Ear-tags
facilitated unequivocal identification of individuals and thereby improved
the quality of the census data throughout the study.
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
930 Rudran and Fernandez-Duque
Changes in Population Size, Density and Rate of Increase
During the 30-year period, the population first expanded, then remained
relatively stable, and finally began a decline that continued through 1999
(Table I). Despite this general trend, the population?s annual rate of increase
fluctuated between one and 6% from 1970 to 1978 (Figure 1), while grew
from 146 to 186 individuals, and density increased from 94 to 120 howlers/
km2. Even after this period of moderate growth, the annual rate of increase
continued to fluctuate until 1989 as the population expanded and reached a
maximum of 346 individuals and density of 223 howlers/km2. In 1990 there
was no increase, but during the next 3 years the population registered mod-
erately negative rates of increase that ranged between one and 5%. This was
followed by substantial reductions in size; sometimes as much as one-third
of the population was lost from one year to the next beginning in 1994: By
the end of March 1999 the population had been reduced to one-fourth of
its maximum size and included only 90 individuals; population density was
58 howlers/km2.
The growth of the population was at least partly due to habitat regen-
eration that increased the size and vegetation density of the matas within
the study area. This enabled dispersing males and females to band together
and to establish new groups that later grew in size as well. Both events con-
tributed to the increase of the study population.
Changes in the Size and Number of Groups
Population growth between 1970 and 1978 resulted in part from slight
increases in group size. The median size of the 13 groups observed by Neville
(1972) that could unequivocally be identified by Rudran increased slightly
during that period (median, range: 8, 6?12 vs. 9, 5?13, n D 13), but the
difference is not statistically significant (Unpaired t-test, two tails, tD?0.282,
df D 12, p D 0.783). Subsequent increases in population size were due to
changes in the size and number of established groups, as well as to the
addition of new groups to the study population (Table I). For instance, 59%
of the population increase that occurred between 1978 and December 1981
(55 of 94 individuals) was due to the increase in median size of established
groups from 8.0 (range: 4?14) to 10.5 individuals (range: 6?18, nD 22 groups,
t D ?4.957, df D 21, p D 0.000). Another 21% represented 20 individuals of
two established groups added to the study, while the remainder belonged to
4 new groups that formed during the same period.
After the established groups reached a stable median size of 10 individ-
uals in 1987, the population continued to expand as a result of the formation
of new groups and an increase in the median size of these groups. Between
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
T
ab
le
I.
C
ha
ng
es
in
po
pu
la
ti
on
si
ze
,p
op
ul
at
io
n
de
ns
it
y,
an
d
si
ze
(m
ed
ia
n)
an
d
nu
m
be
r
of
es
ta
bl
is
he
d
an
d
ne
w
gr
ou
ps
70
72
76
77
78
79
81
84
85
86
87
88
89
90
91
92
93
94
95
96
97
99
Po
pu
la
ti
on
si
ze
14
6a
16
3a
18
2
18
4
18
6
21
9
28
0
27
8
29
4
30
4
32
2
33
6
34
6
34
6
32
8
31
8
31
4
21
9
21
2
15
5
11
7
90
D
en
si
ty
94
10
5
11
7
11
9
12
0
14
1
18
1
17
9
19
0
19
6
20
8
21
7
22
3
22
3
21
2
20
5
20
3
14
1
13
7
10
0
75
58
(i
n
d/
km
2
)
N
o.
gr
ou
ps
To
ta
l
19
19
21
21
22
24
28
30
33
33
34
34
36
36
36
36
33
29
29
23
18
15
E
st
ab
lis
he
d
21
21
21
22
24
24
24
24
24
24
24
24
24
24
22
18
18
15
14
12
N
ew
1
2
4
6
9
9
10
10
12
12
12
12
11
11
11
8
4
3
Si
ze E
st
ab
lis
he
d
9:
0
8:
0
8:
0
9:
0
10
:
5
9:
5
9:
5
9:
5
10
:
0
10
:
0
10
:
0
10
:
0
10
:
0
9:
0
10
:
0
7:
5
7:
5
8:
0
7:
0
6:
0
N
ew
4
4
4:
5
5:
5
6:
0
7:
0
8:
0
8:
0
9:
0
8:
5
8:
0
6:
5
9:
0
6:
0
6:
0
6:
0
5:
5
6:
0
M
in
.s
iz
e
E
st
ab
lis
he
d
4
4
4
4
6
6
5
6
5
6
6
5
5
4
5
5
5
4
4
4
N
ew
4
4
4
4
4
4
5
5
4
5
5
5
5
4
4
2
4
5
M
ax
.s
iz
e
E
st
ab
lis
he
d
15
17
14
15
18
15
15
15
14
17
15
16
16
17
17
14
11
10
10
9
N
ew
4
4
6
7
7
9
10
10
12
12
15
14
15
12
9
8
7
6
%
gr
ou
ps
M
ul
ti
m
al
e
52
43
59
54
46
40
63
64
47
41
42
49
50
55
72
32
24
38
33
7
U
ni
m
al
e
48
57
41
46
54
60
38
36
53
59
58
51
50
45
28
68
76
62
67
93
M
ea
n
si
ze
M
ul
ti
m
al
e
8:
5
8:
7
8:
8
9:
2
10
:
5
9:
1
9:
0
8:
7
9:
3
9:
8
10
:
7
10
:
5
10
:
0
9:
7
9:
1
8:
0
8:
6
7:
6
7:
2
9:
0
U
ni
m
al
e
9:
5
5:
9
7:
9
9:
0
9:
6
9:
4
6:
4
7:
9
8:
6
9:
0
8:
8
8:
6
8:
6
8:
2
8:
9
6:
6
6:
7
6:
9
6:
0
5:
8
N
ot
e.
V
al
ue
s
es
ti
m
at
ed
fr
om
pr
ev
io
us
an
d/
or
fo
llo
w
in
g
ye
ar
s
ar
e
sh
ow
n
w
it
h
on
e
de
ci
m
al
.
a
Fr
om
N
ev
ill
e,
19
76
.
931
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
932 Rudran and Fernandez-Duque
Fig. 1. Changes in Population Rate of Increase (1970?1999).
1979 and 1989 12 new groups were formed and their median size increased
from 4.5 (4?6, n D 3 groups) to 9.0 (4?12, n D 12 groups).
By 1991 the population began its decline and median group sizes of
new and established groups also started a decline that continued more or
less through the next 8 years. Twenty-one groups disintegrated and only 15
established and new groups survived. The established groups decreased in
size more slowly than new groups did (Table I), but both groups ultimately
had a median size of 6 individuals per group in 1999, with established and new
groups having 4?9 and 5?6 individuals, respectively. Density is a good pre-
dictor of the size of established groups (R2 D 0:782, dfD 18, FD 69.089, pD
0.000), as well as of new groups (R2 D 0:385, df D 14, F D 8.76, p D 0.010).
Changes in Group Composition
The population consisted of unimale, and multimale groups (mean ?
s.d.: 2.2? 0.2 adult males, range: 2?6). The sizes of both types of groups were
similarly affected by changes in density, and they became larger as density
increased, and smaller when density declined (Uni-male: adj R2 D 0:359,
FD 11.641, dfD 18, pD 0.003; Multi-male: adj R2 D 0:521, FD 21.628, dfD
18, p D 0.000).
Multimale groups were somewhat larger than unimale groups (meanD
9.3 ? 1.0 vs 8.1 ? 1.2 individuals). Additionally, they had significantly more
small- and medium- juvenile males, and more medium-juvenile, large-
juvenile and subadult females than unimale groups did (Mann-Whitney tests,
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 933
Table II. Group composition of unimale and multimale groups
Unimale Multimale U z p
Adults
Males 1 2:2? 0:2 0 ?5.794 0.00
Females 2:5? 0:3 2:7? 0:3 158.5 ?1.123 0.26
Subadults
Males 1:3? 0:2 1:2? 0:1 142 ?1.647 0.10
Females 1:0? 0:1 1:1? 0:2 142.5 ?1.871 0.06
Large juveniles
Males 1:2? 0:2 1:2? 0:2 178.5 ?0.595 0.55
Females 1:2? 0:5 1:2? 0:2 140 ?1.907 0.06
Medium juveniles
Males 1:2? 0:2 1:4? 0:3 113 ?2.381 0.02
Females 1:1? 0:2 1:3? 0:4 122 ?2.199 0.03
Small juveniles
Males 1:2? 0:2 1:4? 0:3 87 ?3.101 0.00
Females 1:2? 0:2 1:2? 0:2 199.5 ?0.014 0.99
Infants
Males 1:2? 0:2 1:3? 0:2 184.5 ?0.429 0.67
Females 1:3? 0:2 1:2? 0:2 153 ?1.28 0.20
Note. All tests are Mann?Whitney U tests for two independent samples.
two-tailed, Table II). However, there is no significant difference between the
two groups in the number of adult females or the number of large juvenile
and subadult males in them (Table II).
The percentage of uni- and multimale groups in the population changed
over time (Table I). In 1978 there was a slight preponderance of multimale
groups (Rudran, 1979). From then until 1993, the percentage of multimale
groups in the population varied between 40 and 70%. When population
size and density began a rapid decline in 1994, the percentage of multimale
groups began to plummet and reached its lowest level of 7% by the end of
the study.
All but one (11/12) of the new groups that were formed during the
study had a unimale structure when first established. Unimale groups were
vulnerable to male invasions, which are social changes that transformed uni-
male into multimale groups (Crockett, 1984; Rudran, 1979; Sekulic, 1983)
and mainly affected large unimale groups. For instance, the average size
of 9 unimale groups that experienced invasions between 1984 and 1985
is significantly larger than the average size of all unimale groups in the
population (12:2? 2:6 vs 8:1? 1:2 individuals). Since male invasions trans-
formed large unimale into multimale groups, only small unimale groups
remained in the population between 1984 and 1985. Therefore, the average
size of unimale groups was drastically reduced from 9.4 to 6.4 individuals
(Table I).
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
934 Rudran and Fernandez-Duque
Changes in Age Structure
Throughout the 30-year period, approximately half of the individuals
of the study population comprised adults. (Table III). The second most nu-
merous age-class was the juveniles, which included a third of the population,
whereas the rest comprised subadults and infants. This average represen-
tation of age classes notwithstanding, the age structure during population
expansion and decline were different, as indicated by the percentage of indi-
viduals in each age-sex class during both periods (Figure 2). The percentage
of adult males and females is significantly lower during growth than decline
as indicated by a multivariate analysis of variance using the 12 different age-
classes as dependent variables (AM: F D 3.612, p D 0.071, df D 21; AF: F D
8.302, p D 0.009, df D 21). Infants of both sexes were more numerous while
the population was growing than when it was declining (IM: F D 14.208,
df D 21, p D 0.001; IF: F D 4.043, df D 21, p D 0.057). In the small juvenile
class, males were more abundant during expansion than decline (F D 3.603,
p D 0.072), whereas females showed no statistically significant change (F D
1.422, p D 0.247). Conversely, medium-sized juveniles of both sexes were
more abundant during decline than during expansion (MJM: FD 6.993, pD
0.016; MJF: F D 12.725, p D 0.002). Differences between the proportions of
subadults and large juveniles during growth and decline of the population a
not statistically significant for either sex.
The number of adult males and females increased more or less gradu-
ally from 1970 until 1991 (Table III). Then, from 1992 to 1993 there was a
16% decline in the number of adult females that was not accompanied by
a similar change in the number of adult males. The decrease did not affect
all groups similarly, and was due to the loss of 24 adult females from only
14 study groups. At the same time, 17 study groups experienced no change
and 5 groups actually added a total of 7 females. The decrease was partly
due to the sharp decline in the number of medium juvenile females in 1990
to 8 individuals from 19 the previous year (Table III). This decline led to the
low number of large juvenile females reported in 1991 and eventually in the
decreased number of adult females beginning in 1993.
The number of infants has been increasing since 1994, when the pop-
ulation experienced its steepest decline. After producing only 3 infants in
1994, there were 7, 15, 10 and 13 infants born in 1995, 1996, 1997 and 1999,
respectively.
Changes in Sex Ratios
Overall, there were more females than males in the population
(Table III). In the adult class, the sex ratio was strongly biased in favor
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 935
T
ab
le
II
I.
C
ha
ng
es
in
th
e
nu
m
be
r
of
in
di
vi
du
al
s
in
ea
ch
ag
e?
se
x
cl
as
s
70
72
76
77
78
79
81
84
85
86
87
88
89
90
91
92
93
94
95
96
97
99
A
du
lt
M
al
es
28
30
33
30
36
37
42
42
59
61
55
55
58
59
62
57
65
26
26
29
16
16
Fe
m
al
es
44
47
56
55
55
62
76
78
86
90
98
97
10
6
10
6
11
0
10
6
89
44
39
45
33
30
Su
ba
du
lt
s
M
al
es
14
13
11
12
10
16
16
16
16
11
11
7
13
21
15
11
14
12
7
4
1
4
Fe
m
al
es
5
6
6
4
3
6
9
8
6
4
7
6
6
10
10
8
9
1
8
2
0
2
Ju
ve
ni
le
s
L
ar
ge
m
al
es
17
8.
5
13
14
14
13
10
23
8
14
8
26
28
23
13
16
18
5
17
8
9
4
L
ar
ge
fe
m
al
es
15
5
4
3
6
6
9
7
10
12
9
23
18
16
8
12
8
4
7
3
2
3
M
ed
iu
m
m
al
es
6.
5
14
14
13
12
20
15
13
7
20
22
22
12
24
17
18
15
15
8
10
7
M
ed
iu
m
fe
m
al
es
8
7
10
9
13
12
11
16
12
18
22
19
8
17
17
30
11
7
11
7
8
Sm
al
lm
al
es
8
12
9
12
7
20
18
11
22
23
20
16
27
23
17
9
8
10
9
1
1
Sm
al
lf
em
al
es
5
9
9
12
12
26
22
10
16
19
12
11
18
18
19
15
5
8
9
1
2
In
fa
nt
s
M
al
es
8
13
7
9
4
16
21
19
31
29
29
22
26
27
15
21
20
2
1
4
1
3
Fe
m
al
es
15
10
9
13
12
17
19
14
28
26
25
24
23
18
13
17
19
1
0
8
7
10
U
ns
ex
ed
in
fa
nt
s
3
1
2
2
0
5
6
3
2
N
ot
e.
A
ug
70
:f
ro
m
Ta
bl
e
2
(N
ev
ill
e,
19
76
),
ju
ve
ni
le
s
w
er
e
no
td
is
ti
ng
ui
sh
ed
by
si
ze
;J
un
-7
2:
fr
om
Ta
bl
e
3
(N
ev
ill
e,
19
76
);
Ju
n-
76
:f
ro
m
Ta
bl
es
1
an
d
2
(R
ud
ra
n,
19
79
).
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
936 Rudran and Fernandez-Duque
Fig. 2. Age structure of the population during growth (1970?1990) and decline
(1991?1999). M: male, F: female, A: adult, SA: subadult, LJ: large juvenile, MJ:
medium juvenile, SJ: small juvenile, I: infant.
of females, while among subadults and juveniles the bias was in favor of
males. Sex ratios in the adult and subadult classes did not change noticeably
over time and there is no apparent relationship between the proportion of
males and females in the adult and subadult classes and population density
(Table IV). Conversely, population density explains an important propor-
tion of the change in the sex ratio of large and small juvenile categories.
When density was low there tended to be more males than females in the
large juvenile category and more females than males in the small juvenile
category (Table III). In other words, population density is a good predictor of
the sex ratio in the large juvenile and small juvenile categories, as indicated
by linear regression analyses (Table IV).
The number of male and female infants in the population varied ap-
preciably during different years. Relatively more females were born at the
beginning and end than during the central years of the study. Changes in the
ratio of male-to-female infants in the population are linearly associated with
changes in density. The ratio is small, i.e. more females than males were born,
when density was low, but it became large when density increased (Figure 3).
Given the relatively small numbers of infants in the sample beginning in 1995
(Table III), we evaluated statistically the relationship between sex ratio and
density, assigning half of all unsexed individuals to each sex. We dropped the
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 937
Table IV. Tests of linear relationships between population density
and sex ratios of each age class
Ratios R2 adj. Constant Slope F p
AM/AF ?0.04 0.57 0.00 0.28 0.61
SAM/SAF ?0.02 4.17 0.01 0.70 0.42
LJM/LJF 0.28 4.07 0.01 8.43 0.01
MJM/MJF ?0.02 1.47 0.00 0.60 0.45
SJM/SJF 0.11 0.67 0.00 3.37 0.08
IM/IFa 0.77 59.24 0.00 ?0.01 0.01
IM/IFb 0.86 101.36 0.00 ?0.19 0.01
IM/IFc 0.52 19.55 0.00 0.21 0.00
aUnsexed infants assigned equally to both sex classes.
bAll unsexed infants considered females.
cAll unsexed infants considered males.
data point for 1994 from the analysis because the only 3 infants born give an
extreme sex ratio (IM/IF D 2, n D 3) of doubtful biological meaning.
DISCUSSION
Our analyses confirm that the study population expanded during the
1970s and 1980s as reported elsewhere (Crockett, 1996; Crockett and
Eisenberg, 1986; Pope, 1998; Rudran, 1979). After almost two decades of
growth the population declined sharply in the early 1990s; and the marked
increase in births during the last years could indicate that the population was
beginning to recover around 1996.
Fig. 3. Population density plotted against infant sex ratio. Unsexed infants were assigned
50?50 to each sex class.
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
938 Rudran and Fernandez-Duque
Factors Influencing Population Growth
The population?s growth was influenced by several factors, including
the size and formation of social groups. Initially the population grew as a re-
sult of established groups becoming larger until they reached maximum size.
The second stage of growth was primarily due to associations of dispersing
males and females persisting long enough as new social groups to produce
infants. The third stage of growth was mainly the result of new groups increas-
ing in size until they reached maximum size. Group formation during peri-
ods of expansion of howler populations has also been observed in Panama?
(Carpenter, 1934; Collias and Southwick, 1952), Costa Rica (Fedigan et al.,
1998; Fedigan and Jack, 2001) and Argentina (Rumiz, 1990).
A possible explanation for the increase in median size of established
groups during the first stage of growth is that the population could have
been recovering from a previous crash. Conversely, a likely explanation for
the formation and expansion of new groups?the second and third stages of
growth?that began in 1978 is the increase in the amount of habitat suitable
for howlers within the study area. By that time, the ban on deforestation
and burning had been in effect for several decades, which allowed woody
plants to regenerate and increase the size of forest patches occupied by
the study population. It was mainly in the recently regenerated areas and
the interstices between the home ranges of established groups that new
groups were able to establish themselves (Rudran, unpublished). Thus, we
attribute habitat protection resulting in the gradual increase of areas suitable
for red howlers to be a factor that contributed to the observed sequence of
population growth. A process with similar characteristics was observed in
Panama? (Collias and Southwick, 1952) and at two study sites in Costa Rica
(Fedigan and Jack, 2001; Glander, 1992). We also interpret the fact that new
groups were smaller than established groups to be an outcome of living in
recently regenerated areas and as an indicator of the importance of habitat
features, such as food availability, in regulating the size of red howler groups
and populations.
Factors Influencing Population Decline
Perhaps the most convincing evidence for the cause of population de-
cline was the discovery of 9 dead red howlers in 1996 (Rudran, unpublished).
We estimate death to have occurred 3 weeks to several mo before discovery,
indicating that mortality in the population was a gradual process, as would
be expected from a disease epidemic or food shortage. The skeletal remains,
which were almost complete, included 3 adults (one male and 2 females),
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 939
2 subadults and 4 juveniles. Six skeletans were in close proximity to one
another suggesting that they belonged to a single group. The fact that all
age classes experienced mortality, and that entire groups disappeared from
their home ranges, suggests that disease was a factor that contributed to the
decline of the study population. We could not determine the type of disease
that had caused the decline.
During the period of decline, established groups decreased in size more
slowly than new groups did (Table I). Furthermore, only 50% of the estab-
lished groups had disintegrated by 1999, whereas 75% of the new groups
had disappeared by that time. The increased susceptibility of new groups to
size reduction and disintegration suggests that problems of exploiting food
from recently regenerated and relatively unfamiliar areas also contributed
to population decline. Dispersing female red howlers, which must have fre-
quently obtained food from areas unfamiliar to them, ate diets that were
significantly less nutritious than those of group-living females, and they also
traveled farther each day, (Crockett and Pope, 1993; Pope, 1989). Similarly,
new groups, which were essentially associations of dispersing individuals,
may not have been sufficiently familiar with their relatively new home ranges
to find adequate supplies of food, especially during periods of food short-
age. Hence, they would likely have traveled farther to find food and to avoid
hostile interactions with their neighbors that lived in established groups.
Stress due to a poor diet, food shortage,and/or intimidation by established
groups may also have increased the susceptibility of new groups to death
from disease. In mantled howlers, stress due to food shortage was impli-
cated in lowering resistance to bot-fly infestations (Otis et al., 1981), which
can cause mortality (Milton, 1996).
Factors Influencing Irregular Population Fluctuations
The population?s growth rate fluctuated irregularly and also declined
sharply at least once during 30 years. Some of the fluctuations seemed to
be associated with annual rainfall, and population growth tended to slow
down following a relatively dry year. For instance, the rate of increase was
smaller between 1972?1978, than between 1970?1972, and was negative for
the period 1981?1984, and negative again ever since 1990 (Figure 1). 1972,
1982, and 1989 were 3 of the driest years, getting 738, 998, and 966 mm of
rainfall, which are significantly below the annual mean for the area (1400 mm,
1920?1997, nD 77 years, D. Thielen, pers. com.). During the 1990?s, when the
population?s rate of increase was always negative, there were only 2 years
when annual rainfall was higher than the average (1991: 1465 mm and 1996:
1507 mm).
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
940 Rudran and Fernandez-Duque
The effects of droughts on terrestrial communities have been poorly
investigated (Holmgren et al., 2001), but they are gradually attracting more
attention (Chapman and Peres, 2001; Leigh, 1999; Wright et al., 1999). One
likely effect of droughts is the reduction of red howler foods, which may
have been responsible for the irregular fluctuations of the population. Food
scarcity could also have led to deterioration of the general health of the
individuals making them less resistant to diseases. Hence, food shortage due
to droughts in combination with disease could have been the reason for the
population crash in the early1990?s.
If droughts and disease affected the mata population, they could also
have affected the population living in the gallery forest nearby. When Neville
(1972) surveyed the gallery forest population in 1970 the mean group size
was 9.6. The mean group size was reduced to 4.5 by 1978 (J. Robinson pers.
comm.), indicating that the gallery forest population had suffered a dramatic
decline a few years earlier. In subsequent years, mean group size fluctu-
ated between about 7.8 and 8.2 until 1987 (Crockett, 1996), and between
7.6 and 9.4 from 1988 through 1993 (X. Valderrama, K. Sestrich, and G.
Agoramoorthy pers. comm., and Rudran unpublished data). There were no
further surveys in the gallery forest until 1997. Because social groups were
difficult to locate then, we recorded data on bouts of howling. The rates of
howling declined from 423/100 hr in 1997 to 200/100 hr in 1999 and 82/100 hr
in 2000. Along with the decline in howling rates, the sightings of dead howlers
reported by local people during 2000 provided additional evidence that the
gallery forest population had again crashed in the late 1990s.
The gallery forest population crashed some years after the mata pop-
ulation was affected by a similar decline. The time lag may have been due
to differences in habitat features. The gallery forest is floristically richer
than the mata (Troth, 1979) and offers a greater variety of foods to howlers
(Crockett, 1987). Furthermore, it includes a river and a stream, which prob-
ably made the vegetation less susceptible to droughts than that of the mata.
Therefore, the gallery forest population may have been able to withstand
the effects of droughts and food shortages somewhat longer than the mata
population could before succumbing to disease.
Several other howler populations have experienced irregular popu-
lation fluctuations or crashes or both. Two other red howler populations
crashed as a result of disease in Venezuela between 1992?1996 (Pope, 1998).
A population of Alouatta caraya in northern Argentina crashed in 1982, pos-
sibly due to bot-fly infestation (Rudran, unpublished data). The population
on Barro Colorado Island (BCI), Panama?, experienced a crash between 1933
and 1951; yellow fever, botfly infestation and drought are possible causes
(Collias and Southwick, 1952). The population eventually recovered, but
fluctuated irregularly and declined sharply at least once between 1977 and
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 941
1993 (Milton, 1996). It appeared to be regulated by unpredictable periods
of food scarcity (Milton, 1982) coupled with the primary and secondary ef-
fects of bot fly parasitism (Milton, 1996). A population of Alouatta palliata
in Santa Rosa National Park also experienced irregular fluctuations in pop-
ulation size, and a sharp decline during a span of 28 years (Fedigan and Jack,
2001).
Since numerous howler species experience irregular population fluctu-
ations and periodic crashes, their demographic features may reflect adapta-
tions or responses to cope with unpredictable events. With this premise in
mind we interpret the demographic details of our study population.
Group Size and Composition
Our analysis indicated that density was a good predictor of the size of
established and new groups. This result is consistent with a previous analysis
based on 10 years of data from the same population (Crockett, 1996) and
with information from mantled howlers (Fedigan et al., 1998).
Contrary to expectations, the number of adult females in uni- and mul-
timale groups did not differ significantly, suggesting that adult males in mul-
timale groups may have access, on average, to fewer females than the adult
male of a unimale group. Nevertheless, sexually mature males may have pre-
ferred to remain in multimale groups because they offered greater resistance
to male invasions than unimale groups did (Agoramoorthy and Rudran,
1995), and thereby reduced the likelihood of infanticide, which could in-
crease the survival of their infants. When adult males of multimale groups
are related (Pope, 1990), remaining in them would also have increased the
survival of their offspring, and therefore, enhance their inclusive fitness.
Because the number of adult females was similar in uni- and multimale
groups, there were no differences in the number of infants produced in both
types of groups (Table II). Therefore, the resistance of multimale groups to
infanticide should have made their small juvenile recruitment rates higher
than those of unimale groups. Despite this expectation, our results showed
that multimale groups had higher rates of small juvenile recruitment only
for male infants, whereas recruitment of female infants was the same as in
that unimale groups. This suggests that small juvenile females were more
vulnerable to death in multimale than in unimale groups. The increased vul-
nerability of small juvenile females in multimale groups may have been the
result of aggression directed at them by unrelated adult males, as in mantled
howlers (Clarke, 1982 cited in Glander, 1992). Our finding that group com-
position and mating systems may have been important determinants of the
survival of small juvenile females helps to clarify the details of the general
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
942 Rudran and Fernandez-Duque
impression that females of the study population experienced a high rate of
mortality as juveniles (Crockett and Pope, 1993).
After the small juvenile stage, females were better represented in the
older immature age classes of multimale than of unimale groups (Table II).
This situation could have arisen in two different ways. One is via faster rates
of dispersal of immature females from unimale than from multimale groups
in order to avoid the deleterious effects of inbreeding (Packer, 1979; Pusey,
1980). This suggestion is contrary to the assumption that inbreeding avoid-
ance is unimportant to explain female dispersal (Crockett, 1984). However,
the assumption fails to consider female dispersal in the context of group
composition and mating systems, which our investigations indicate may be
important considerations in female dispersal. Another possible reason why
there were more medium juvenile and older immature females in multimale
than in unimale groups is that the presence of several adult males in mul-
timale groups could have encouraged immature females to remain in their
natal groups because of future reproductive opportunities with unrelated
sexual partners. In contrast, the presence of several adult males in multi-
male groups may have induced subadult and large juvenile males of the
groups to disperse earlier than males born in unimale groups did, thereby
resulting in similar numbers of males of these age classes in both groups
(Table II).
The proportion of uni- and multimale groups fluctuated throughout
the study. When density was lowest towards the latter part of the study,
unimale groups vastly outnumbered multimale groups (Table I). The large
proportion of unimale groups at low densities, and the fact that 11 of 12
new groups were unimale when first established suggest that males prefer
to monopolize a social group whenever possible. However, when density
increases or a group matures, internal recruitment, male invasions, dispersal
and mortality can transform unimale into multimale groups and vice versa.
The transformations would depend on the peculiarities of a group?s history,
composition and dynamics and would therefore be hard to predict from
population parameters. This may explain why the proportion of unimale
and multimale groups in the population fluctuated somewhat haphazardly
at medium and high densities.
Age Structure and Sex Ratios
The age structure of the population during growth and decline fitted
theoretical expectations. The population included a larger proportion of
infants when it was growing than when it was declining. In contrast, the
population consisted of a relatively larger number of adults when it was
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 943
declining than when it was growing. At all times females outnumbered males
in the adult age class, but they tended to be less numerous than males in the
subadult and juvenile age classes. Sex ratios favoring females in the adult
age class and males in the immature age classes, can in part, be explained
by differential rates of maturation of the two sexes. However, we believe
that socially mediated mortality of small juvenile females and of males at or
near adulthood (Dittus, 1979, 1980) also contributed to the sex ratios and
age structure of the population (Crockett and Pope, 1988; Rudran, 1979).
Between 1992?1993, there was an appreciable decline in the number of
adult females without similar changes in any of the other age classes. High
rates of mortality of medium juvenile females in 1990, resulting in low rates
of recruitment explain only part of the decline. The rest of the decline was
probably due to the death of females after reaching adulthood. A similar
phenomenon occurred in another Venezuelan red howler population, Hato
El Fr??o, where, adult female mortality was supposed to have been the result
of disease (Pope, 1998).
Sex ratios varied with density, with the changes being less pronounced
in the subadult or adult classes than they were among infants and juveniles.
Among infants, more females than males were born at low densities, whereas
the reverse was true at high densities. Since infant production is an impor-
tant determinant of population increases, the proportion of adult females
in a population will influence the rate of population increase. Hence, at low
population densities, female biased birth sex ratios will help to enhance rates
of female recruitment, which in turn will result in higher rates of population
increase. Under these circumstances, adults of both sexes that produce fe-
male offspring would likely contribute disproportionately more to the gene
pool and thereby increase their fitness. Furthermore, the female biased birth
sex ratio would also compensate for high rates of mortality of small juvenile
females that otherwise undermines their recruitment, and therefore, the rate
of population increase. At high densities, when there is a full complement
of breeding females in social groups, young females would find it difficult to
breed in their natal groups as a result of intrasexual competition (Crockett,
1984). Moreover, seeking mates through dispersal would become difficult
because saturated habitats are unlikely to provide young females with op-
portunities to enter established groups or to find unoccupied areas to form
new groups. Conversely, breeding opportunities in saturated habitats for
males would be better, because they could disperse to form male coalitions
and invade other social groups or stay in their natal groups even past adult-
hood (Agoramoorthy and Rudran, 1993) to breed with unrelated females.
Remaining in the natal group would also help to increase inclusive fitness.
Under these conditions individuals that produce male offspring are likely to
enhance their fitness more than those that produce female infants do. Hence
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
944 Rudran and Fernandez-Duque
selection would be expected to favor a male biased birth sex ratio at high
densities.
Skewed birth sex ratios occur in several mammals including primates
(Clark, 1978; Silk, 1983), and many reasons have been suggested for the de-
viation from a 50/50 birth sex ratio (Clark, 1978; Clutton-Brock et al., 1981;
Jones, 1988; Silk, 1983; Trivers and Willard, 1973; Zschokke, 2002). In red
howlers the skewed birth sex ratio appears to be a function of population
density. It should be noted that the we detected influence of population
density on the birth sex ratio only when data from the entire study was con-
sidered. This illustrates how information from shorter study periods could
sometimes lead to erroneous interpretations of the actual situation (Crockett
and Rudran, 1987b).
The ability of red howlers to adjust birth sex ratio may be an adapta-
tion to population fluctuations experienced by the species due to periodic
food shortages and disease epidemics. Recall also that survival of small ju-
venile females was better in uni- than in multimale groups and that unimale
groups were most numerous at low densities. Therefore, when a population
declines and reaches low density, adaptations such as the dispersal of both
sexes, formation of unimale groups and female biased birth sex ratios would
have contributed to a rapid build up of the population. It is possible that such
adaptations may also be found in other howler species that experience irreg-
ular population fluctuations and that they function to build up a population
rapidly after it declines.
Final Remarks
Our investigation shows that long-term studies are essential for a clear
understanding of the demography of long-lived species such as red howlers.
Assuming population stability based on a short- term study can lead to flawed
conclusions if a population is in fact unstable or fluctuating. The duration of
a study should be considered when analyzing and interpreting the results of
an investigation (Chapman and Balcomb, 1998; Crockett, 1985; Fleagle et al.,
1999). Our long-term investigations indicate that the demographic features
of our study population were influenced by social as well as environmental
factors.
ACKNOWLEDGMENTS
Our research was funded by the National Institutes of Mental Health
Grant No. MH 28840-01 awarded to J.F.Eisenberg and R. Rudran, and by the
Smithsonian Institution?s International Environmental Sciences Program
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 945
and the Friends of the National Zoo. Rudran thanks Tomas and Cecilia
Blohm for their long years of friendship and unfailing support for the red
howler project that made the whole endeavor feasible. He also thanks
F. Boccardo, N. A. Muckenhirn, D. S. Mack, J. G. Robinson, R. W.
Thorington Jr., D. E.Wilson, C. M. Crockett, C. Saavedra, T. Pope, S. Crissey,
D. Rumiz, X. Valderrama, K. Sestrich, G. Agoramoorthy and B. Kilber for
various types of field assistance throughout the study. Thanks are also due
to J.F. Eisenberg who helped to set up the project during its initial stages.
Finally, we thank Claudia Valeggia for helping with the long and tedious
process of data tabulation.
REFERENCES
Agoramoorthy, G., and Rudran, R. (1992). Adoption in free-ranging red howler monkeys
(Alouatta seniculus) of Venezuela. Primates 33: 551?555.
Agoramoorthy, G., and Rudran, R. (1993). Male dispersal among free-ranging red howler
monkeys (Alouatta seniculus) in Venezuela. Folia Primatol. 61: 92?96.
Agoramoorthy, G., and Rudran, R. (1994). Field application of Telazol (Tiletamine hydrochlo-
ride and Zolezepam hydrochloride) to immobilize wild red howler monkeys (Alouatta
seniculus) in Venezuela. J. Wild. Dis. 30: 417?420.
Agoramoorthy, G., and Rudran, R. (1995). Infanticide by adult and subadult males in free-
ranging red howler monkeys. Ethology 99: 75?88.
Carpenter, C. R. (1934). A field study of the behavior and social relations of howling monkeys.
Comp. Psychol. Monogr. 10: 1?168.
Caughley, G. (1977). Analysis of Vertebrate Populations, Wiley, Chichester, UK.
Caughley, G. (1994). Directions in conservation biology. J. An. Ecol. 63: 215?244.
Chapman, C. A., and Balcomb, S. R. (1998). Population characteristics of howlers: Ecological
conditions or group history. Int. J. Primatol. 19: 385?403.
Chapman, C. A., and Peres, C. A. (2001). Primate conservation in the new millenium: The role
of scientists. Evol. Anthropol. 10: 16?33.
Charnov, E. L., and Berrigan, D. (1993). Why do female primates have such long life spans and
so few babies? Or life in the slow lane. Evol. Anthropol.: 191?194.
Clark, A. B. (1978). Sex ratio and local resource competition in a prosimian primate. Science
201: 163?165.
Clarke, M. R., Zucker, E. L., and Glander, K. E. (1994). Group takeover by a natal male howl-
ing monkey (Alouatta palliata) and associated disappearances and injuries of immatures.
Primates 35: 435?442.
Clarke, M. R., Zucker, E. L., and Scott, N. J. J. (1986). Population trends of the mantled howler
groups of La Pacifica, Guanacaste, Costa Rica. Am. J. Primatol. 11: 79?88.
Clutton-Brock, T. H., Albon, S. D., and Guinness, F. E. (1981). Parental investment in male and
female offspring. Nature 289: 487?489.
Collias, N., and Southwick, C. (1952). A field study of population density and social organization
in howling monkeys. Proc. Am. Philos. Soc. 96: 143?156.
Cowlishaw, G., and Dunbar, R. (2000). Primate Conservation Biology, Chicago University Press,
Chicago.
Crockett, C. M. (1984). Emigration by female red howler monkeys and the case for female
competition. In Small, M. (ed.), Female Primates: Studies by Women Primatologists, Alan
R. Liss, Inc., New York, pp. 159?173.
Crockett, C. M. (1985). Population studies of red howler monkeys (Alouatta seniculus). Natl.
Geogr. Res. 1(2): 264?273.
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
946 Rudran and Fernandez-Duque
Crockett, C. M. (1987). Diet, dimorphism and demography: Perspectives from howlers to ho-
minids. In Kinzey, W. G. (ed.), Evolution of Human Behavior: Primate Models, Suny Press,
Albany, NY, pp. 115?135.
Crockett, C. M. (1996). The relation between red howler monkey (Alouatta seniculus) troop
size and population growth in two habitats. In Norconk, M. A., Rosenberger, A. L., and
Garber, P. A. (eds.), Adaptive Radiations of Neotropical Primates, Plenum, New York, pp.
489?510.
Crockett, C. M., and Eisenberg, J. F. (1986). Howlers: Variations in group size and demography.
In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R., and Struhsaker, T. T. (eds.),
Primate Societies, University of Chicago Press, Chicago, pp. 54?68.
Crockett, C. M., and Pope, T. R. (1988). Inferring patterns of aggression from red howler monkey
injuries. Am. J. Primatol. 15: 289?308.
Crockett, C. M., and Pope, T. R. (1993). Consequences of sex differences in dispersal for juvenile
red howler monkeys. In Pereira, M. E., and Fairbanks, L. A. (eds.), Juvenile Primates: Life
History, Development and Behavior, Oxford University Press, pp. 104?118.
Crockett, C. M., and Rudran, R. (1987a). Red howler monkey birth data I: Seasonal variation.
Am. J. Primatol. 13: 347?368.
Crockett, C. M., and Rudran, R. (1987b). Red howler monkey birth data II: Interannual, habitat,
and sex comparisons. Am. J. Primatol. 13: 369?384.
Dittus, W. P. J. (1979). The evolution of behaviors regulating density and age-specific sex ratios
in a primate population. Behavior 63: 266?302.
Dittus, W. P. J. (1980). The social regulation of primate populations: A synthesis. In Lindburg,
D. G. (ed.), The Macaques: Studies in Ecology, Behavior and Evolution, Van Nostrand
Reingold, New York, pp. 263?286.
Dobson, A. P., and Lyles, A. M. (1989). The population dynamics and conservation of primate
populations. Conserv. Biol. 3: 362?380.
Eisenberg, J. F. (1979). Habitat, economy, and society: Some correlations and hypotheses for
the Neotropical primates. In Bernstein, I. S., and Smith, E. O. (eds.), Primate Ecology and
Human Origins: Ecological Influences on Social Organization, Garland Press, New York,
pp. 215?262.
Estrada, A. (1982). Survey and census of howler monkeys (Alouatta palliata) in the rain forests
of ?Los Tuxtlas?, Veracruz, Mexico. Am. J. Primatol.
Estrada, A., Anzures, D., and Coates-Estrada, R. (1999). Tropical rain forest fragmentation,
howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas, Mexico. Am. J. Pri-
matol. 48: 253?262.
Fedigan, L. M., and Jack, K. (2001). Neotropical primates in a regenerating Costa Rican Dry
Forest: A comparison of howler and capuchin population patterns. Int. J. Primatol. 22:
689?713.
Fedigan, L. M., Rose, L. M., and Avila, R. M. (1998). Growth of mantled howler groups in a
regenerating Costa Rican dry forest. Int. J. Primatol. 19: 405?432.
Fleagle, J. G., Janson, C. H., and Reed, K. E. (1999). Spatial and temporal scales in primate
community structure. In Fleagle, J. G., Janson, C. H., and Reed, K. E. (eds.), Primate
Communities, Cambridge University Press, Cambridge, pp. 284?288.
Glander, K. E. (1992). Dispersal patterns in Costa Rican mantled howling monkeys. Int. J.
Primatol. 13: 415?436.
Herrick, J. G., Agoramoorthy, G., Rudran, R., and Harder, J. D. (2000). Urinary progesterone
in free-ranging red howler monkeys (Alouatta seniculus): Preliminary observations of the
estrous cycle and gestation. Am. J. Primatol. 51: 257?263.
Holmgren, M., Scheffer, M., Ezcurra, E., Gutierrez, J. R., and Mohren, G. M. J. (2001). El Nin?o
effects on the dynamics of terrestrial ecosystems. Trends in Ecol. Evol. 16: 89?94.
Jones, W. T. (1988). Variations in sex-ratios of banner tailed kangaroo rats in relation to popu-
lation density. J. Mammal. 69: 303?310.
Kinzey, W. G. (1997). New World Primates, Aldine de Gruyter, New York.
Krebs, C. J. (1996). Population cycles revisited. J. Mammal. 77: 8?24.
Leigh, E. G. J. (1999). Tropical Forest Ecology. A View From Barro Colorado Island, Oxford
University Press, New York.
P1: GRA
International Journal of Primatology [ijop] pp985-ijop-472817 October 6, 2003 15:30 Style file version Nov. 18th, 2002
Population Dynamics of Alouatta seniculus 947
Milton, K. (1982). Dietary quality and demographic regulation in a howler monkey population.
In Leigh, E. G. J., Rand, S. A., and Windsor, D. M. (eds.), The Ecology of a Tropical Forest.
Seasonal Rhythms and Long-Term Changes, Smithsonian Institution Press, Washington,
DC, pp. 273?289.
Milton, K. (1996). Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler
monkey (Alouatta palliata) population in Panama. J. Zool. Lond. 239: 39?63.
Neville, M. K. (1972). The population structure of red howler monkeys (Alouatta seniculus) in
Trinidad and Venezuela. Folia Primatob. 17: 56?86.
Neville, M. (1976). The population and conservation of howler monkeys in Venezuela and
Trinidad. In Thorington, R. W., Jr., and Heltne, P. G. (eds.), Neotropical Primates: Field
Studies and Conservation, National Academy of Sciences, Washington, DC, pp. 101?109.
Otis, J. S., Froelich, J. W., and Thorington, R. W., Jr. (1981). Seasonal and age-related differential
mortality by sex in mantled howlers, Alouatta palliata. Int. J. Primatol. 2: 197?205.
Packer, C. (1979). Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim. Behav.
27: 1?36.
Pope, T. R. (1989). The influence of mating systems and dispersal patterns on the ge-
netic structure of red howler monkey population. University of Florida, Gainesville,
pp. 172.
Pope, T. R. (1990). The reproductive consequences of male cooperation in the red howler
monkey: Paternity exclusion in multi-male and single-male troops using genetic markers.
Behav. Ecol. Sociobiol. 27: 439?446.
Pope, T. R. (1992). The influence of dispersal patterns and mating system on genetic differen-
tiation within and between populations of the red howler monkey (Alouatta seniculus).
Evolution 46: 1112?1128.
Pope, T. R. (1998). Effects of demographic change on group kin structure and gene dynamics
of populations of red howling monkeys. J. Mammal. 79: 692?712.
Pope, T. R. (2000). Reproductive success increases with degree of kinship in cooperative coali-
tions of female red howler monkeys (Alouatta seniculus). Behav. Ecol. Sociobiol. 48: 253?
267.
Pusey, A. E. (1980). Inbreeding avoidance in chimpanzees. Anim. Behav.-552.
Ross, C. (1991). Life history patterns of new world monkeys. Int. J. Primatol. 12: 481?502.
Rudran, R. (1979). The demography and social mobility of a red howler (Alouatta seniculus)
population in Venezuela. In Eisenberg, J. F. (ed.), Vertebrate Ecology in the Northern
Neotropics, Smithsonian Institution Press, Washington, DC, pp. 107?126.
Rumiz, D. (1990). Alouatta caraya: Population density and demography in Northern Argentina.
Am. J. Primatol. 21: 279?294.
Sekulic, R. (1982). Daily and seasonal patterns of roaring and spacing in four red howler
(Alouatta seniculus) troops. Folia Primatol. 39: 22?48.
Sekulic, R. (1983). The effect of female call on male howling in red howler monkeys (Alouatta
seniculus). Int. J. Primatol. 4: 291?305.
Silk, J. B. (1983). Local resource competition and facultative adjustment of sex ratios in relation
to competitive abilities. Am. Nat. 121: 56?66.
Stenseth, N. C. (1999). Population cycles in voles and lemmings: Density dependence and phase
dependence in a stochastic world. Oikos 87: 427?461.
Thorington, R. W., Jr., Rudran, R., and Mack, D. (1979). Sexual dimorphism of Alouatta senicu-
lus and observations on capture techniques. In Eisenberg, J. F. (ed.), Vertebrate Ecology in
the Northern Neotropics, Smithsonian Institution Press, Washington, DC, pp. 97?106.
Trivers, R. L., and Willard, D. E. (1973). Natural selection of parental ability to vary the sex
ratio of offspring. Science 179: 90?92.
Troth, R. G. (1979). Vegetational types on a ranch in the central llanos of Venezuela. In
Eisenberg, J. F. (eds.), Vertebrate Ecology in the Northern Neotropics, Smithsonian In-
stitution Press, Washington, DC, pp. 17?30.
Wright, J. S., Carrasco, C., Calderon, O., and Paton, S. (1999). The El Nin?o southern oscillation,
variable fruit production, and famine in a tropical forest. Ecology 80: 1632?1647.
Zschokke, S. (2002). Distorted sex ratio at birth in the captive pygmy hippopotamus. J. Mammal.
83: 674?681.