International Journal of Primatology, Vol. 2, No.

3, 1981

The Demography of Howler Monkeys

(Alouatta paUiata) on Barro Colorado
Island, Panamd

J. W . F r o e h l i c h , x R . W . T h o r i n g t o n , Jr., 2
and J. S. O t i s 3

ReceivedNovember 26, 1980; revisedApril 8, 1981

Chronological ages o f Alouatta on Barro Colorado Island (BC1) were

estimated from longitudinal dental wear. Combining these data with
visual censuses, we approximated the study population's age profile. A
stable model was then constructed; from it we derived age-specific mortality
rates. Mortality o f immature animals is high, with 88070 o f the males and
65070 o f the females dying before 5 years. Adult mortality is low until 11
years, when it accelerates. The average adult life span is 16.6 years for
males and 15.5 for females. The maximum life span is over 20 years. A
pubertal male growth spurt occurs from 3 to 5 years, at which time females
are primiparous. Sexual size differences develop primarily during this time.
The 1976 age profile had anomalously f e w animals aged 7 years and males
aged 8-9 and 15-16 years. With corroborating evidence, we hypothesize
that these deficits resulted from excessive rainfall in 1963 and 1971, which
reduced the fall fruit crop and led to a high juvenile mortality. Within half
o f our study troops, some adult males have nearly identical ages, suggesting
an active process o f age-mate coalition. We hypothesize a form o f kin
selection, wherein peripheral male cohorts from the same natal troop have
greater survival and social success than solitary animals. The stable model
suggests an annual growth rate o f 1.5~ during the 1970s. Estimates o f 16. 7
and 4070for the previous two decades, following a yellow-fever epidemic,

'Department of Anthropology, University of New Mexico, Albuquerque, New Mexico

87131.
~Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560.
3Department of Statistics, University of New Mexico, Albuquerque, New Mexico 87131.
207
0 1 6 4 - 0 2 9 1 / 8 1 / 0 9 0 0 - 0 2 0 7 $ 0 3 . 0 0 / 0 9 1981 Plenum Pubhshlng Corporation
208 Froehlich, Thorington, and Otis

imply that the BCI population is becoming stationary. A very different

age structure existed on neighboring Orchid Island in 1976, suggesting
general f o o d limitation. By contrast, the lowered, but continuing growth
on BCI suggests a less drastic limiting mechanism. We hypothesize that
intratroop social competition limits population growth by regulating
subadult survival rates during f o o d scarcity cycles.
KEY WORDS: Alouatta palliata; demography;maturation;mortality;populationregulation.

INTRODUCTION

This study was conducted on the northeast corner of Barro Colorado

Island (BCI), Republic of Panamfi. Our study area constituted approx-
imately 10% of the island, bordering the central plateau and extending
from the Lutz watershed to the Fairchild and Gross Peninsulas, as well as
the adjoining Orchid Island (see Fig. 1).
BCI was formed in 1914 by the rising waters of Gatun Lake, during
the construction of the Panama Canal. Prior to its formation, the island
was a hill in the midst of low-lying, swampy forests, adjacent to the
Chagras River (Bartlett and Barghoorn, 1973). The island has an area of
155 km 2. Its geography and geology were described by Woodring (1958),
who also discussed relevant historical facts. Kenoyer (1929), Standley
(1933), Bennett (1963), Croat (1978), Knight (1975), and Thorington
et al. (1982) provided descriptions of the species composition and structure
of the forest.
The northeast corner of BCI was subjected to considerable dis-
ruption from the 1850s, the gold-rush period, through 1914, with the
abortive French canal and subsequent American canal construction. This
disruption was particularly severe on Fairchild Point, small neighboring
Orchid Island, and areas around the laboratory clearing, where portions
of the forest are usually described as being younger than other areas
(Bennett, 1963; Knight, 1975), On Gross Point, the forest appears to be
older (Bennett, 1963; Carpenter, 1934) and, particularly along the ridge,
was probably less disturbed in the past. Portions of the forest bordering
the central plateau were mostly undisturbed during the 19th century
(Bennett, 1963; Chapman, 1929).
In 1923, the island was declared a biological reserve and, with time,
the protection given to the flora and fauna has become quite strict. In the
1930s, howler monkeys occurred mainly in the "tall primary forest" of
central and western BCI, but not beyond the bases of Gross and Fairchild
Points (Carpenter, 1934; Chapman, 1938). By 1951, monkeys were well
established on all of Gross Peninsula and Orchid Island, but still only at
Demography of Howler Monkeys 209

Orchid Is.
Gross Pt.
;child PL

N. 9010'
'<'--Lutz _: o,
..~..j "-......*.

~.o~

( ,. ....... PJateau -
-....- ,.... -
i, :..:
i
.~
%~176
[-.j .... ? _,
9"~ %.o..."

Meters [
dTi
I
6 ' lobo 79~ i w.
Fig. 1. Map of Barro Colorado Island, Panama, showing principal landmarks discussed in the
text (modified from Carpenter, 1965). See Froehlich and Thorington (1982) for outlines of
eensused troop ranges.

the base o f Fairchild Peninsula (Collias and Southwick, 1952). The distri-
bution was much the same in 1959 (Carpenter, 1964). By 1967, howler
troops occurred all the way to the tip of Fairchild Point (Smith, 1977).
Thus, the present distribution o f howler monkeys throughout our study
area is a relatively recent phenomenon, having occurred within the last two
decades.
The howlers of BCI have been censused many times since Carpenter's
(1934) pioneering studies in 1932 and 1933, but it has been difficult to
obtain good demographic data on the population. Only the major popula-
tion fluctuations have been reasonably well documented. In 1932, Carpenter
counted approximately 500 animals. The population was reduced by a
yellow-fever epidemic in 1949 (Collias and Southwick, 1952), but it in-
creased rapidly from approximately 237 in 1951 to an estimated 814 in 1959
210 Froehlich, Thorington, and Otis

(Carpenter, 1964) and an estimated excess of 1100 in 1967 (Smith, 1977).

Various investigators (Chivers, 1969; Mittermeier, 1972; Smith, 1977) have
considered the population to be approaching a stationary condition.
However, their census techniques do not seem accurate enough to us to
confirm this trend. Moreover, the relative age structure of the population
has always been difficult to estimate. Carpenter's age categories--infant
1,2, and 3; juvenile 1, 2, and 3; and adult--have been variously interpreted
by different investigators. For example, Chivers (1969) and Smith (1977)
estimated the immature proportion of the BCI population in 1967 to be
36 and 28%, respectively. This difference suggests either censusing inac-
curacy or a disagreement about when a juvenile becomes an adult, which
should be one of the least arbitrary transitions.
There also has been little agreement on the absolute ages of infants
and juveniles. Carpenter (1934, 1965) gave two different estimates, and
both are in disagreement with the inconsistent estimates of Glander (1980),
Neville (1972), and Smith (1977). The only published adult age estimates
are based on a single troop (Glander, 1980). These age estimates cannot
be augmented by data from caged animals, since these data are limited and
inconsistent (Malinow et aL, 1968; Shoemaker, 1979). Furthermore, it has
not been possible to determine the sex of juvenile and infant animals with-
out capturing them. Prepubertal males are also indistinguishable from
nonreproductive adult females. Accordingly, previous comparisons of
demographic conditions in different populations have been restricted to
such crude parameters as the ratio of adult females to infants and juveniles
(Heltne et aL, 1976). These wildlife management estimates are of dubious
value, because of the subjective nature of the age/sex categories and a
paucity of longevity data.
Since accurate demographic data are essential for wildlife manage-
ment and for detailed evolutionary studies of animal populations, we
present in this paper our estimates of maturation rates, age structure,
mortality rates, and longevity of howler monkeys on BCI, based on longi-
tudinal and cross-sectional data derived from 125 captured animals.

MATERIALS AND METHODS

Howler monkeys were captured and recaptured by means of a CO2-

powered dart gun, which propelled and injected a liquid anesthetic. This
"Pneudart" system has been described by Scott et al. (1976). Our pro-
cedures differed only slightly from theirs. We used phencyclidine-HC1
(Sernylan) for capturing and ketamine-HCl for maintaining immobilization
after capture. As previously described, the darts originally held only 0.4
ml of Sernylan, but the capacity was later increased to approximately
Demography of Howler Monkeys 211

0.6 ml. This enabled us to increase the injection to 60 mg, which reduced
the time between darting and capturing the animal (cf. " d o w n t i m e " o f
Scott et al., 1976).
After the animals had been captured, they were marked individually
in at least four ways. The most successful techniques were freeze-branding
for recognition at a distance and tattooing, ear-notching, and ear-tagging
for absolute identification of recaptured animals. For a branding iron,
we used a heavy curved piece o f brass extracted from the inner workings
o f a toilet. It was attached to a stick, dipped into liquid nitrogen, and ap-
plied to a shaved place on the tail for 25-30 sec. Brand widths of approx-
imately 3 cm seemed optimal. Narrower brands would become overgrown
and difficult to read. The hair usually grew in white and the brand was
then conspicuous for at least 5 years, perhaps for life. Some brands did not
take, for reasons obscure to us. Others gradually disappeared, probably
due to the reinvasion o f the area by melanocytes. Broader bands were
conspicuous, but seemed to cause the animal disproportionately more
trauma for about a week after branding. Freeze-branding caused the skin
to blister, but contrary to Scott et al. (1976), we never observed infection
or dipteran invasion in freeze-brands, although we have frequently seen
both in other wounds on Alouatta. The brands were placed on the tail in
patterns unique to each individual. Intervals between brands of 5, 10, 20,
and 30 cm were readily distinguishable from one another. Axillary tattoo-
ing, and ear-tagging are conventional techniques, and our procedures did
not differ from those described elsewhere (Thorington, 1981).
Collars were relatively unsuccessful for long-term observations o f
BCI howlers. Most leather or synthetic collars disappeared within 1 year.
Loss seemed to result from failure o f the fasteners rather than the material.
Collars fastened with broad-flange pop rivets lasted the longest. Stiff
collars o f other materials (e.g., polyurethane) caused sometimes fatal
abrasion and were exceedingly disliked by the animals. Ball-chain collars
of stainless steel with color-coded beads were most successful, although
even these were lost at a discomforting rate, especially by adult males,
which tend to have a greater neck than head circumference.
We obtained tooth casts from the anesthetized animals. The molds
were made with dental alginate in specially prepared plastic trays; they
were kept moist until the casts were made with dental stone within a few
hours. These casts were examined under low magnification and each tooth
on the right side of the mouth was given an ordinal score based on the
amount of wear (see Appendix 1). We summed these wear scores for the
distal two premolars and three molars o f the maxilla and mandible to
obtain a combined quantitative assessment o f dental wear for each in-
dividual. Longitudinal data from recaptured animals were used to cali-
brate the total wear scores in terms o f years (see Appendix 2). We used a
212 FroehHch, Thorington, and Otis

similar wear scale on the deciduous teeth of captured immature monkeys.

It was calibrated from eruption sequences and longitudinal observations
of known individuals (Altmann, 1959; Glander, 1975a; personal observa-
tions). Since this scale overlapped the scale of adult dental wear, we were
able to estimate the ages of all captured animals (see Appendix 2). By regres-
ing body weight against these age estimates, we obtained maturation curves
for both sexes.
We used the census data from seven contiguous troops to supplement
our small sample o f captured immature animals and to expand the sampled
adult age profile into a population pyramid for the entire northeast BCI
howler population, as it appeared in July 1976. For these censuses, the
relative ages of young animals were estimated on the basis o f size and
behavior, using Carpenter's (1934) categories, approximately calibrated
in years as shown in Appendix 2. It was assumed that half of each im-
mature cohort was male and half was female. This assumption was tested
on a total capture sample of 19 infants and young juveniles. There was no
significant sex difference (X~ = 0.61, P > 0.75, 2 df). Since howlers have
no distinct birth season, eight infants were added to the first cohort (ages
0-1 year) to account for neonates which had died during the 6 months
immediately prior to censusing. This correction was based on the infant
mortality recorded by Glander (1975a) in Costa Rica. Since prepubertal
males are often mistaken for adult females because of their genital mimicry,
we corrected our census data on the basis of the proportions (4:7) of
prepubertal males to young adult females in the 4.5- to 5.5-kg weight range
among our capture sample. The corrected census data showed an adult
sex ratio of 3:1 females older than 3 years to males older than 4 years.
Accordingly, the adult sex ratio in the population pyramid was adjusted
proportionately to the sampled age profile, in order to eliminate our capture
biases. For ease of interpretation, the age profile was standardized to
a population pyramid of 200 animals (plus the eight uncensused neonates),
which was close to the actual number of animals censused. An age profile
for the animals on Orchid Island Was similarly obtained by combining
census data and a 4007o capture sample.
From the age distribution of the sampled population, we modeled
a stable life table for BCI howlers. For this purpose, we assumed that the
birth rate was constant and that censused sex and relative age categories
were stable characteristics of the population. With repeated estimates at
a desk calculator, we smoothed the age-specific mortality rates to an even
gradient, keeping the modeled and actual adult survival curves (with
sexes combined) roughly equivalent and reaching 100~ mortality for the
last age indicated by our data. The low rate of population growth implicit
in our data was dismissed as negligible in these calculations. The modeled
life table was then tested for overall goodness of fit with the actual popula-
Demography of Howler Monkeys 213

tion pyramid by the Kolmogorov-Smirnov statistic (Siegel, 1956). Specific

cohort deviations from the model were tested by chi-square distributions.
For the latter test, the degrees of freedom were approximated by estimating
the number of parameters necessary to describe the survival curve.
A stable population model also assumes a stationary or constant
growth rate. Using the estimates of birth rates and average 4-year female
life span, we calculated the annual rate of population growth for both
the adult female and the adult male portions of the population, as a final
test of internal consistency for our model.

RESULTS

Maturation

The body weights of 56 immature and young adult animals are plotted
against estimated age in Fig. 2. These data include all young animals cap-
tured from 1973 to 1977, for whom dental casts were made. Some of these

I
8

7
:/ 9 0
0

0
6
o~ .....
0 0

5
/.
9 o ~

3
///
-- 2
o~

t- 1

Age (Yr) 1 2 3 5 6 7
Mates-- 9 Femates- -- - - o

Fig. 2. Weight maturation in Barro Colorado howlers, with male and female regression curves
superimposed on the raw data
214 Froehlich, Thorington, and Otis

individuals are omitted in subsequent analyses, either because they were

not alive in 1976 or because they were captured outside the primary study
area. The details of calibrating subadult ages and developmentai events,
such as tooth eruptions, are presented in Appendix 2. In general, infancy
ends with weaning at about 10-12 months. In slightly more than 1 additional
year of transition, the animal is indisputably an intermediate and indepen-
dent juvenile. Full dental maturity occurs at approximately 3 years, except
for the dimorphic and slowly occluding canine, and puberty soon follows,
with females primiparous at about 4 years. Males appear fully mature
and behave as such at 5 years. Both sexes achieve full adult body weight
between 5 and 6 years.
We have fitted maturation curves to these data by regressing weight
on age. The upper limit for each curve is the average young adult weight
(8.3 kg+for males and 6._1 kg for females). The growth curve for females
is quadratic, with dental wear scores (see Appendix 2), the square root
of the scores, and the square o f the scores used as predictors (r~ = 0.82).
Females show a smoothly decelerating growth trajectory, which ends
after most are primiparous.
The male data required a cubic regression for a comparable fit
(r~ = 0.90). The fourth term was the cube of the wear score. The male
growth curve is strikingly different from the female curve. It suggests that
males grow more rapidly than females during infancy. They then slow to
a moderate growth rate for about 2.5 years until puberty, when they gain
over 3 kg in 18 months. This is a marked adolescent growth spurt, com-
parable to that seen for both sexes in human growth (Tanner, 1962).
Comparing the two curves, it is easy to see why immature males are
frequently mistaken for young females.

Population Age Structure

The age profile of the subadult and adult animals captured in our
study area is shown in Fig. 3. It is based on 75 animals from seven con-
tiguous troops which inhabit Lutz Ravine, Fairchild Peninsula, and Gross
Peninsula. The age profiles in these three geographical regions were
relatively homogeneous (X2 = 4.1, P > 0.25, 3 dr). We have excluded the
animals from Orchid Island, because the age structure of that population
differed significantly from that of the BCI population. We also excluded
small samples from neighboring troops. Our data are standardized to
July 1976, including only animals known to have been alive then. The
figure reflects our sampling biases of avoiding females which were pregnant
or carrying young infants.
The oldest male in this sample is estimated to be 20.5 years of age;
the oldest female was approximately 19 years old. A slightly greater male
Demography of Howler Monkeys 215

F 171 -]
15
I I ....
I':
I.
11 J
F
I
7
J
F
F a I
h
<
54321 1 234.
Fig. 3. Age profile of captured adult and sub-
adult Barro Colorado howlers (N = 75). t~ Number O~C~

longevity is also suggested by the numbers of each sex older than 15 years.
Among the sexually mature animals (females more than 3 years of age,
males more than 4), about one-half are more than I0 years old and one-
fourth are more than 13 years.
The age profile in Fig. 3 is not smooth; there are striking cohort
fluctuations, particularly for males. For example, there are too few animals
between the estimated ages of 7 and 8.5 years. We think these fluctuations
in cohort numbers are real phenomena, not sampling artifacts. They are
tested for significance and discussed below.
Census data from the seven contiguous troops on BCI are shown
in Table I. They represent actual counts, without "Lincoln index" ex-
trapolations from the ratios of marked to unmarked individuals. Again,
a test of homogeneity (X2 --- 1.03, P > 0.9, 4 df) allowed us to pool these
data. Combining the data from Table I and Fig. 3, we approximated the
age profile for the whole population in Fig. 4. qlae separated blocks
represent the census adjustments described above. With 83 adult females
216 Froehlich, Thorington, and Otis

Table I. Census Data in Percentage from Three Contiguous Geographical Regions on BCI
and from Orchid Islanda

Females Total
Census category Males and J3 J2 J1/I3 I2/I1 sample
Estimate age (years) 5+ 3+ 2 1 0
Geographical area on 13(31
Lutz Ravine 16.7 41.7 16.7 12.5 12.5 48
Fairchild Point 15.3 54.2 4.2 9.7 16.7 72
Gross Point 15.7 48.0 6.9 11.8 17.6 102
Orchid Island 26.9 53.8 0 11.5 7.7 26

aSamples include only animals actually seen; age estimates are discussed in Appendix 2.

and 40 infants less than 1 year of age, this figure suggests an annual re-
productive rate o f 0.48 offspring per adult female per year, which is similar
to the rate o f 0.53 documented for howlers in Costa Rica (cf. Glander,
1980).

Stable Population Model

Table II is an abbreviated life table, abstracted from the above census

and capture data. It is based on a stable population model, assuming
constant birth and mortality rates for the years since the oldest animal
was born (Deevey, 1947). Since the population is nearly stationary (see
below), adjustments for the small growth rate were negligible. This modeled
age profile is superimposed on Fig. 4. We assumed that infant mortality
is highest among the youngest animals and then decreases rapidly, as
seems best to fit our census data. We deduced from the extrapolated
population pyramid (Fig. 4) that immature male mortality is highest at
puberty (from 3.5 to 5 years). Finally, we assumed for adults that mortality
rates would smoothly accelerate with age, without yearly fluctuations, and
a stable population model best fit the adult age profile when we assumed
mortality rates below 1% during early adulthood.
The overall fit between the abstracted life table and the actual den-
tally aged data base is compared in the last two columns o f Table II.
Here we present both actual and modeled adult survival rates. With a
maximum deviation (K) o f 0.095 for age 7 years, the overall fit o f the two
curves falls well within the criterion defined by Kolmogorov and Smirnov
( f o r N = 17 and P < 0.05, K -- 0.32; Siegel, 1956). Put another way, an N
of 205 would be necessary for a K of 0.095 to be significant.
Figure 5 portrays age-specific mortality rates, based on the modeled
life table. It shows that mortality is quite high for the young o f both sexes,
but that subadult males suffer a much higher mortality than young adult
Demography of Howler Monkeys 217

20 16 12 8 4 .< 4 8 12 16 20

~ Number O~C~

Fig. 4. Population pyramid for howler monkeys on north-

east Barro Colorado Island in 1976. Separated boxes indicate
estimates and adjustments as discussed in the text. Super-
imposed dots denote extrapolated stable population.

females, leading to an observed 3:1 adult sex ratio. Between birth a n d

age 5 years, 88~ o f the males and 65% o f the females die. At maturity,
mortality rates level o f f and are virtually equal for both sexes. However,
our data suggest slightly greater mortality rates for older females t h a n
for males o f the same ages, leading to a slightly greater male longevity.
These suggested sex differences in longevity are also shown in the
survival curve in Fig. 6, plotted on a log scale. After the sharp reduction
of males between 3 and 5 years, the two survival curves are parallel and
virtually level for several years. The female curve, however, begins to
decline earlier and faster than the male curve, overtaking the latter at
19 years. Based on a hypothetical initial cohort o f 1000, these curves
project that the m a x i m u m life span is about 22 years in females and 23
years in males. In terms o f life expectancy at age 5 years, our data suggest
16.6 years for males but only 15.5 for females. Moreover, a m o n g 12- to
16-year animals, we captured two females for every male, but a m o n g
animals older than 16 years, the sex ratio o f our sample was reversed
218 Froehlich, ThoHngton, and Otis

0 ~

0 0 ~ 0 0 0 0 o o 0 0 0 0 0 0 0 0 0 0 0 ~

e~
i)

~-~

N ~'~

i o

~o

or,.)

,r

o
Demography of Howler Monkeys 219

IOO0 I
l
900 I
I
800 I
I
?O0 I
I
600 I

500

~--~ ~oo
80
300

,'," 200
..,=
.20 IO0

Age 2 4 6 8 10 12 14 16 18 20

Holes - - ; Females -- --

Fig. 5. Age- and sex-specific mortality rates in Barro Colorado

howlers

1000

-.g
o
\
~o

C
v_
o

o
o
o
1C
r,

u1
Age 2 /. 6 8 10 12 1/, 16 18 20 22
Hales - - = Females - - - -

Fig. 6. Male and female survival curves in Barro Colorado howlers, plotted
on a log scale.
220 Froehlich, Thorington, and Otis

(1 female:2.5 males). The binomial probability is 0.04 that the older sample
was drawn f r o m a population with a sex ratio o f two females to one male,
which tends to support our suggestion that adult males m a y outlive females.

Deviations from Demographic Stability

As noted above, we consider the deficit o f animals aged 7 years to be

a real p h e n o m e n o n , not a sampling artifact. In terms o f the actual dental
wear scores (see A p p e n d i x 2), this deficit is even m o r e striking, with only
one female f r o m 36 to 44 units (an interval o f 1.8 years) and two males
f r o m 40 to 47 (1.6 years). The significance of this obvious paucity o f
animals aged 7 years was appraised using a chi-square c o m p a r i s o n between
the sampled age distributions and the expectations based on the modeled
life table. Table I I I presents this comparison for eight adult age classes,
with the sexes combined. The chi-square contributions f r o m each age class
are also shown in the table. In this analysis, it is difficult to estimate the
degrees o f freedom, but a total chi-square of 11.7 would be significant
at the 5070 level with a df o f 5. Since the expected values are based on a
complex survival curve, for which the mortality curves in Fig. 5 are equiv-
alent to differential functions, m o r e than a cubic regression would be
required to describe the modeled population, thus leaving us with only
4 degrees o f freedom. Moreover, the two distinctive adjacent cells have
a total chi-square o f 10.0 and a significance at the 0. 1% level, with 1 degree
o f freedom. Although the K o l m o g o r o v - S m i r n o v statistic confirms the
overall fit o f the actual and modeled age distributions, the chi-square test
is significant because o f these two adjacent age classes. There is a paucity

Table III. Nonparametric Comparison Between Actual

Adult Population Pyramid Cohorts and Predictions from
a Stable Population Model a
Cohort size
Contribution
Age(s) Actual Predicted to chi-square
4 6 7.83 0.43
5-6 20 11.52 6.24
7 1 5.60 3.78
8-9 9 11.05 0.38
10-12 17 15.97 0.07
13 3 4.81 0.68
14 5 4.31 0.11
15-20 11 11.30 0.01
Total 72 72.39 11.70
aThe sexes are combined and adjacent cohorts which
deviated in the same direction have been pooled.
Demography of Howler Monkeys 121

of animals aged 7 years and a plethora o f 5- and 6-year animals in our

sample. We conclude that there was some extrinsic factor in the past which
virtually eliminated the 7-year cohort.
The extreme fluctuations in male cohort sizes were similarly tested in
Table IV. The total chi-square o f 10.1 would be significant at 4 degrees
o f freedom. By logic similar to that o f the previous analysis, fewer degrees
o f freedom seem warranted. Moreover, the four middle cells are significant
with 3 degrees o f freedom. In this case, the contributions to the overall
chi-square are spread out over several cells. The reality o f an oscillating
trend in the table is confirmed by the individual contributions of neigh-
boring cells. Thus, it appears that the fluctuation o f male cohort sizes is
a real phenomenon, not strictly a function o f sampling.
Finally, we examined the ages of adult males within each troop in
1976 (Fig. 7). Some of the troops seem to have an age-graded series o f
males as hypothesized by Eisenberg et al. (1972), but in other troops
(e.g., 3, 7, and 14) there are subgroups o f males with very similar ages.
The statistical significance of these clusters of similar-aged animals was
tested by comparison with randomly aged male groups, generated (with
25 repetitions) from the age structure of the whole male population. In
the four troops bounded by two or more other troops (i.e., not isolated by
water), there are more age clusters o f animals within 0.5 year of each other
than would be expected if the males were randomly assorted among troops
(X~ = 11.2, P < 0.001, 1 df). Also, five apparently young adult males were
observed by Otis to have taken over troop 7 between 1976 and 1977. Two
were captured and found to be less than 1 year apart in age. By 1978,
only three remained and some o f the former troop males had returned.
These data suggest that age-mate coalitions have higher adult recruitment
rates than solitary males, successfully entering new troops by cooperation.

Table IV. Nonparametric Comparison Between Actual

Male Cohorts and Predictions from a Stable Population
Model, Using Collapsed Age Classesa
Cohort size
Contribution to
Age(s) Actual Predicted chi-square
8-9 3 4.5 O.5O
10-11 7 4.4 1.54
12-13 2 4.1 1.08
14 4 1.9 2.32
15-16 0 3-1 3.10
17-20 5 2.9 1.52
Total 21 20.9 10.06
aSee Kempthorne (1967) for justification of small
expected cell sizes.
222 Froehlich, Thorington, and Otis

100 0

90

80

70
0

~e0 0
0
0 0

50
o 0
u
u) l.O
(p
o
~:30 o
"6
| 20 0 Fig. 7. Age distribution of captured subadult
O
and adult male howlers within troops. See
Troop 13 2 7 14 3 5 Table AI for yearly age equivalences.

Population Growth

The stable population model used in the above analysis does not
necessarily imply a static population, but rather one in which the growth
rate is constant, in balance with natality and mortality (Cox, 1976). In
fact, our model implies an annual growth rate of slightly over 1.5~ for
the howler population of BCI. We derived this figure by combining the
life expectancy of 11.3 years for 4-year-old females with an annual birth
rate of 0.48 to produce a lifetime average female productivity of 6.42,
adding the first born at age 4 years. If half of these infants are females
with a survival rate to age 4 years of 0.37, then 1.19 females are recruited
by each adult female during her reproductive years. From these figures,
a female recruitment rate of 0.017 adult per year can be used as an estimated
growth rate for the population as a whole. A similar analysis for males
recruited at age 5 years gives an almost identical estimate (0.016) for every
three adult females.
The 1976 age profile of howler monkeys on BCI contrasted with
that on nearby Orchid Island, as shown in Fig. 8 (X~ = 26, P < 0.001, 2 df).
Orchid is a small island (16 ha) where the population appears to be severely
food-limited (Froehlich et al., 1981). With 50% of the population over 13
years, the age profile suggests that infant survival and the recruitment of
juveniles into the adult population had been extremely low during the
preceding decade. If this age profile is typical of carrying capacity in
Demography of Howler Monkeys 223

C
18
16

E 1/.
12
10
8
6
4
2
II I
Fig. 8. Age profile of captured and censused howlers on Orchid
Island. Each square represents one individual. ~" ~ ' <dd'

Alouatta, then the slowly expanding BCI population cannot be considered

similarly constrained.

DISCUSSION

Maturation

Our data show that howler monkeys grow rapidly, in contrast with
other large monkeys, such as macaques (Dittus, 1977; Tanner, 1962) and
spider monkeys (Eisenberg, 1976). This result is corroborated by our own
and other longitudinal observations of Alouatta, as described in Appendix
2; but they disagree with the maturation estimates of Malinow (1968) and
Carpenter (1965).
In the work of Malinow (1968) several investigators reported that
Alouatta caraya both matures later and dies earlier than we suggest for
A. palliata. In the basic study, Rosenthal (1968) used the dental strontium-
90 content to estimate age, relative to the known period of radioactive
fallout in Argentina. However, his results lead to several inconsistencies
in the companion reports. Moreover, they are in disagreement with Shoe-
maker's (1979) data from a captive colony of A. caraya. Pope's (1968)
ordinal data on tooth wear are similar to ours, except that she calibrated
them according to the strontium-90 scale. We find suspiciously low cor-
relations between her relative adult ages and the absolute ages estimated
by strontium-90 content (r = 0.24 for males, 0.37 for females). When we
224 Froehlich, Thorington, and Otis

analyzed Pope's (1968) age profile, based on the strontium-90 estimates

of reproductive age and longevity, we calculated a population recruitment
rate o f - 7 % per year, which we consider extremely unlikely. Thus, we
believe that the strontium-90 age calibration is inaccurate. Consequently,
the developmental data presented by Stahl et al. (1968) were biased by
overestimating young ages. Indeed, the body weights at which ontogenetic
events occurred in their analysis are similar to ours; only the time scales
are different.
Carpenter (1965) changed his maturational age estimates from those
of his earlier study (1934). Some of these earlier age estimates are similar
to ours. Presumably without any additional longitudinal data, he was at-
tempting to bring his earlier estimates into accord with those for other,
well-documented primates. Instead, we conclude that Alouatta maturation
rates are more rapid than might be predicted on the basis of phylogeny or
body weight.
We suspect that this rapid maturation is generally related to the
predominantly leaf diet of Alouatta. The high protein content and low
caloric foraging cost of young leaves may be conducive to rapid growth.
Also, we speculate that toxin tolerance (Glander, 1975b) may favor rapid
physiological maturation in newly weaned animals. In an unpublished study,
Froehlich has also found early cranial suture closure in Alouatta, ap-
parently in response to the stresses of extensive leaf mastication. It is
conceivable that these early ontogenetic events may be associated with
other accelerated maturational processes. However, we also acknowledge
that early sexual maturation may be a poorly understood, evolved feature
of Alouatta, rather than a proximate consequence of its diet.
It is clear from our maturation analyses that only male howler
monkeys have a postpubertal growth spurt, when females may already be
gravid. Crude growth curves in the toque monkey (Dittus, 1977) suggest
a similar, but less striking sex difference. Previously, adolescent growth
spurts have been documented for both sexes in humans, and in captive
chimpanzees and rhesus macaques (Tanner, 1962). In the nonhuman
primates, the process was much more pronounced in males. The present
study is the first documentation of a male growth spurt in a wild, neo-
tropical primate population. Tanner (1962) remarked that the differential
weight gain in male macaques was primarily in shoulder breadth and
muscle mass. Our data on sexual dimorphism similarly suggest differential
growth in limb lengths.
It has been argued, however, that the adolescent growth spurt is a
uniquely human characteristic; that sexual dimorphism of macaques
develops during prolonged, rather than more rapid growth in males
(Gavan and Swindler, 1966). Tanner (1962), however, noted the link
between sexual dimorphism and differential adolescent growth rates.
Demography of Howler Monkeys 225

Our weight data and longitudinal observations of postpubertal males

support the latter view. Both howler sexes grow into the sixth year, with
the more rapid adolescent male growth and possibly also the constraints of
early female pregnancy (Rowell, 1972) being the essential proximate causes
of adult size differences associated with sexual dimorphism.

Longevity

Our estimates of maximum howler life span are in disagreement with

the conclusions of Rosenthal (1968) and Stahl et al. (1968), which we have
discounted above. Based on strontium-90, they concluded that no in-
dividual in their sample of 314 Alouatta caraya was older than 12-13 years.
Our estimates, however, are supported by Glander's (1980) documentation
of A. palliata over 15 years of age in his Costa Rican study and by our
data on "Scar-lip." This distinctive male was initially observed as an
adult in 1967 by Chivers (see Richard, 1970), suggesting that he was born
prior to 1962. We captured him in 1973 and 1978, estimating his age by
tooth wear at 17 years when he was recaptured and implying his birth in
1961. He was still alive and well in July 1979, at an estimated age of 18.5
years. We do not think that A . caraya is significantly shorter-lived than
A . palliata. Indeed, Pope's (1968) description of tooth wear in the former
suggests to us that some of these animals were 15 to 20 years old. Thus,
we conclude that the strontium-90 system (Rosenthal, 1968) seriously
underestimated the ages of old animals. There are few data available to
test whether we are also underestimating the longevity of Alouatta. How-
ever, the 21 animals captured in 1973 all tested negative for yellow-fever
antibodies, implying that none was alive 24 years earlier during an epidemic
on BCI (Collias and Southwick, 1952).
Although sparse and confounded by capture biases and the dif-
ferential cohort survival of males (Table IV), our capture data on old
animals indicate that life expectancy at age 5 years is greater for males than
females. Glander's (1980) data on Costa Rican animals over 16 years
suggest the same conclusion, but the equally small, cadaver sample from
BCI of Otis et aL (1981) contained only females over 15 years. If males
do survive longer, this is unexpected on theoretical grounds (see review
by Ralls et al., 1980), but it is perhaps understandable in terms of howler
social structure. Males usually must fight and/or migrate to achieve social
acceptance as adults. Consequently, they suffer a high subadult mortality
(see below). Subsequent to this strong selective filter, a male's status may
be secure and long lived. Aggression toward outsiders (i.e., potential
male recruits) may be shared by all experienced troop males and thereby
less risky to each individual than to the challenging male(s). For females,
226 Froehlich, Thorington, and Otis

however, there may be cumulative negative effects from their subordinate

status and continuous reproductive activity.

Differential Subaduit Male Mortality

We conclude that there is a high rate of mortality among subadult

males. This is based on three asumptions: (1) the sex ratio at birth is close
to equality; (2) the disappearance of males is not due to emigration; and
(3) the absent males are not living solitary existences between troops.
The first assumption, that the sex ratio is approximately 1:1 at
birth, is highly probable on theoretical grounds (Leigh, 1970). Glander
(1980) found that the neonatal sex ratio in his Costa Rican study did not
differ significantly from 1:1 (15 males, 9 females, and 7 unknown). Among
19 prepubertal animals, we also found a nearly equal sex ratio, as reported
above.
The second assumption, that disappearancesare not due to emigration,
is always difficult to demonstrate, as discussed by Caughley (1966), Deevey
(1947), and Dittus (1977). Since our study area encompasses two peninsulas
on the northeast corner of an island, however, undetected emigration
could occur only to the west and south. Water is a relatively impassable
boundary, because howler monkeys rarely swim. As noted earlier and
elsewhere (Froehlich and Thorington, 1982; Thorington et al., 1982), we
have adduced evidence that the older parts of the forest to the southwest
offer a more favorable habitat for Alouatta, that the peninsulas have been
colonized more recently than the old forest on BCI, and that gene flow has
been and probably continues to be from the more central parts to the more
peripheral parts of the island. Therefore, we suspect that male immigration
into our study area slightly exceeds emigration. We have no reason to
suspect that emigration is greater than immigration.
The third assumption is that undetected solitary males do not account
for a significant number of the missing animals. Carpenter (1934), for
example, thought that the "complemental" males partially explained the
adult sex ratio. In order to bring the adult sex ratio to 1:1, however, there
would need to be two solitary males for each one in a troop. This is highly
improbable, as there would then be nearly 500 of them on BCI. Although
we located solitary males infrequently, we found the same ones repeatedly.
Accordingly, we do not think that there were many undetected solitary
males in our study area.
If these assumptions are accepted, there must be a high mortality
rate among subadult males, which results in the biased adult sex ratio.
In an analysis o f the age at death of BCI Alouatta cadavers and skel-
etons, Otis et al. (1981) reported a disproportionate number of young
Demographyof HowlerMonkeys 227

males, approximately 5 to 7 years old. Their age estimates often were

based on only a couple of remaining teeth and cannot be considered as
precise as those of the present study. Nevertheless, this demographically
important and independent source of mortality data (see Caughley, 1966)
corroborates our conclusion of a high subadult male mortality.
Although death is almost never actually observed, we suspect that the
high mortality rate for subadult males results from a combination of
social, developmental, and nutritional factors. Otis et aL (1981) and Young
(1981) have documented cases of adult male aggression toward subadults,
some of which resulted in fatal injuries. It is likely that such aggression
frequently leads to the exclusion of young males from their natal troops.
This often coincides with the adolescent growth spurt, when young males
have high nutritional needs. Widdowson (1976) has found that male mam-
mals are more vulnerable to starvation than females, especially at puberty
when androgens act anabolically and limit available energy. Similarly,
Case (1978) views higher mortality in the more rapidly growing sex as a
generality in mammals. Thus, when their needs are greatest, young males
may be subject to ostracism and consequential exclusion from the best
sources of food. It is also possible that these young animals still have in-
adequate detoxifying mechanisms (Glander, 1975a, b; 1977) and insuf-
ficient foraging experience for a marginal diet. Thus, we hypothesize that
the proximate cause for increased subadult male mortality is an inadequate
diet, ultimately caused or potentiated by adult male aggression.

Factors Disturbing Demographic Stability

In the adult age profile (Fig. 3), there are significant fluctuations
in cohort sizes. We do not believe that there are variations of this magni-
tude in the annual birth rates. Rather, there is suggestive evidence for
variations in juvenile mortality, dependent upon extreme oscillations in
environmental factors. Foster (1973) noted a chain of events in 1970, when
extremely heavy rains during the early dry season affected flower pollina-
tion adversely, leading to a failure of the wet-season fruit crop and causing
a high mammalian mortality. We hypothesize that young juvenile howlers
were severely stressed by these events, with a high mortality of the newly
weaned, 1-year-old animals resulting in the underrepresentation of the 7-
year cohort in 1976. We believe that animals with an inadequate toxin
tolerance would be most affected by this fruit collapse; they could not
cope with a nearly total leaf diet in the latter part of the wet season, when
food is normally most scarce (Carpenter, 1934).
A similar nutritional explanation may apply to the relative paucity
or total absence of some male cohorts in the 1976 age profile. The reduction
228 Froehlich, Thorington, and Otis

of the 8- to 9-year cohort may have occurred when it was 2-3 years old
during the 1970 bottleneck. Reviewing the BCI rainfall records, we found
that 1963 was the only other year in the last 20 with comparably heavy
dry-season rainfall. This might explain the absence of 15- to 16-year-old
males in 1976, who would have been 2-3 years in 1963. We hypothesize that
young males may be more vulnerable to food shortages because they have
greater maternal independence and lower social status than their female
age-mates. It is also probable that aggressive ostracism by adult males
increases during bad years and possibly extends to the prepubertal males,
even though the latter mimic females in their genitalia.
The correlation between rainfall cycles and male cohort sizes is not
perfect; for example, there is no recognizable environmental event to ex-
plain the deficit of 13-year males in 1976. However, the hypothesized link
between rainfall and juvenile mortality is adequate to explain most signifi-
cant deviations between the observed age profile and that modeled for a
stable population. Furthermore, for males there is another reasonable
hypothesis to explain cohort fluctuations, i.e., there could be annual dif-
ferences in adult recruitment rates. This is not an alternative hypothesis,
because we might expect compensatory recruitment following years of
high juvenile mortality. The age profile of 5- to 6-year animals in 1976
suggests such an effect.
Moreover, the age distribution of males within troops (Fig. 7) suggests
that two or three males of closely similar ages may enter a troop at the
same time. Since stable all-male bands have never been reported in Alouatta,
we envision this event as the recruitment of a coalition of males, probably
derived from the same natal troops. Thus, we hypothesize that these males
are at least moderately related, with mutually supporting bonds developed
during juvenile play. Similar "kin selection" or "reciprocal altruism"
arguments have been advanced by Bertram (1976) for lions, Bygott (1979)
for chimps, Kurland (1977) for macaques, and Ligon (1978) for green
woodhoopoes.
Although these social and environmental factors disturb the age
profile away from the expectations of a stable population model, we still
view the latter as a useful heuristic device for evaluating the viability (c.f.
Heltne et al., 1976) and growth characteristics of a population for conser-
vation management decisions. Moreover, in a long-lived animal with no
distinct birth season (Caughley, 1966), stability may be approximated
by averaging the negative disruptions with positive factors (Deevey, 1947).
The relatively high survival rates of the cohorts following the 1970 fruit
failure may be an example of such balancing.
Demography of Howler Monkeys 229

Population Growth and Regulation

By assuming an approximately stable population, we find that the

current annual growth rate of BCI howler monkeys is about 1.5070. This is
markedly lower than the 16.7070 rate estimated for 1951-1959, following
the yellow-fever epidemic. For the next 8 years, Smith (1977) estimated
a reduced annual rate of appoximately 4~ Thus, the population is
gradually approaching a stationary equilibrium, but it continues to increase
at a moderately low rate.
The increased juvenile mortality during adverse climatic years sug-
gests that the growth rate decline has a nutritional component. However,
the age structure and general physical condition of animals on Orchid
Island in 1976 were very different from those of animals on BCI. Male
weight, for example, was 2007o lighter on Orchid Island than in the Lutz
Ravine of BCI (Froehlich et al., 1982). With virtually no recruitment of
juveniles and a subequal adult sex ratio, the Orchid population appears
to be at the small island's carrying capacity. By contrast, less drastic
factors are necessary to account for the apparent population regulation
on BCI.
Data from western Panam~t demonstrate that howlers can exist at
much higher densities than on BCI, at least temporarily, without signs of
habitat depletion or increased intertroop aggression (Baldwin and Baldwin,
1972). Thus, howler populations do not appear to be regulated by the social
effects of crowding. Dittus (1975) reached a similar conclusion in com-
parisons between provisioned and wild macaques. Moreover, our ob-
servations on BCI in recent years suggest that density, intertroop famil-
iarity, and social tolerance are positively correlated.
Under intermittent conditions of nutritional stress, however, toler-
ance may decrease within social groups. Our data indicate that l-year
females and 1- to 3-year males suffer a high mortality during nutritionally
poor years. This increased mortality is best explained by the social ex-
clusion of juveniles from optimal foods, compounded by their lack of
experience and intolerance of leaf toxins. Dittus (1975) reached a similar
conclusion for toque monkeys during an exceptionally dry year. Thus,
we hypothesize that howler monkey populations are limited by a mechanism
of status-determined, differential access to cyclically limited food re-
sources, within stable social groups. We believe that the estimated fe-
cundity rate of approximately 50070 has remained relatively constant,
while a periodically increased mortality of immature animals has slowed
the annual rate of population increase.
230 Froehlich, Thorington, and Otis

APPENDIX 1: DENTAL-WEAR SCALES

As follows, the ordinal tooth-wear scales ranged from 1 to 12, from a

tooth in occlusion with little discernible wear to a tooth with no occlusal
enamel. These scales were developed by initially placing a series of dental
casts in a subjective sequence of least to most worn, describing them in
terms of ordinal changes on each cusp, and then standardizing the scales
for consistency between two observers.

Teeth Score Description

p~ ,, 1 Occluding, with barely discernible wear facets

2 Buccal cusp with pitted enamel
3 Buccal pit extended by longitudinal wear facet
4 Buccal groove into dentine, with lingual pits
5 Buccal and lingual grooves coequal
6 Major grooves, with lingual broader
7 Deep grooves, turning mesial and distal margins
8 Distal margin of buccal cusp deeply worn, often
with grooves joining along distal margin
9 Entire distal margin deeply worn
10 Longitudinal enamel "island" in middle of tooth
11 Enamel island divided along transverse ridge
12 No occlusal enamel; deeply worn, especially on
distal margin
P3 ~4 1 Occluding, with slight facets
2 Small pit on buccal cusp
3 Large pit
4 Large pit, with wear facet on talonid basin
5 Small buccal groove, with lingual pit
6 Major buccal groove, large lingual pit, and ex-
exposed talonid dentine
Large buccal groove extending around mesial
margin; talonid with reduced enamel
Buccal and lingual grooves join, leaving partial
transverse enamel islands
9 Talonid and buccal grooves deeply joined
10 Deep wear, with small enamel ridge along lingual
margin
11 Deep wear, with enamel ring around entire tooth
12 Worn below and through enamel ring
Demography of Howler Monkeys 231

Teeth Score Description

M t ,2,3 1 Occluding, with slight facets

2 Small pits on lingual cusps (buccal on M~)
3 Small lingual groove; pits on buccal cusps
4 Moderate lingual goove; large buccal pits
5 Major lingual groove; large buccal pits
6 Deep lingual groove, with tendency for buccal
"grooves"
Deep lingual groove, with large round holes in
buccal cusps
8 Grooves joined on distal and mesial margins
9 Deep wear over one-third of lingual margin
10 Deep wear over one-half of tooth
11 Deep wear of entire tooth, with small enamel
islands
12 No occlusal surface enamel; dentine concave
M! ,2,3 1 Occluding, with slight facets
2 Wear pits only on buccal cusps
3 Buccal and lingual wear pits
4 Small buccal grooves
5 Major buccal grooves; large lingual pits
6 Major buccal grooves; small lingual groove
7 Buccal and lingual grooves join mesially
8 Deep buccal groove joined to lingoal
9 Deep grooves joined, isolating talonid enamel
islands
10 Small enamel islands
11 No occlusal surface enamel; dentine flat or convex
12 Dentine worn concavely

APPENDIX 2: CALIBRATION OF TOOTH-WEAR SCORES

The same wear scales were used twice--once for the deciduous teeth
and the other for the permanent. Since the first and second permanent
molars erupt before the deciduous molars are replaced, we were able to
score some individuals for dental wear on both scales. The two scales were
also highly correlated (r = 0.94). Thus, we were able to estimate all sub-
adult ages by aligning the scales as follows:
232 Froehlich, Thorington, and Otis

Wear score for Wear score for

6 deciduous 10 permanent
cheek teeth cheek teeth Comments

6-10 1-2 First permanent molar occluding

26-39 5-6 First molar showing initial wear
12-16 Deciduous teeth all replaced,
with canine just erupting and
upper third molar not yet
occluding
20-25 Full permanent dentition, but
canines not in full occlusion

The tooth-wear scores were calibrated in years from longitudinal

data. We recaptured nine animals and obtained two tooth casts from each.
The time intervals between first and second captures ranged from 1 to 5
years. The wear score for permanent teeth changed at a rate of 5.1 points
per year (range, 3.6-8.5; SD, 1.7; median, 4.2). This distribution was
skewed because young males wear their teeth more rapidly than other
animals. Accordingly, we used 5 to 8 points per year for juvenile and
subadult animals, depending on sex, and 5 points per year for adults. The
faster wear rate of immature males is supported by the fact that at maturity
they weigh 50% more than females, but have only 7.5% more occlusal
surface area on their molars.
Our tooth-wear age estimates are corroborated by longitudinal
observations and are aligned in Table A1 with Carpenter's (1934) age cate-
gories and with maturational events. Altmann (1959) established that the
infant 1 (I1) stage, defined by ventral transport, lasted less than 1 month.
Our observations agree with this assessment. Carpenter's 12 and 13 stages
are distinguished by color, size, and degree of independence of the infant
from its mother. Infancy is terminated by weaning, which is normally
recognized in censusing by independent progression. We marked three
young infants and observed that they became independent and weaned
juveniles within 1 year. In one case, a 15-month female migrated to a neigh-
boring troop without her mother. Four authors (Glander, 1975a; Neville,
1972; Shoemaker, 1979; Smith, 1977) have also concluded that weaning
occurs before 1 year of age.
We estimate that the juvenile stages last for 2-3 years, as did Neville
(1972) for Alouatta seniculus. Glander's (1980) longitudinal data on A.
palliata in Costa Rica show that the testes of males may start descending
at approximately 3 years o f age and that a female may bear her first infant
 Demography of Howler Monkeys 233

~g
-E
0

d 0

~g

"~'~ I:1 ,, ,I , i ('4

I
I i
~o <~ ..o ~ "t::A

I I I~
e-,

! , i
g
! u i I

I I !
o

r,.)
s

.<
[ I t 1 I t I '~

o~

[..,
234 Froehlich, Thorington, and Otis

at 43 months o f age. In two of our marked males, we have observed the

transition f r o m prepubertal or early pubertal stages, with the testes just
descending, to young adult males in l year and fully mature males in 1 ad-
ditional year. We therefore show in the Table A1 that females are mature
by 4 years o f age, and males by 5. These ages are similar to those reported
for captive A . caraya by Shoemaker (1979).
Our interpretation o f Carpenter's age categories in Table A1 dif-
fers f r o m the set o f age categories reported b y Glander (1980), whose
purpose was to estimate the birth m o n t h f r o m precise first year cate-
gories. Our purpose, instead was to facilitate age estimates f r o m cen-
susing (see Table I). The I3/J1 distinction is difficult because o f the
animal's transitional activities; consequently, we have overlapped these
stages. For a p p r o x i m a t e age estimates in censusing, we have used the
11 and 12 stages for the first year, 13 and J1 for the second, and J2 for
the third. The J3 stage has been reserved for subadult males, who are
indistinguishable f r o m nulliparous adult females until their testes descend.
The J3 stage extends until the animal appears and behaves as an adult
male.

ACKNOWLEDGMENTS

Support was provided by the Smithsonian Environmental Science

P r o g r a m , the University o f New Mexico Research Allocations Committee,
and Sigma Xi Grants-in-Aid o f Research. We are grateful to the Smith-
sonian Tropical Research Institute for the assistance of the staff, to m a n y
of our colleagues and students who have assisted us, particularly Drs.
N o r m a n Scott, Peter W o r k m a n , and Stan Rand, and especially to Lee
Benshoof and Drs. Wolfgang Dittus, H e n r y Harpending, and Larry
Heaney for comments on the text.

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