Professional Documents
Culture Documents
Received for publication January 27, 1994; revision accepted July 19, 1994.
Address reprint requests to Linda Marie Fedigan, Department of Anthropology, University of Alberta,
Edmonton, Alberta, Canada, T6G 254.
- --.Q..-
Rainfall (m)
Capuchins
-
----A-- Spiders
Howlers
3-01
2.5 -
2.0 -
1.5-
1.0-
0.0 : I I I I 1 I I I
1984 1985 1986 1987 1988 1989 1990 1991
Year
Fig. 1. Annual rainfall (in meters) and birthrate in subsequent year for capuchins, howlers, and spider mon-
keys.
14 I Fedigan and Rose
100
DlySeason
Wetseason
80
60
40
20
0
Capuchins Howlers Spiders
Fig. 2. Births during dry season (December through May) and wet season (June through November) at Santa
Rosa National Park, Costa Rica, 1985-1993. Only births to known mothers on known dates are included.
Capuchins: n = 22; Howlers: n = 31, Spiders: n = 18.
gestation. Unfortunately, neither the field conditions of the present study, nor our
knowledge of the reproductive biology of captive neotropical cebids [e.g. Nagle and
Denari, 19821 allowed us to reliably separate the early lactation (and presumably
anovulatory) phase from the cycling phase of the IBI as has been done for baboons
[Altmann et al., 1978; Smuts & Nicholson, 19891; but see some information on
howler gestation and lactation in Crockett & Sekulic [1982], Crockett and Rudran
[1987al, and Glander [19801. However, it was possible to roughly divide the mean
IBI lengths found in this study into gestation versus lactation-cycling phases.
Figure 3 shows that although howlers have the shortest absolute IBI of the three
species, they devote the largest proportion of their IBIS to gestation: 31% as com-
pared to 20% and 22% in capuchins and spiders. If body size should predict relative
IBI length, these findings suggest that the apparent “reversal” of capuchin and
howler IBI values is not due to gestation length, but due to the lactation/cycling
phases of the cycle.
To further test this idea, we compared our capuchin and howler values for
gestation length, and lactationlcycling lengths to values published for other pri-
mates [see Table 16-1 in Harvey et al., 19871. Using T-tests [single observation
against the mean of a sample, Sokal & Rohlf, 19811, we determined that howlers
are not significantly different in gestation or lactationlcycling lengths from other
primate species of similar adult female body size, adult brain size, neonatal size, or
adult braidbody ratio (Table 111). Similarly, capuchin gestation length is not sig-
nificantly different from gestation lengths given for other primate species of sim-
ilar body size, brain size, neonatal size, or braidbody ratio. However, the capuchin
lactation/cycling phase is significantly longer than that of other primate species of
similar body size (T = 3.081, P = .05), brain size (T = 3.414, P = 0.05), neonatal
size (T = 3.858, P = 0.021, and braidbody ratio (T = 6.242, P = 0.01). This
16 / Fedigan and Rose
Lactation - Cycling
Alouaftu puUiata (5.7 kilos)
Gestation
!
Anovul.
13.7 19.9
I Lactation - Cycling
Ateles geo.ffroyyi(6.5 kilos)
Gestation
22 %
/Months 0 27.1 34.7
Fig. 3. The characteristic interhirth interval and its component phases in capuchins, howlers, and spidc
monkeys.
suggests t h a t capuchins are slow for their body size with respect to the lactation/
cycling phase of the IBI.
DISCUSSION
In this study we found no significant differences in IBI lengths that were at-
tributable to individual differences in the age, parity, weight, or rank of the moth-
ers. It is possible that these variables, often identified in the literature as proxi-
mate causal factors in IBI length, are not operating in the life histories of this
study sample of capuchins, howlers, and spider monkeys; however, we were only
able to test for weight relationships in two of the three species and a relationship
between IBIS and dominance in one of the three. It is also possible that, despite the
near-decade length of this study, we do not yet have a sufficient sample size to
discriminate individual differences brought about by age, parity, weight, or rank
patterns.
We did find t h a t “older” capuchin and spider females tended to have shorter
intervals than younger females, and that multiparous capuchin females tended to
have shorter intervals than primiparous females. (Parity could not be tested for
spider monkeys a s there were no primiparous spider monkeys females in our sam-
ple.) This non-significant trend corresponds to previous reports on other primate
species [e.g., Silk, 1990; Smuts & Nicholson, 19891. However, we found that the
trend was reversed in howling monkeys; in this species younger and primiparous
females tended to have shorter intervals. This reversal supports earlier conclu-
sions by Glander [1980] and Clarke & Glander [19841that reproduction in mantled
howling monkeys is biased toward early fecundity in young adult females. Crock-
ett and Rudran [1987a] found that age had no significant effect on IBI length in red
Birth Intervals in Neotropical Monkeys / 17
TABLE 111. Gestation and LactatiodCycling Length Comparisons Between Capuchins,
Howlers, and other Primates of Similar Body Weight, Brain Weight, Neonatal Body
Weight, and Brain. Body Ratio (Harvey et al., 1987)
Mean
Species Variable Comparison values for
being being groups comparison
compared compared similar in- groups n t= P Comment
Capuchins Gestation Body weights 145 6 0.96 n.s. Slightly long
(days) 162 Brain weights 168 6 0.29 n.s. Typical
Neonate weights 167 6 0.50 ns. Typical
Brain:body ratios 161 7 0.08 n.s. Typical
Capuchins Lactation/ Body weights 28 1 5 3.29 c.05 Long
cycling Brain weights 282 4 2.97 <.05 Long
(days) 629 Neonate weights 259 5 2.72 <.05 Long
Brain:body ratios 183 4 6.06 C.01 Very long
Howlers Gestation Body weights 187 8 0.02 ns. Typical
(days) 186 Brain weights 167 10 1.42 n.s. Slightly long
Neonate weights 179 18 0.27 ns. Typical
Brain:body ratios 178 24 0.20 n.s. Typical
Howlers Lactation/ Body weights 439 7 0.12 n.s. Typical
cycling Brain weights 252 6 1.76 n.s. Slightly long
(days) 412 Neonate weights 385 11 0.15 ns. Typical
Brain:body ratios 442 18 0.04 n.s. Typical
howlers. In capuchins, the only species for which dominance ranks were available,
high-ranked females had a non-significant tendency toward shorter intervals. The
same trend has been reported in wedge-capped capuchins [Robinson, 1988b1,black
spider monkeys [Symington, 19871, and baboons [Smuts & Nicholson, 1989; but cf.
Altmann et al., 19881.
The one significant finding in our intraspecific analysis, that loss of an infant
shortens the interbirth interval in all three species, supports the observation made
in several previous studies that infant survivorship affects interbirth intervals
[e.g., Altmann et al., 1978; Crockett & Sekulic, 1984; Cords & Rowell, 1987;
Harley, 1985; Scucchi, 1984; Tanaka et al., 19701. This is likely due to the physi-
ological relationship between suckling, lactation, and amenorrhea [Williams,
19841. Simpson et al. [1981] suggested that even mothers who simply reject their
infants earlier and more forcibly experience shorter IBIS than mothers who con-
tinue to allow their infants to nurse.
Another variable that has often been identified as affecting the fecundity of
female primates is the size of the group in which they reside. A major review of 13
primate species by van Schaik [19831 found a significant negative correlation
between group size and fecundity for the vast majority of cases. This effect is
believed to be brought about by increasing competition for food and social stress in
larger groups [e.g., Dunbar, 19871. On the other hand, Robinson [1988al has ar-
gued that larger groups are able to displace smaller groups from monopolizable
resources, and thus females in larger groups should experience greater reproduc-
tive success. In Robinson’s study population of wedge-capped capuchins, fecundity
was much higher in large groups than small ones. In our study sample of white-
faced capuchins, the trend is for larger groups to have higher birthrates than
smaller groups, but the difference is not significant.
18 I Fedigan and Rose
Although there were considerable annual fluctuations over the 8 years of birth
rate data presented in this paper, there was no consistent pattern across the 3
species, and we were not able to isolate specific factors responsible for “good”
versus “bad” reproductive years. The total amount of annual rainfall is only a
broad inferential measure of the relative amount of resources that should be avail-
able to cycling females, and in this study sample, i t does not correlate significantly
with the proportion of infants born in the subsequent year [cf., Crockett & Rudran
1987bl.
In Guanacaste, almost all of the rainfall occurs during the rainy season, from
June through November, and 70% of the infants in this study were born in the dry
season from December through May. Gestation lengths for the 3 primate species
are approximately 5 to 7 months, which indicates a peak in conceptions during the
rainy season. Most researchers have concluded that birth seasons are not evident
in these cebid species [see Clarke & Glander, 1984; Eisenberg, 1973; Glander,
1980; references in Lindburg, 19871. However, seasonal concentrations of births
have been reported in some populations of spider monkeys [Chapman & Chapman,
1990; Milton, 1981; Symington, 1987; van Roosmalen, 19851, howlers [Jones, 1980;
Crockett and Rudran, 1987133, and capuchins [Defler, 1979; Janson, 1984; Robin-
son, 1988133. It is clear that strict seasonality is not the case in the three species
found in Santa Rosa National Park, since some births did occur in the rainy season.
It would be more appropriate to suggest that a birth peak occurs from December-
May.
When we compared the three primate species in the park we found that howl-
ers give birth approximately every 1.5 years, capuchins give birth approximately
every two years, and spider monkeys only every three years. What might be de-
termining these interspecific differences? An interbirth interval is a composite
variable made up of 3 very different reproductive phenomena-the length of ges-
tation, the period of post-partum amenorrhea, and the number and length of cycles
that occur before the female conceives again. We normally think of gestation
length a s being tightly biologically circumscribed, and relatively invariable across
the females of a given species. As well, the length of post-partum amenorrhea may
have a n evolutionarily-fixed aspect, but is subject to environmental variables,
especially the effects of suckling and lactation, and nutritional factors. Finally, the
length of estrous cycles is a biologically-determined phenomenon, but the number
of cycles that it takes for a female to conceive is likely to be highly influenced by
social and other environmental circumstances.
Since length of gestation is the component of IBI least subject to environmen-
tal influences, we might expect that gestation would best fulfill the prediction of
a n allometric relationship with body size. Indeed in this study of cebids, relative
gestation length is the ONLY life history trait that corresponds to relative body
size across the three species. All of the other life history characteristics reflecting
the pace of development and reproduction, indicate that capuchins are “slower”
than would be predicted from their body size. Comparisons with a wide range of
primate life history data (see Table 111) indicate that the long IBIS of capuchins can
be traced to the lactatiodcycling phase of their interbirth intervals. This means
that the white-faced capuchins in our study population either have a long period of
post-partum amenorrhea, andlor they take a long time to conceive again after
resuming cycling. Galdikas and Wood [19901 identified suckling-induced anovula-
tion as the principle determinant of IBI in their study samples of humans and great
apes. In our study of free-ranging, natural cebid populations, it was not possible to
separate the anovulatory from the cycling phase of the IBI, so they were considered
together. From a social point of view, a cycling female primate is usually still
Birth Intervals in Neotropical Monkeys I 19
caring for her last offspring, even if it is partially or fully weaned, and thus
maternal care may be implicated in the lengths of both the anovulatory and the
cycling phases of the IBI. Why would spider infants need to be cared for longer than
capuchin infants and capuchin infants longer than howler infants?
As a general rule, bigger species take longer to grow up, and experience
“slower” life histories (i.e., lower birth rates, slower rates of development, and
longer lives). Most of the variation in life history traits can be accounted for by
scaling to body mass. Spider monkeys are the largest of the three species under
consideration and are thus predicted to have the slowest rate of development. Once
body weight is accounted for, the remaining variation has been attributed to a
number of different factors, including brain size. Capuchins have the greatest
braidbody ratio of the three species, and they have the lowest neonatal braidadult
brain ratio. When a capuchin infant is born, its brain is only Y3 of its adult size,
whereas howler and spider neonates have brains 1/z of adult size. According to
Watts [19901, neontatal capuchins are less mature than newborn cercopithecoids,
and are more similar to the apes than to monkeys in skeletal maturity at birth.
There has been some debate in the literature as to whether body size or brain
size or basal metabolic rate is the factor that best explains variation in life history
patterns [e.g., Economos, 1980; Harvey et al., 1991; Hofman, 1983; McNab, 1988;
McNab & Eisenberg, 1989; Ross, 19921. Without entering into that debate, it is
clear that in this comparison of three cebid species representing 3 different sub-
families (Cebinae, Alouattinae, Atelinae), body size does not provide an adequate
explanation of the relative pace of life history patterns. Perhaps as noted by Galdi-
kas and Wood [19901, Harvey et al. [19871, and Rasmussen & Izard [19881, the
allometric relationships that characterize primates as an order break down when
attention is focused on closely-related species. However, if the energetic demands
of brain growth and the maintenance of a relatively large brain size do act as a
“pacemaker” for life history patterns, then we might predict that capuchins with
their unusually high brain to body ratio, would have slower than expected life
histories patterns for their size [see Parker, 1990; Watts, 1990; and Sawaguchi,
19921. We might also predict that since a cebus neonatal brain is only % of its adult
size, capuchin mothers would devote relatively long periods of time to nurturing
each infant before giving birth to the next (i.e., exhibit relatively long interbirth
intervals). One independent test of this argument would be to determine the rel-
ative length of the IBI (especially the lactationlcycling phase) in free-ranging
squirrel monkeys, another cebid species with an unusually high brainlbody ratio.
A second major variable that has been implicated in the pace of reproduction,
once the effects of different body sizes have been removed, is the pattern of habitat
andor resource use [Cords and Rowell, 1987; Ross, 19881. Monkeys found in pri-
mary forests tend to exhibit slower life histories and those found in open, variable
habitats have faster life histories. Capuchins have been identified as an exception
[ROSS, 19911. They have very slow life histories for their body size but they are not
limited to primary forests. Indeed their habitats today are more likely to be char-
acterized as secondary growth areas. Ross suggests that perhaps capuchins evolved
in stable primary forests, and later colonized secondary forests.
Diet is another aspect of habitat use that may be pertinent to this consider-
ation of variation in IBIs. It has been correctly pointed out to us (Crockett, pers.
comm.) that the relative length of average IBIs in howlers, capuchins, and spider
monkeys corresponds to the proportion of fruit in their diets. Although based on a
sample of only three species, we would suggest that in this apparent relationship
between fruit-eating and birth intervals, the intervening variables are intelligence
and relative brain size. The “ecological origin” theory of intelligence holds that
20 / Fedigan and Rose
ecological pressures, such as foraging strategies, selected for intelligence and large
relative brain sizes in primates [e.g., Gibson, 1986, Milton, 19881. Foraging on
fruit, in particular, has been identified as selecting for intelligence, since fruit is
patchily distributed in time and space. Milton [19881 noted that spider monkeys,
who are strictly frugivorous, have larger relative brain sizes than howlers, who
will eat some fruit, but are fundamentally folivorous. Capuchins are omnivorous
and eat a higher proportion of fruit than howlers, but a lower proportion than
spider monkeys [Chapman, 19881.Furthermore, capuchins are noted for their abil-
ity to find, extract, and process embedded foods and these extractive foraging
techniques have been argued to be indicative of higher order cognitive skills, and
related to their large brain sizes [Gibson, 1986; Parker, 19903. Thus, it is possible
to argue that differential foraging patterns was one of the selective pressures for
relative brain sizes in these three species, and that brain size in turn acts as a
“pacemaker” for life history traits such as interbirth intervals.
The IBIS reported in this study are comparable to those suggested by some
earlier reports for these three species and their congeners. The median IBI for
Alouatta palliata (19.9 months) falls between the averages of 17 and 22.5 months
previously reported for this species by Milton [1982], Glander [1980], and Clarke
and Glander [1984], and is close to the 17 months reported for A. seniculus [Crock-
ett and Sekulic, 1984; Crockett and Rudran, 1987al. However, the range of IBI’s in
the Santa Rosa population (9-40 months) exceeds those previously reported for
either species [see also Crockett & Eisenberg, 19871. The median IBI for Ateles
geoffroyi is similar to the 31.9 months reported by Milton [19811 and the 34.5
months reported for A. paniscus chamek [Symington, 19873.However, the range of
IBI’s a t Santa Rosa (13-48 months) again exceeds that previously reported [see
also Eisenberg, 1973; van Roosmalen, 19851. There are no comparable data from
wild populations for Cebus capucinus, but the median IBI of 26.4 months exceeds
the 22 months reported for C . apella, and is similar to the 26 months reported for
C . oliuaceus [Robinson & Janson, 19871.
In summary, the comparative pattern of interbirth intervals that we found in
our three study species is most consistent with allometric variation in brain size.
However, interbirth intervals may also be affected by the constraints of other life
history variables such as infant survivorship. Further, there may be some type of
selection for the overall pace of reproduction (e.g., K versus r selection, or pleiot-
ropy), such that IBI is only one aspect of a lifetime reproductive pattern. Finally,
environmental factors, such as habitat and diet, may affect the pace of reproduc-
tion. Although interbirth interval is a widely used life history trait, with a re-
spected tradition behind it, we found it to be a heterogeneous category. If we wish
to address the question of why females of a species space their births in a particular
manner, we need to focus in on the components of interbirth intervals-gestation,
amenorrhea, and cycling to conception-and the factors which affect these compo-
nents in multivariate ways.
CONCLUSIONS
1. We found significant differences in the length of interbirth intervals of
capuchins (26.36 months), howlers (19.90 months), and spider monkeys (34.72
months).
2. Capuchins have a “long” interbirth interval for their relative body size,
attributable to a prolonged lactatiodcycling phase.
3. Differences in interbirth interval length correspond to relative brain size,
rather than relative body size.
Birth Intervals in Neotropical Monkeys / 21
4.Within species, there were no significant differences in interbirth interval
length due to age, parity, weight, or dominance rank.
5. Loss of an infant resulted in shorter subsequent birth intervals in all three
species.
6 . We found no clear correlation between birth rates and annual rainfall, but
births in all three species clustered in the dry season.
ACKNOWLEDGMENTS
We are grateful to the National Park Service of Costa Rica for allowing us to
work in Santa Rosa National Park from 1983 to 1988, and to the administrators of
the Area de Conservaci6n Guanacaste for permission to continue research in the
park to the present day. Many people contributed to the collection of data for this
ten year project, but the efforts of Colin Chapman, the late Larry Fedigan, Ken
Glander, Francois LaRose, Katie MacKinnon, and Rodrigo Morera are particularly
acknowledged. Terry Taerum assisted with the SURVIVAL analyses, and John
Addicott with the tables. We thank Carolyn Crockett, Samuel Wasser, Michael
Raleigh, and one anonymous reviewer for many helpful suggestions that improved
the manuscript. The research of L.M.F. is funded by a n on-going operating grant
(A7723 from the Natural Sciences and Engineering Research Council of Canada
[NSERCCI), and that of L.M.R. was funded by a n NSERCC post-graduate schol-
arship.
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