Behavioral Ecology Vol. 11 No. 5: 560-564
© 2000 International Society for Behavioral Ecology
Ecological and social determinants of birth intervals in baboons
Centre for Economic Learning and Social Evolution, School of Biological Sciences, Nicholson Building, University of Liverpool, Liverpool L69 3BX, UK
Address correspondence to R. A. Hill. E-mail: r.a.hill{at}liverpool.ac.uk .
Received 7 June 1999; revised 24 November 1999; accepted 24 January 2000.
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ABSTRACT |
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Birth rates in primates have long been proposed to result from an interaction between ecological and social factors. We analyzed a variety of social and environmental variables to determine which ones best explain the observed variation in interbirth intervals across 14 baboon populations. Both the number of females in the group and mean annual temperature were found to be important, and a multivariate equation containing the quadratic components of both these variables accounts for almost all the observed variance in interbirth intervals. The quadratic relationship with temperature is explained in terms of the energetic costs of maintaining a stable body temperature at both low and high temperatures. The quadratic relationship with number of females results from relationships with both food availability and the costs of increasing intragroup competition as group size increases. Although females may be able to exert a certain degree of choice in their reproductive scheduling decisions, they are ultimately constrained by limits imposed upon them by the complex interactions between their ecological and demographic environment.
Key words: baboons, birth rate, interbirth interval, intragroup competition, Papio, thermoregulation.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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For mammals, birth rate is one of four key factors that underlie a female's lifetime reproductive output (Dunbar, 1988
) and is affected by both ecological and social elements. In
terms of ecological correlates, a number of studies have reported an
association between food availability and birth rate (California vole,
Microtus californicus: Ford and
Pitelka, 1984; African rodents, Arvicanthis nioticus, Mastomys
natalensis: Taylor and Green,
1976; Japanese macaques, Macaca fuscata:
Mori, 1979; long-tailed
macaques, Macaca fascicularis: van Schaik and van Noordwijk, 1985;
baboons, Papio cynocephalus:
Hall, 1963), in which birth
rate declines during periods of reduced food availability. Among klipspringer
antelope (Oreotragus oreotragus), ambient temperature has been
identified as the key factor influencing interpopulation variability in birth
rate (Dunbar, 1990). Similar
trends have also been observed for gelada baboons (Theropithecus
gelada), in which altitude, which is highly correlated with ambient
temperature, was found to correlate negatively with birth rate
(Dunbar, 1980;
Ohsawa and Dunbar, 1984).
Furthermore, litter sizes have been reported to decline with altitude in the
goldenmantled ground squirrels (Spermophilus lateralis:
Bronson, 1979), providing
further evidence of a thermal constraint on reproductive options. It has also
been suggested that environmental seasonality influences birth rate through
its effect on reproductive synchrony, which often results in oscillations in
birth rate from year to year (Dunbar,
1988). Goldizen et al.
(1988) demonstrated that
rainfall (probably acting via fruit production) correlates with the monthly
distribution of births in saddle-back tamarins (Saguinus
fuscicollis), and Lycett et al.
(1999) and Wasser and Norton
(1993) found similar trends
for baboons. Similarly, Stravistava and Dunbar
(1995) reported that birth
rates and rainfall seasonality are negatively related for Hanuman langurs
(Presbytis entellus), while Dunbar
(1995) found that interbirth
intervals increase with latitude (and hence environmental seasonality) in
South American callitrichids.
Social factors are thought to influence birth rate through the demographic
structure of a group. Van Schaik
(1983) reported a negative
correlation between the number of offspring per female and the number of
females in a group for the majority of Old and New World monkey species
reviewed. Kumar (1995) found a
similar relationship for Japanese macaques, with birth rate linearly
decreasing with group size. These data were taken to support van Schaik's
(1983) assertion that birth
rates should decrease as group size increases due to intragroup competition.
However, Wrangham (1980)
predicted that birth rate should exhibit a humped curve against group size due
to the interaction between intragroup and intergroup competition. In a recent
paper, Takahata et al. (1998)
found general support for this idea with data from Japanese macaques.
Other demographic factors have also been implicated. Dunbar and Sharman
(1983) found that, for
baboons, the more females per male in a group, the lower was the mean birth
rate. They explained this relationship in terms of female-female competition
for access to male coalition partners as a means of reducing harassment from
other group members. Srivastava and Dunbar (1996) found that birth rates
increased with the proportion of groups containing a single male in hanuman
langurs, possibly because overt competition between males in multimale groups
adversely influences female fertility. Dunbar
(1987) reported a similar
relationship for African colobines. In the langurs, birth rates were also
negatively associated with female group size confirming the adverse effects of
stress due to between-female competition (Srivastava and Dunbar, 1996). Wasser
and Starling (1988) provide
evidence from baboons to support this, since attacks from female coalitions
led to reproductive suppression in the attacked individuals.
More recently, Lycett et al.
(1998) examined the influence
of predation risk and the relationship between care-dependent and
care-independent sources of mortality on female reproductive scheduling. They
found that for mothers with surviving infants, the range of interbirth
intervals across nine baboon populations could be partly accounted for by the
level of predation risk at that site. Females living under conditions of low
predation risk are able to care for infants for longer periods; longer
interbirth intervals are consequently a feature of these habitats. Where the
risk of care-independent mortality to offspring is high, the emphasis shifts
to producing offspring at a faster rate, and thus interbirth intervals are
reduced. However, the degree to which females are able to exhibit this
behavioral plasticity will ultimately depend on their ecological and
demographic situation.
In this study we considered a number of demographic and environmental
variables that might influence interbirth intervals across baboon populations.
We used data from the original baboon data set analyzed by Lycett et al.
(1998), as well as data from
additional Papio baboon studies that were not available at that
time.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Papio baboons are widespread throughout sub-Saharan Africa and inhabit a wide variety of habitats including forest, swampy woodland, savannah, desert, coastal scrub, and high montane slopes. Their ecological flexibility is paralleled by variation in demography and social organization, with baboons forming social groups ranging from small one-male units to large cohesive multimale groups and females generally remaining in their natal group throughout their lives.
Data on interbirth intervals are available for 14 populations of
Papio baboons (see Table
1). Data were extracted from the literature, with populations only
included for which data had been collected from unprovisioned troops for a
minimum observation period of 12 months. Where data on actual interbirth
intervals were not available, alternative estimates of mean birth rates were
obtained by summing the total number of adult female-months studied and
dividing by the number of infants born in those troops over that time (sensu
Dittus, 1975;
Dunbar and Dunbar, 1975).
Although these estimates may not equate precisely to observed interbirth
intervals, they are unlikely to be significantly biased. Where possible, we
also took climatic and demographic data from the sources from which the
interbirth interval data were obtained. Where the original sources did not
contain these data, we took values from literature relating to the same study
period. Where climatic data were not available from these sources, the data
were taken from Dunbar
(1992b).
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All data were loge transformed to ensure normality for
parametric analysis. We used regression analysis to determine the
relationships between interbirth intervals and the independent variables.
However, many of the relationships with interbirth intervals were quadratic,
and thus stepwise procedures could not be used because the linear and
quadratic components did not always have significant independent effects. As a
consequence, a combination of enter and backward regression was used to
determine the best fit equations where necessary. All tests are two tailed.
This paper follows convention in considering the five Papio species
as subspecies of a single superspecies, Papio cynocephalus (e.g.,
Dunbar, 1992b;
Jolly, 1993), and thus no
distinctions are made on the basis of phylogeny during analysis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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With respect to the demographic variables, there were significant quadratic regressions between interbirth intervals and both number of females (r2 =.753, F2,11 = 16.774, p <.001) and group size (r2 =.741, F2,11 = 15.769, p =.001), although there were no significant relationships with number of males (r2 =.148, F2,11 =.955, p > 0.40) or the adult sex ratio (r2 =.025, F1,12 =.308, p >.55).
It is possible that the highly significant correlations with number of
females and group size may result from a strong linear interrelationship
between these two variables (r2 =.876,
F1,12 = 84.579, p <.001). Incorporating the
quadratic components of both of these independent variables into a backward
regression reveals that number of females is the principal factor because only
this quadratic relationship remains significant (see
Figure 1). The best-fit
equation is:
 | (1) |
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Of the climatic variables, only temperature shows a significant
relationship with interbirth interval, and again the bestfit equation was
quadratic (Figure 2;
r2 =.633, F2,11 = 9.482, p
=.004). This relationship is independent of the number of females because
there is no correlation between temperature and the number of females
(r2 =.026, F1,12 = 0.318, p
>.55). The best-fit equation with respect to temperature is:
 | (2) |
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Entering both temperature and the number of females into the same
regression model yields the following best-fit equation:
 | (3) |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Mean annual temperature and the number of adult females in the group between them explain 84% of the variance in interbirth intervals across baboon populations. Interbirth intervals showed a significant quadratic U-shaped relationship with the number of females. Because group size is a function of the number of females in the group, there is a superficial relationship between birth rate and group size that appears to conform to the predictions of Wrangham (1980
). [Note that
in this analysis we are considering interbirth intervals and not birth rates
as originally discussed by Wrangham
(1980), so the predicted
direction of the relationship is reversed.] Wrangham
(1980) proposed that
interbirth intervals should initially decrease with troop size because larger
troops have advantages in intergroup competition over smaller troops; however,
interbirth intervals should then increase again as intragroup competition
becomes more intense as group size increases, resulting in a U-shaped
relationship.
Although Wrangham's (1980)
hypothesis may have some explanatory value within populations (e.g., Japanese
macaques: Takahata et al.
1998), it is difficult to see how this relationship can be
extended across populations, at least with respect to intergroup competition,
since most of the parameters are population dependent. Both the competitive
advantage that a troop can expect to gain and the intensity of intergroup
competition for a troop of a given size will depend on the range of group
sizes that exist within that population. Because the range of realizable group
sizes is a function of the environmental conditions experienced by a
population (Dunbar 1992b,
1996), the pattern observed
here may not reflect the levels of competition proposed by Wrangham
(1980) but instead reflect
differences in group sizes between sites due to differential resource
availability.
Both number of females and group size show significant quadratic relationships with rainfall (number of females: r2 =.474, F2,11 = 4.952, p <.03; group size: r2 =.435, F2,11 = 4.238, p <.05), with these effects being independent of the relationship between interbirth interval and temperature, since there is no relationship between rainfall and temperature (r2 =.002, F1,12 = 0.021, p >.85). This quadratic relationship can be explained by a trade-off between two opposing effects; namely, the effects of resource availability on the one hand and intragroup competition on the other.
Rainfall is known to be a reliable predictor of primary productivity in
sub-Saharan habitats (e.g., Deshmukh, 1984;
le
Houérou, 1984). Populations with
low group sizes and numbers of females are likely to be occupying habitats
with low primary productivity. Female mammals must attain a minimum
nutritional plane before they can ovulate; consequently, irrespective of the
physiological mechanism involved, physical condition is likely to be a key
factor determining female fertility. Females occupying poor-quality habitats
are thus likely to have longer interbirth intervals. Some evidence to support
the relationship between interbirth intervals and the resource base comes from
the observation that birth rates decline in a number of primate species once
provisioning is removed (Japanese macaques:
Mori, 1979; baboons:
Hall, 1963; long-tailed
macaques: van Schaik and van Noordwijk, 1985), and this reduction in birth
rates is attributed to correlated declines in female body weight and
condition.
Food availability does not completely explain the relationship with number of females, however, because it cannot account for the observed increase in interbirth intervals with large female group sizes. If food availability alone was underlying the relationship, then interbirth intervals would decline linearly as habitats become increasingly richer. Furthermore, because primary productivity is related to rainfall, we would also expect interbirth intervals to be directly related to rainfall if food availability was the sole explanation. Since the observed relationship does not conform to either of these predictions, other factors must be important.
Intragroup competition is likely to be significant in this respect.
Irrespective of the level of resource base, increasing female group size
inevitably leads to increasing levels of intragroup competition. Even where
resources are not monopolizable and competition is primarily of the scramble
type, larger group sizes result in increased within-group competition. Some
evidence for this comes from baboons in Drakensberg, South Africa, where
females in larger troops spent more time feeding and may have taken lower
quality food items, despite the shallow resource gradient in this mountain
population (Henzi et al.,
1997). Furthermore, competition levels may be independent of
resource availability. Dominance rank significantly influences interbirth
intervals of baboons at Gilgil (Smuts and
Nicholson, 1989); although nutritional factors may underlie this
relationship, stress mechanisms are also likely to be important. Evidence from
baboons in the Masai Mara National Reserve indicates that, for males at least,
levels of stress hormones differ markedly with dominance rank
(Sapolsky and Ray, 1989).
Similar patterns have been observed for gelada, in which birth rates declined
with declining dominance rank (Dunbar,
1984). This relationship is also likely to be stress related
because subordinate individuals experienced much higher rates of attacks than
dominant animals (Dunbar,
1984), despite the virtual absence of contest feeding competition
in gelada due to the nature of their grazing lifestyle. In situations where
intragroup feeding competition is more intense, however, these relationships
become even more pronounced. At Mikumi, Wasser and Starling
(1988) reported that female
attack coalitions served to reproductively suppress their recipients, such
that they experienced more cycles to conception and lengthened interbirth
intervals. Wasser and Starling
(1988) suggested that the
attack coalition behavior among females functioned to reduce competitive
conditions likely to be faced by the attackers' offspring, through a decrease
in birth cohort size.
Although the relationship between interbirth intervals and number of
females reported here may in part reflect the pattern predicted by Wrangham
(1980), we would argue that
these findings probably provide better support for the van Schaik
(1983) model. We suggest that,
rather than reflecting intergroup competition as proposed by Wrangham
(1980), the initial decline in
birth intervals with increasing group size has more to do with the fact that
resource availability limits the range of permissible group sizes for
populations occupying poor-quality habitats. In other words, the apparent
correlation between small group size and long interbirth intervals is actually
due to the fact that poor-quality habitats independently constrain both group
sizes and female fecundity. This factor may not be reflected in the data sets
analyzed by van Schaik (1983)
and Kumar (1995), and this may
account for their more straightforward linear results.
We found no evidence for the relationship between interbirth intervals and
adult sex ratio reported by Dunbar and Sharman
(1983). However, Dunbar and
Sharman (1983) concluded that
their relationship also reflected female-female competition, specifically in
this respect for access to males, and that this relationship may also have
been underpinned by a relationship with rainfall. Furthermore, although Dunbar
and Sharman (1983) found no
specific relationship between birth rate and number of females, their linear
correlational approach would have masked any quadratic effects that might have
been present in their data. The findings of Wasser and Starling
(1988), demonstrating a
proximate role for female-female competition in reproductive suppression in
baboons, further supports this suggestion.
Environmental factors, through their influence on primary productivity and
thus female group size, therefore appear to be important determinants of birth
interval variation in baboons. However, climatic factors may also have direct
effects on baboon physiology and condition, and the influence of temperature
and its costs in terms of thermoregulation are significant in this respect. We
found a significant quadratic relationship between interbirth interval and
temperature, with birth intervals being longer at extremes of low and high
mean annual temperature. This also seems to reflect a tradeoff between two
temperature-related effects. Thermoregulatory considerations appear to impose
energetic costs on female baboons: at low temperatures, females experience
elevated energy expenditures to maintain a stable body temperature, the costs
of which are reflected in longer interbirth intervals as ambient temperatures
decline. Ohsawa and Dunbar
(1984) showed that for gelada,
reduced birth rates at lower temperatures were a consequence of the females'
inability to carry fetuses to term when low temperatures placed heavy
energetic demands on them. Similar results have been reported for klipspringer
(Dunbar, 1990). At the same
time, it seems that the energetic costs of keeping the body cool
(Mount 1979) have the reverse
effect (interbirth intervals increase with rising temperature), resulting in
the pattern of birth intervals observed in this study.
Differences in interbirth intervals between baboon populations thus result
from a complex interaction between environmental factors (notably temperature
and food availability, which place energetic constraints on female condition)
and demographic considerations (especially female group size, which results in
increased female-female competition and elevated stress levels). These factors
serve to constrain a female's maximum reproductive rate for a given population
and group size. While females may then exhibit a certain degree of plasticity
in birth rates in response to factors such as predation risk (e.g.,
Lycett et al., 1998), they are
ultimately constrained by the limits imposed upon them by their ecological and
demographic situation. Differentiating Equations 1 and 2 indicates that, for
baboons, mean birth rates are maximal in groups containing on average 14.2
females in populations with a mean annual temperature of 21.7°C. These
values might serve to define optimal habitat for baboons, at least with
respect to reproductive output.
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ACKNOWLEDGEMENTS |
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We thank two anonymous referees for comments on an earlier drafts of this manuscript. J.E.L. was supported by an Economic and Social Research Council (ESRC) program grant for the Economic Learning and Social Evolution (ELSE) Research Centre.
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