In our study of the Cayo Santiago rhesus macaque population, we integrated long-term demographic data on survival and reproduction with new morphometric and behavioral data collected from a sample of mothers and infants. The association between old age and declines in physical condition and activity levels, decreases in reproductive output, and a reduction in early offspring survival, constitute evidence in favor of the senescence hypothesis. Although we had predicted that offspring sex ratio would be skewed toward the costlier sex in accordance with the terminal investment hypothesis, this prediction was not met. However, increased time spent in ventro-ventral contact may suggest that older mothers invest more in their offspring and therefore represents potential evidence in favor of the terminal investment hypothesis. Longer interbirth intervals among older mothers could be interpreted as evidence for either process. As such, our study provides strong evidence for senescence and some weaker evidence for terminal investment.
As previously observed in a captive rhesus macaque population (Gagliardi et al. 2007
), infant survival on Cayo Santiago decreases sharply as females enter their late teens. Our data highlight at least 2 factors that may lead to this. First, although there were no age-related differences in grooming or resting prebirth, older mothers were involved in less grooming interactions after the birth of their infant than younger mothers were. Unfortunately, previous studies that have characterized rhesus behavior in wild habitats have not included female age, rank, or infant presence in their analyses (e.g., Teas et al. 1980
), preventing comparison of these results with wild populations. Given that cercopithecine non-mothers and mothers with young infants tend to be attracted to females with young infants (e.g., Papio anubis
, Frank and Silk 2009
; Papio cynocephalus ursinus
, Silk et al. 2003
; M. mulatta
, Whitham et al. 2007
), this reduced grooming time may mean that the offspring of older rhesus females are less attractive to other females. This observed decrease in sociality may affect the likelihood of infant survival, given the potential links between social support and survivorship in primates (Silk et al. 2006
). In baboons, strong social bonds may increase infant survival and benefit infants by providing mothers with support in agonistic interactions, lowering mother’s basal cortisol levels, increasing infant protection from harassment, or making more resources accessible to mother–infant dyads (Silk et al. 2003
One might expect that by engaging in fewer social interactions and resting more, older females are reserving energetic resources for lactation. However, morphometric data show that older females’ infants weigh less than younger females’ infants. This may be related to the fact that older females had lower BMIs than younger females, which in turn may be attributable to reduced feeding time before birth among older females compared with younger females. Low infant mass is predictive of infant mortality in common marmosets (Callithrix jacchus
, Tardif et al. 2002
) and may be a second factor leading to high mortality rates for rhesus infants born to older mothers.
Most infants born to older females do not survive to reproductive age. However, for those daughters who do survive to reproductive age, mother’s age at daughter’s birth does not affect age at first parturition or annual birth rate. It may be that the mothers of those few daughters who survive to reproductive maturity were in exceptionally good body condition for their age or were high ranking, but unfortunately, long-term records do not contain morphometric or hierarchical information. From the short-term data set, however, we did observe that high-ranking females spent more time feeding during pregnancy than low-ranking females, and this may confer fitness-related advantages to the offspring of high-ranking females.
Although, according to the terminal investment hypothesis, increasing interbirth intervals and suckling time may increase infant survival for older females, this is not the case for females in our study. Consistent with a vast body of literature on primate life history (e.g., Malik et al. 1992
; Okamoto et al. 2000
; Higham et al. 2009
), we might expect interbirth intervals to be shorter for females whose infants die, but we see no evidence of this; whereas infant survival was lower for the older females in our study, their interbirth intervals were longer. These patterns are consistent with general reproductive senescence in these females. Additional data are needed to determine if lengthening interbirth intervals are associated with hormonal or behavioral changes. Hormonal data would indicate whether the increasing interbirth intervals are associated with increasingly irregular ovulatory patterns, as they are in captive rhesus populations (Gilardi et al. 1997
). Furthermore, behavioral data collected from mothers and infants between 2 and 8 months post-parturition would reveal whether age-related differences in suckling intensity affect time between parturition and the resumption of mating (see Johnson et al. 1998
). If extended interbirth intervals among older females are clearly related to increased lactational effort, this would be consistent with a terminal investment interpretation for longer interbirth intervals. Conversely, if extended interbirth intervals occur among older females even though overall lactational effort is similar across the adult lifespan, this would be consistent with a senescence interpretation of the effect.
Our findings show that although rhesus macaque females on Cayo Santiago have the physical and physiological ability to conceive and give birth virtually until the end of their life span, their ability to sustain lactation and guarantee infant survival decreases steadily but markedly in their last 5–10 years of life. Because the probability of offspring survival for females older than 23 years is virtually zero, extremely old females would fare better if they ceased reproducing and, instead, invested their resources in their existing offspring. In wild populations of macaques, predators, disease, and unpredictable food sources make it unlikely that adult females will survive into their third decade (Johnson et al. 1991
; Jones-Engel et al. 2006
) such that selective pressures for early termination of reproduction are probably negligible or nonexistent in the wild. As such, the absence of strong evidence for terminal investment in our population, even when females would apparently benefit from it, may be related to the provisioned nature of our population and consequent increased female longevity. Although it is possible that longer interbirth intervals of females in the mid- to late-teen years may alleviate the negative effects of their declining physical condition on the probability of offspring survival, there are no apparent fitness benefits associated with increased maternal investment for rhesus females who continue reproducing into very old age (i.e., above 20 years).
In conclusion, we detected a number of age-related changes in behavior, body condition, reproduction, and infant mortality among Cayo Santiago mothers and their infants. Although female rhesus macaques do show some signs of increased maternal investment, they do not increase investment by producing larger offspring as red deer do (Clutton-Brock 1984
), increasing reproductive rate as red squirrels do (Descamps et al. 2008
), or producing a larger number of sons as Nile lechwe do (Bercovitch et al. 2009
), perhaps because they suffer such strong senescence effects. Taken together, our results provide strong evidence for senescence and only weak evidence for terminal investment. Our approach, which utilized multiple measures of individuals and both long-term and short-term data sets, is useful for assessing which of the 2 hypotheses best explain age-related changes in reproduction within a given species. Although we analyzed a great deal of data, we lacked information about mother–infant interactions beyond the first month postpartum. Future tests of these hypotheses should combine life-history and morphometric data with more extensive behavioral observations on maternal investment throughout infant and juvenile development.