Low demographic variability in wild primate populations: fitness impacts of variation, covariation, and serial correlation in vital rates

Abstract

In a stochastic environment, long-term fitness can be influenced by variation, covariation, and serial correlation in vital rates (survival and fertility). Yet no study of an animal population has parsed the contributions of these three aspects of variability to long-term fitness. We do so using a unique database that includes complete life-history information for wild-living individuals of seven primate species that have been the subjects of long-term (22-45 years) behavioral studies. Overall, the estimated levels of vital rate variation had only minor effects on long-term fitness, and the effects of vital rate covariation and serial correlation were even weaker. To explore why, we compared estimated variances of adult survival in primates with values for other vertebrates in the literature and found that adult survival is significantly less variable in primates than it is in the other vertebrates. Finally, we tested the prediction that adult survival, because it more strongly influences fitness in a constant environment, will be less variable than newborn survival, and we found only mixed support for the prediction. Our results suggest that wild primates may be buffered against detrimental fitness effects of environmental stochasticity by their highly developed cognitive abilities, social networks, and broad, flexible diets.

Figure 1

Estimated vital rates (logit scale) for all species in all years. Sn, Sj, and Sa are survival of newborns, juveniles, and adults, respectively; Fj and Fa are fertilities (mean number of new daughters per female per year) for juveniles and adults, respectively. Estimates are corrected for sampling variation (see text); a flat line indicates that the variability in the raw estimates could not be distinguished from pure sampling variation, so the mean value is shown for all years. In this and all other figures and tables, species are presented in order of mean female adult body size (table 2) from smallest (sifaka) to largest (gorilla). S_n is the probability that a newborn survives to the first census after its birth; S_j and S_a are the probabilities of survival over 1 year for juveniles and adults, respectively; and F_j and F_a are the mean number of daughters produced by a juvenile or adult female, respectively, during the following year.

Figure 2

Process variances, covariances, and serial (between-year) correlations for pairs of vital rates shown at the bottom. A, The first bar in each group is the variance of the specified rate, and subsequent bars are covariances between that rate and the other rates. Nonzero variances and covariances that are too small to be visible at the scale of the Y-axis are written in scientific notation. B, The correlation between the first vital rate of a pair in year t and the second vital rate in year t + 1. All measures of variability are based on vital rate estimates that have been corrected for sampling variation. Sif = sifaka, Cap = capuchin, Blu = blue monkey, Mur = muriqui, Bab = baboon, Chi = chimpanzee, Gor = gorilla. S_n is the probability that a newborn survives to the first census after its birth; S_j and S_a are the probabilities of survival over 1 year for juveniles and adults, respectively; and F_j and F_a are the mean number of daughters produced by a juvenile or adult female, respectively, during the following year.

Figure 3

Percent change in fitness in a stochastic environment relative to fitness in a constant environment. Three scenarios are shown: V is variation in vital rates with no covariation or serial (between-year) correlations; VC is variation and covariation with no serial correlations; VCS is variation, covariation, and serial correlations. Percent change is 100(λ_s − λ₁)/λ₁, where λ_s is the stochastic growth rate and λ₁ is the deterministic growth rate in a constant environment (i.e., the dominant eigenvalue of the mean projection matrix). Error bars are 2 SEs around the mean of 10 simulations, each of 50,000 years. Sif = sifaka, Cap = capuchin, Blu = blue monkey, Mur = muriqui, Bab = baboon, Chi = chimpanzee, Gor = gorilla.

Figure 4

Levels of temporal variability in survival for primates estimated in this study compared with published values for other vertebrates. A, Process variance in survival of adults relative to its maximum possible value given mean survival. Primates are shown in red. Note that relative process variance is shown on a one-dimensional logarithmic scale. B, The ratio (log scale) of relative process variance of newborn survival (RV(newborn)) to relative process variance of adult survival (RV(adult)) for all studies that provided nonzero estimates of both process variances. The horizontal dashed line indicates equal relative process variances for the two survival rates; points above the line therefore show higher relative variability in newborn survival than in adult survival. Muriqui is not included, because the estimated process variance in survival was zero for both newborns and adults. Details of literature estimates are provided in appendix B.

Figure 5

Deterministic sensitivities of the population growth rate (dominant eigenvalue of the mean projection matrix) to the underlying vital rates. Sif = sifaka, Cap = capuchin, Blu = blue monkey, Mur = muriqui, Bab = baboon, Chi = chimpanzee, Gor = gorilla. S_n is the probability that a newborn survives to the first census after its birth; S_j and S_a are the probabilities of survival over 1 year for juveniles and adults, respectively; and F_j and F_a are the mean number of daughters produced by a juvenile or adult female, respectively, during the following year.

Figure 6

Relationship between climate variability (coefficient of variation in annual rainfall) and relative variance in newborn survival (A), relative variance in adult survival (B), and the effect of variability on long-term fitness (C; these are the same values shown for the VCS case in fig. 3). Sif = sifaka, Cap = capuchin, Blu = blue monkey, Mur = muriqui, Bab = baboon, Chi = chimpanzee, Gor = gorilla.