The ecology of motherhood: the structuring of lactation costs by chacma baboons

1. Data from a long-term study of Papio hamadryas ursinus (L.) in the De Hoop Nature Reserve, Western Cape, South Africa, were used to test the assumptions and predictions of Altmann's model of maternal time budgets. 2. Female baboons' feeding time was below model predictions, and there was no evidence for a consistent increase in feeding time with infant age. In addition, female feeding time was not significantly higher than observed baseline feeding times for nonlactating females. 3. Female baboons reduced activity levels in the first few months post-partum, as reflected in significant increases in resting time, and there was some indication that females lost body mass over the course of lactation. When feeding demand was high, females sacrificed social time, and conserved resting time. 4. Females increased vigilance levels during the first 4 months of infant life and were more vigilant overall during lactation than when nonlactating. There was a negative relationship between feeding time and vigilance, but a positive relationship between resting time and vigilance. 5. Female baboons at De Hoop appear to cope with the energetic costs of lactation by reducing activity levels, although this cannot compensate completely for increased energetic costs. This may not be so much an'energy-sparing' strategy as a response to threats presented by infanticidal males in this population. Females therefore trade-off feeding time against vigilance.     

Effects of climate variability on the demography of wild geladas

Nonhuman primates are an essential part of tropical biodiversity and play key roles in many ecosystem functions, processes, and services. However, the impact of climate variability on nonhuman primates, whether anthropogenic or otherwise, remains poorly understood. In this study, we utilized age‐structured matrix population models to assess the population viability and demographic variability of a population of geladas (Theropithecus gelada) in the Simien Mountains, Ethiopia with the aim of revealing any underlying climatic influences. Using data from 2008 to 2019 we calculated annual, time‐averaged, and stochastic population growth rates (λ) and investigated relationships between vital rate variability and monthly cumulative rainfall and mean temperature. Our results showed that under the prevailing environmental conditions, the population will increase (λ _s = 1.021). Significant effects from rainfall and/or temperature variability were widely detected across vital rates; only the first year of infant survival and the individual years of juvenile survival were definitively unaffected. Generally, the higher temperature in the hot‐dry season led to lower survival and higher fecundity, while higher rainfall in the hot‐dry season led to increased survival and fecundity. Overall, these results provide evidence of greater effects of climate variability across a wider range of vital rates than those found in previous primate demography studies. This highlights that although primates have often shown substantial resilience to the direct effects of climate change, their vulnerability may vary with habitat type and across populations.     

Climate variability and child height in rural Mexico

We examine the impacts of weather shocks, defined as rainfall or growing degree days, a cumulative measure of temperature, more than a standard deviation from their respective long run mean, on the stature of children between 12 and 47 months of age in Mexico. We find that after a positive rainfall shock children are shorter regardless of their region or altitude. Negative temperature shocks have a negative impact on height in the central and southern parts of the country as well as in higher altitudes. Although on average there are no statistically significant impacts from positive temperature shocks, certain sub-populations - namely boys, children between 12 and 23 months at the time of measurement, and children of less educated mothers - in some of the regions are negatively impacted. The results also suggest that potentially both agricultural income and communicable disease prevalence contribute to the effects.     

Infant carrying by adult male mangabeys (Cercocebus atys)

Sixty-five interactions where an adult male carried an infant in the proximity of a second male were observed during a 19-mo period in a captive sooty mangabey (Cercocebus atys) social group. The behavior was distributed nonrandomly in both the adult male and infant classes. In all but three of the interactions, the recently deposed alpha male carried an infant in the presence of the newly ascendant dominant male. In the first phase of the study, infants that were carried included the entire unweaned infant cohort (n = 5) born before the rank reversal. The rate of carrying in this class declined as a function of increasing infant age and time since the rank reversal. Infant carrying was not observed in the context of fighting, which was rare, and intermale aggression never preceded the behavior. However, in 40% of the cases, carrying occurred after an infant had been threatened by the dominant male. These results suggest that infant carrying served to protect the infant from aggression rather than to exploit the infant as an agonistic buffer. The data did not unequivocally support the postulate that carrying may be a form of paternal care since paternity could not be assessed. The similar structural and contextual patterns of infant carrying in this species suggest a common origin for triadic male-infant interactions in mangabeys and baboons.     

Variation in stem radial growth of the Australian conifer, Callitris columellaris, across the world’s driest and least fertile vegetated continent

Climate change could alter the biogeography of many tree species. However, there have been few studies of tree growth across climatic gradients at a continental scale. Callitris columellaris is a widespread conifer that spans many climates and landscape positions across Australia. Our aim was to determine how stem radial growth of C. columellaris varies with tree size and with the biogeographic factors of rainfall, temperature, soil fertility and inter-tree competition. We sampled cores from trees at 85 sites in biomes ranging from tropical savanna to arid desert and temperate forest, and measured widths of the 100 outermost growth rings. We analysed ring width in relation to changes in tree age and diameter, and also evaluated the influence of the biogeographic factors on the width of the ten most recently formed rings. The average width of outermost rings varied only slightly with stem diameter, because the decrease in ring width with age and diameter within trees is offset by an increase with diameter among trees. Our analyses thus explain the weak, inconsistent relationships often observed between stem diameter and growth rate amongst trees. The most important biogeographic factors were the climatic ones: across Australia, ring width increased with both mean annual rainfall and mean annual temperature. These relationships were largely driven by continental scale differences between the tropical and the southern (arid plus temperate) sites, while relationships within climate zones were comparatively weak. Ring width decreased with intense inter-tree competition but showed little correlation with available soil nitrogen or phosphorus.     

Grazing behavior responses of rangeland beef cows to winter ambient temperatures and age

A trial was conducted on Montana native rangeland to examine the effects of cow age and ambient air temperatures on mid-winter grazing activity of pregnant beef cows. Cows were fitted with vibracorders and pedometers for 50 continuous days in January and February to monitor daily grazing time (DGT) and distance traveled. Three-year-old cows grazed 0.7 h day⁻¹ longer (P<0.005) and traveled 0.85 km day⁻¹ further (P<0.05) than 5-and 7-year-old cows. Total DGT averaged 8.8 h day⁻¹ across ages and was insensitive (P>0.05) to mean ambient temperature departures (either increases or decreases) from average temperatures of the previous 1–20 days. DGT did not remain below 8 h day⁻¹ for more than one successive day. However, examination of grazing times within daily periods indicated significant linear respones to temperature changes. Morning (07.01–13.00 h) grazing times exhibited variable responses (P<0.05) to temperature departures from averages across the previous 17, 19 and 20 days. Grazing times during afternoons (13.01–19.00 h) and evenings (19.01–07.00 h) declined (P<0.05) when temperatures either increased or decreased from averages of the previous 6–10, and 1, 2 and 4 days, respectively. Only 17% of DGT occurred during the evening period. We concluded that in the foothill grasslands of the Northern Rockies, range beef cows maintained consistent total grazing time despite fluctuating mid-winter temperatures (8 to −26°C) and that cow age influenced grazing activity.     

Age-Related Shifts in the Density and Distribution of Genetic Marker Water Quality Indicators in Cow and Calf Feces

Calves make up about 16% of the current bovine population in the United States and can excrete high levels of human pathogens in their feces. We describe the density and distribution of genetic markers from 9 PCR- and real-time quantitative PCR-based assays, including CF128, CF193, CowM2, CowM3, GenBac3, Entero1, EC23S857, CampF2, and ttr-6, commonly used to help assess ambient surface water quality. Each assay was tested against a collection of 381 individual bovine fecal samples representing 31 mother and calf pairings collected over a 10-month time period from time of birth through weaning. Genetic markers reported to be associated with ruminant and/or bovine fecal pollution were virtually undetected in calves for up to 115 days from birth, suggesting that physiological changes in calf ruminant function impact host-associated genetic marker shedding. In addition, general fecal indicator markers for Bacteroidales, Escherichia coli, and Enterococcus spp. exhibited three separate trends across time, indicating that these bacteria respond differently to age-related physiological and dietary changes during calf development. The results of this study suggest that currently available PCR-based water quality indicator technologies can under- or overestimate fecal pollution originating from calves and identify a need for novel calf-associated source identification methods.     

Synchronization of weaning time with peak fruit availability in squirrel monkeys (Saimiri collinsi) living in Amazonian Brazil

Many mammals coincide their reproductive activities with factors such as ambient temperature, rainfall, and food availability. In primates that invest immediate food intake into reproduction, the periods of maximum fruit production often coincide with the peak of lactation (to maximize maternal survival) or the occurrence of weaning (to maximize infant survival). This study investigates the relationship between reproductive periods and the availability of ripe fruit in the habitat of a population of wild squirrel monkeys (Saimiri collinsi) in Amazonian Brazil. We combine data from several years (2002–2003; 2011–2015) during which we followed the monkeys and quantified the occurrence of matings, gestations, births, and the number of lactating females. We also collected rainfall and plant phenological data for 24 months. Our results confirm that reproductive events are highly seasonal in S. collinsi. The period of weaning corresponded to the peak in the abundance of ripe fruits consumed by the monkeys. This indicates that the period of infant nutritional independence is optimally timed to coincide with periods of greater food production in this habitat. We suggest that seasonal breeding in these primates does not necessarily reduce maternal energetic stress, but likely improves infant survivorship.     

Species Richness-Environment Relationships of European Arthropods at Two Spatial Grains: Habitats and Countries

We study how species richness of arthropods relates to theories concerning net primary productivity, ambient energy, water-energy dynamics and spatial environmental heterogeneity. We use two datasets of arthropod richness with similar spatial extents (Scandinavia to Mediterranean), but contrasting spatial grain (local habitat and country). Samples of ground-dwelling spiders, beetles, bugs and ants were collected from 32 paired habitats at 16 locations across Europe. Species richness of these taxonomic groups was also determined for 25 European countries based on the Fauna Europaea database. We tested effects of net primary productivity (NPP), annual mean temperature (T), annual rainfall (R) and potential evapotranspiration of the coldest month (PET_min) on species richness and turnover. Spatial environmental heterogeneity within countries was considered by including the ranges of NPP, T, R and PET_min. At the local habitat grain, relationships between species richness and environmental variables differed strongly between taxa and trophic groups. However, species turnover across locations was strongly correlated with differences in T. At the country grain, species richness was significantly correlated with environmental variables from all four theories. In particular, species richness within countries increased strongly with spatial heterogeneity in T. The importance of spatial heterogeneity in T for both species turnover across locations and for species richness within countries suggests that the temperature niche is an important determinant of arthropod diversity. We suggest that, unless climatic heterogeneity is constant across sampling units, coarse-grained studies should always account for environmental heterogeneity as a predictor of arthropod species richness, just as studies with variable area of sampling units routinely consider area.     

Thermal effects on movement patterns of yellow baboons

This paper examines the effect of thermal environment on movement patterns of free-ranging yellow baboons (Papio cynocephalus). For Amboseli baboons, one source of potential thermal stress is intense midday heat, and a plausible thermoregulatory response is for animals to simply move into the shade. I therefore examined the hypothesis that baboons would choose quadrats with higher shade availability (as measured by vegetation cover) in response to increasing midday heat loads (as measured by air temperature and solar radiation). Surprisingly, this was not the case—neither ambient air temperature, ambient solar radiation, nor quadrat plant species composition had a significant effect on shade availability of quadrat selected. Instead, thermal conditions affected a different aspect of baboon movements; namely, spatial displacement rates. At high air temperatures, baboons as a group traversed woodland habitats more slowly, and bare pans more quickly, than at lower air temperatures. I surmised that this relationship might reflect thermal effects on movement patterns at a smaller scale: if individuals exposed to high heat loads spent more time resting in shade under clumps of vegetation, they would thereby traverse densely-vegetated (hence shaded) quadrats more slowly. To address this question directly, I obtained focal sample data on activity and microhabitat budgets of individual baboons in relation to environmental temperature. The frequency of most combinations of activity state (e.g., grooming, social behavior) and microenvironment state (e.g., elevation, proximity to vegetation) did not vary monotonically with air temperature. However, baboons in shaded locations (but not those in unshaded locations) spent more time resting and less time moving at high air temperatures than low. In other words, baboon activity budgets depended on both microclimate and microhabitat—animals reduced their activity, particularly movement, when they encountered shade under hot conditions. This pattern of microhabitat choice in turn led to temperature-dependent changes in travel rate at the habitat level. These observational studies of movement patterns suggest that Amboseli baboons employ opportunistic thermoregulation—they do not seek out densely-shaded habitats or individual patches of shade at high air temperatures. Instead, they respond to environmental heat loads by resting, and thereby slowing down, when they happen to encounter plant shade. Aspects of baboon ecology that favor such an opportunistic mode of thermoregulation include large body size and non-thermal constraints on movement patterns.     

Identification of the Key Weather Factors Affecting Overwintering Success of Apolygus lucorum Eggs in Dead Host Tree Branches

Understanding the effects of weather on insect population dynamics is crucial to simulate and forecast pest outbreaks, which is becoming increasingly important with the effects of climate change. The mirid bug Apolygus lucorum is an important pest on cotton, fruit trees and other crops in China, and primarily lays its eggs on dead parts of tree branches in the fall for subsequent overwintering. As such, the eggs that hatch the following spring are most strongly affected by ambient weather factors, rather than by host plant biology. In this study, we investigated the effects of three major weather factors: temperature, relative humidity and rainfall, on the hatching rate of A. lucorum eggs overwintering on dead branches of Chinese date tree (Ziziphus jujuba). Under laboratory conditions, rainfall (simulated via soaking) was necessary for the hatching of overwintering A. lucorum eggs. In the absence of rainfall (unsoaked branches), very few nymphs successfully emerged under any of the tested combinations of temperature and relative humidity. In contrast, following simulated rainfall, the hatching rate of the overwintering eggs increased dramatically. Hatching rate and developmental rate were positively correlated with relative humidity and temperature, respectively. Under field conditions, the abundance of nymphs derived from overwintering eggs was positively correlated with rainfall amount during the spring seasons of 2009–2013, while the same was not true for temperature and relative humidity. Overall, our findings indicate that rainfall is the most important factor affecting the hatching rate of overwintering A. lucorum eggs on dead plant parts and nymph population levels during the spring season. It provides the basic information for precisely forecasting the emergence of A. lucorum and subsequently timely managing its population in spring, which will make it possible to regional control of this insect pest widely occurring in multiple crops in summer.     

Age and annual growth rate cause spatial variation in body size in Phrynocephalus przewalskii (Agamid)

Whether or not biogeographic rules dealing with spatial patterns of animal body sizes are valid for ectotherms is controversial. As the ectotherms grow all their lives, we explored the role of age and annual growth rate in body size variation in Phrynocephalus przewalskii in northern China. Morphological data were collected from 11 populations across a broad geographic gradient. Correlations between age, sex, climatic factors, and body size were analyzed using generalized linear model (GLM) and generalized linear mixed model (GLMM). GLM analysis indicated that the general body size of both sexes and the appendage size of females increased significantly with increasing temperature; however, the coefficient of determination was very small. GLMM analysis indicated that body size only correlated with age, whereas appendage size was affected by age, temperature, rainfall, and sunshine. Annual growth rates were positively correlated with temperature. We concluded that body size variation was mainly caused by age structure and plasticity of the growth rate in P. przewalskii and did not follow Bergmann''s rule; however, females followed Allen''s rule. Future studies to investigate the effect of energy restriction are needed to further understand the relationship between growth rate and body size. We also suggest that further studies on thermal advantage and sexual selection may be helpful to understand appendage size variation in P. przewalskii.     

Formula-fed and breast-fed baboons: Weight growth from birth to adulthood

The objective of this study was to compare the immediate and long-term effects of type of infant diet (formula-fed vs. breast-fed) on the weight growth of baboons. Longitudinal (serial) weight data were collected from 44 savannah baboons (Papio cynocephalus anubis) for the total preadult period of growth from birth to approximately 8 years of age. Fifty percent of the sample (11 females and 11 males) were fed a standard infant formula by a nursery care technician for the first 18 weeks of postnatal life. The remaining 11 females and 11 males were breast-fed by their mothers for an equivalent period of time. After 18 weeks of age the animals were removed from their infant environments (either nursery or mother-reared) and assigned to one of four age-cohort social groups. Each age-cohort group was balanced for infant treatment and gender. The animals remained in these social groups for the duration of the project and were provided nutritionally identical postweaning diets. No significant weight differences were found between the two rearing conditions for either gender during the initial 15 weeks of growth. Following this period, however, females of breast-fed environments averaged greater weight at all ages than their bottle-fed peers. The intensity of the adolescent growth spurt was also slightly greater among the female breast-fed group. No postinfant average weight-per-age disparity was observed between the male treatment groups.     

Infants as a commodity in a baboon market

We used data from adult female chacma baboons, Papio cynocephalus ursinus, to provide the first test of hypotheses on interchange trading and the structure of a biological market (Noë & Hammerstein 1994, Behavioral Ecology and Sociobiology,35, 1-11) within a primate group. The interchange commodities selected were grooming and handling of infants less than 3 months of age. Patterns of grooming in relation to infant handling showed strong evidence for interchange. Grooming for infant access was initiated by potential handlers and was significantly likely to be nonreciprocated. More critically, the data show that infant ‘supply’ created a market effect: grooming bout duration (the price ‘paid’ for handling) was inversely related to the number of infants present in the group. In addition, there was an inverse relationship between grooming bout duration and the rank distance between mothers and handlers, suggesting that higher-ranking mothers could demand a higher price for infant handling. Where rank distance was high, females were able to handle infants without grooming. Dominance could thus be used to disrupt the infant market effect. If biological markets models are to be fully applicable to primate groups (and those of other social mammals) then the potentially distorting effect of dominance needs to be incorporated into the framework. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Trade-offs between activity and thermoregulation in a small carnivore,the least weasel Mustela nivalis

We studied factors influencing daily energy expenditures (DEE) of male least weasels (Mustela nivalis) using the doubly labelled water technique. The relationship between ambient temperature and DEE formed a triangular pattern, characterized by invariance of the maximum DEE and an inverse relationship between minimum DEE and temperature. A simple energetic model relating the DEE of male weasels to activity time (AT) and ambient temperature predicted that, across seasons, less than 10 per cent of measurements approach the upper bound of observed DEE. Male weasels were able to maintain a relatively constant maximum energy output across varying temperatures by adjusting their AT to changes in temperature. They achieved maximum energy expenditures in winter due to high thermoregulatory costs, and in spring and summer due to high levels of physical activity. This pattern exemplifies a ‘metabolic niche’ of a small mammal having extremely high energy expenditures primarily driven by ambient temperature.     

Body composition in baboons: Evaluating a morphometric method

The objective of this study was to determine whether noninvasive morphometric measurements of olive baboons (Papio cynocephalus anubis) can reliably predict lean body mass and fat mass in this species. Crown-rump length, triceps circumference, and skinfold measures at the neck, subscapular, suprailiac, and triceps sites were obtained prior to necropsy from 21 clinically normal infant baboons at 18 weeks of age and from 22 clinically normal adolescent baboons at 5 years of age. At necropsy, the lean body mass and body fat mass were measured using gravimetric methods. Pearson's correlations and regression analysis were used to test the relationship between direct measures of lean and fat mass obtained at necropsy with calculated estimates based on morphometric measures obtained prior to death. Our null hypothesis was that the morphometric measures (individually or in combination) were not related to direct measures of fat mass or lean mass. Non-linear and multiple regression estimators, by age and gender, were derived and provided increased predictability. Our results indicate that (1) morphometric measures can accurately predict lean body mass in male and female baboons; (2) morphometric measures used to predict lean body mass change with age; (3) morphometric measures are strongly associated with body fat mass at 18 weeks of age but are not as strongly associated with body fat mass in 5-year-old baboons; (4) triceps circumference provides the best single indicator of lean body mass for both genders and age periods; (5) baboons are like humans in that adolescent females tend to accumulate body fat while males of the same age tend to develop lean mass; and (6) combinations of these morphometric measurements explain between 70% and 100% of the variability and can be used to estimate lean and fat mass in baboons.     

Life history of yellow baboons: Physical development,reproductive parameters,and infant mortality

Longitudinal data from a population of yellow baboons,Papio cynocephalus, in the Amboseli National Park, Kenya, provide life history parameter estimates. Females reached menarche at approximately four-and-a-half years of age and then cycled for approximately a year before first conception. Postpartum anestrum averaged 12 months but ranged from six to 16 months. In cases of still births or infant death during postpartum amenorrhea, females commenced cycling after approximately one month. In mature females the time spent cycling before conception was five months on the average with a range from one to over 18 months. Only half of all full-term pregnancies resulted in infants who survived the first year of life; only a third, in infants who survived until the birth of their mother’s next infant. In comparison with data from laboratory colonies, our data indicate that female baboons in Amboseli are older at birth of first infant. They have, on the average, a somewhat shorter interbirth interval than was estimated from earlier crossectional field data, and therefore spend a larger portion of their adult life pregnant, but have a much longer interval—at least three years on the average—between the birth of an infant and the birth of that infant’s next older surviving sibling. A number of morphological changes in immature baboons are described.     

Ecology and age,but not genetic ancestry,predict fetal loss in a wild baboon hybrid zone

Objectives

Pregnancy failure represents a major fitness cost for any mammal, particularly those with slow life histories such as primates. Here, we quantified the risk of fetal loss in wild hybrid baboons, including genetic, ecological, and demographic sources of variance. We were particularly interested in testing the hypothesis that hybridization increases fetal loss rates. Such an effect would help explain how baboons may maintain genetic and phenotypic integrity despite interspecific gene flow.

Materials and Methods

We analyzed outcomes for 1020 pregnancies observed over 46 years in a natural yellow baboon-anubis baboon hybrid zone. Fetal losses and live births were scored based on records of female reproductive state and the appearance of live neonates. We modeled the probability of fetal loss as a function of a female's genetic ancestry (the proportion of her genome estimated to be descended from anubis [vs. yellow] ancestors), age, number of previous fetal losses, dominance rank, group size, climate, and habitat quality using binomial mixed effects models.

Results

Female genetic ancestry did not predict fetal loss. Instead, the risk of fetal loss is elevated for very young and very old females. Fetal loss is most robustly predicted by ecological factors, including poor habitat quality prior to a home range shift and extreme heat during pregnancy.

Discussion

Our results suggest that gene flow between yellow and anubis baboons is not impeded by an increased risk of fetal loss for hybrid females. Instead, ecological conditions and female age are key determinants of this component of female reproductive success.