Living near the limits: Effects of interannual variation in food availability on diet and reproduction in a temperate primate,the Taihangshan macaque (Macaca mulatta tcheliensis)

Nutrient intake of animals is influenced by an interplay of external and internal factors, such as food availability and reproductive state, respectively. We used the nutritional geometry framework to analyze individual-based data on energy and nutrient intake in relation to reproductive state in a population of rhesus macaques (Macaca mulatta tcheliensis), which live in a harsh high-latitude habitat, the Taihangshan mountains of China, and exhibit strong reproductive seasonality. We combined data over a 3-year period on food availability, diets, reproductive output, and components of maternal investment to understand how Taihangshan macaques respond to variation in food availability and nutrition in reproduction. Our results show there was high interannual variation in availability of an important staple source of fat and carbohydrates (nonprotein energy), seeds of oak (Quercus spp). Despite this variability in seed availability skewing the dietary macronutrient ratios considerably (from 12.96% to 30.12% dietary energy from protein), total metabolizable energy intake was maintained across years during pregnancy. Lactating females had higher mean daily energy intakes than pregnant females. As in pregnant females, energy intake was maintained constant across years, but only when seed availability enabled the contribution of available protein to energy intake to be maintained between 15.32% (2013) and 17.97% (2015). In 2014, when seeds were scarce, lactating females had a shortfall in energy intake compared with 2013 and 2015. This corresponded with a reduction in the number of females giving birth (11 out of 23), but there was no interannual difference in survival rates. Compared to 2013 and 2015, in 2014 females had greater weight loss (drew on body reserves), moved less, and spent more time nursing their offspring. We discuss implications of these results for range limitation in Taihangshan macaques.     

Effect of reproductive state and body size on food consumption in captive Galago senegalensis braccatus

Measurements of food consumption for different types of foods were made for seven Galago senegalensis braccatus. Differences because of reproductive state in females and body size were found. Lactating females consumed more food in total and had greater energy and protein intake than they did during other reproductive states. Near-term pregnant females consumed less food, energy, and protein than they did during other reproductive states. Body size affected food intake, with smaller animals ingesting more per unit metabolic weight than larger subjects.     

Resource base,parity, and reproductive condition affect females' feeding time and nutrient intake within and between groups of a baboon population

Summary We examined within- and between-group differences in aspects of feeding and nutrient intake among adult females of a single population of baboons (Papio cynocephalus) in Amboseli National Park, Kenya. Differences in time spent feeding, daily energy and protein intake and feeding efficiency (nutrient intake per minute spent feeding) reflected differences in resource base, reproductive condition and parity. Baboons that partially fed from a lodge garbage dump spent less than half the time feeding than those that were feeding totally in the wild. During this greatly reduced feeding time, the garbage-feeding group had a similar daily energy intake and only a slightly lower daily protein intake relative to wild-feeding baboons. Consequently, the feeding efficiency of the semi-provisioned baboons was appreciably higher than that of the non-provisioned baboons. For the totally wild-feeding baboons, samples were large enough to permit analyses of feeding time and nutrient intake during different reproductive states and parity. Females spent more time feeding and had higher daily energy and protein intake when they were pregnant or lactating than when they were sexually cycling. Nulliparous females spent more time feeding than their multiparous counterparts. The daily energy intake of nulliparous females was higher than that of their multiparous counterparts, but their daily protein intakes did not differ significantly. Pregnant or lactating and nulliparous females had higher feeding efficiency than their sexually cycling and multiparous counterparts. The two nulliparous females in the garbage-feeding group spent more time feeding but did not take in more energy or protein per day than their multiparous counterparts.     

Reproductive Energetics of Female Mantled Howlers (<Emphasis Type="Italic">Alouatta palliata</Emphasis>)

The energetic costs of reproduction have an important influence on the life histories of female primates. At present, however, the interplay of female reproductive state, food availability, and strategies aimed at maintaining energy balance has been described for only a few species, limiting our ability to understand intra- and interspecific variation in female life histories. We assessed how female mantled howlers (Alouatta palliata) are affected by reproductive seasonality, and whether they alter their behavior to cope with the energetic demands of reproduction. From August 2013 to July 2015 we measured the reproductive state, behavior (1100 h of focal animal observations), and energetic condition (312 urine samples collected for C-peptide analysis) of 7 adult females, and assessed food availability (weekly phenological sampling of 397 food trees). Female behavior did not vary with reproductive state or reproductive seasonality. There were, however, differences in how females responded to variation in food availability according to reproductive state. Cycling and gestating females spent more time feeding than lactating females, and cycling females less time resting than females in other reproductive states, when food was more available. C-peptide concentrations were unaffected by either individual or overall variation in reproductive state, except for cycling females, whose concentrations increased during periods of high food availability. The energetic condition of female mantled howlers is broadly maintained over different stages of reproduction, but is sensitive to variation in food availability.     

Female weight and reproductive condition in a population of olive baboons (Papio anubis)

The study reported here tested Altmann's prediction [Baboon Mothers and Infants. Cambridge, Harvard University Press, 1980] that lactating female baboons endure a weight loss. Data from 64 adult female olive baboons (Papio anubis) residing in six troops in Kenya revealed that reproductive condition was related to weight. Lactating females weighed less and pregnant females weighed more than cycling females. There was a negative correlation between the weight of cycling females and the number of months postweighing to their next conception. These results indicate that lactation in wild baboons imposes energy costs that result in lost weight. It is suggested that female baboons may have to surpass a minimum weight threshold prior to resumption of postlactational cycling and that nutritional status is more influential than rank in affecting female reproductive success.     

Energetics during reproduction: a doubly labeled water study of lactating baboons

Understanding the costs and regulation of reproduction in primates requires understanding the separate but linked effects of energy availability and total energy expenditure (TEE). We compared variation in TEE and energy intake (EI) between two periods, early lactation and after the resumption of sexual cycling, for eight females from two groups of normally reproducing colony-living baboons (Papio h. anubis). Total energy expenditure was assessed using the doubly labeled water method. TEE was correlated with maternal mass both during early lactation and after the resumption of cycling. TEE after the resumption of cycling was positively related to infant growth rates; mothers with rapidly growing infants had higher energy expenditure. TEE was however unrelated to maternal rank and only weakly associated with reproductive parameters such as delay to conception. EI in early lactation was related to infant mass and interbirth intervals, but unrelated to infant growth or reproductive parameters once cycling had resumed. Energy availability (EA; the difference between intake and expenditure) differed significantly between subordinate and dominant females during early lactation, was highly variable among individuals as a function of body composition, and is suggested to follow a nonlinear relationship as a complex function of social status, lactation stage, infant growth, and female fertility. Thus, as a consequence of reduced energy availability, subordinate females in this captive context may experience reproductive delays even though the total energy expenditure after the return of cycling was similar between high and low ranking females.     

The effect of supplemental food on the growth rates of neonatal,young, and adult cotton rats (Sigmodon hispidus) in northeastern Kansas,USA

In food-limited populations, the presence of extra food resources can influence the way individuals allocate energy to growth and reproduction. We experimentally increased food available to cotton rats (Sigmodon hispidus) near the northern limit of their range over a 2-year period and tested the hypothesis that seasonal growth rates would be enhanced by supplemental food during winter and spring when natural food levels are low. We also examined whether additional food resources were allocated to somatic growth or reproductive effort by pregnant and lactating females. The effect of supplemental food on growth varied with mass and season, but did not influence the growth rates of most cotton rats during spring and winter. In winter, small animals on supplemented grids had higher growth rates than small animals on control grids, but females in spring had lower growth rates under supplemented conditions. Growth rates of supplemented cotton rats were enhanced in summer. Northern cotton rat populations may use season-specific foraging strategies, maximizing energy intake during the reproductive season and minimizing time spent foraging in winter. Adult females invest extra resources in reproduction rather than in somatic growth. Pregnant females receiving supplemental food had higher growth rates than control females, and dependent pups (≤ 1 month of age) born to supplemented mothers had higher growth rates than those born to control mothers. Increased body size seems to confer an advantage during the reproductive season, but has no concomitant advantage to overwinter survival.     

Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques

Lactating female rats without their pups exhibit lower HPA responsiveness to stress than nonlactating females. However, responsiveness to stress is similar when lactating females are tested with their pups and the stressor involves a potential threat to the offspring. This study constitutes the first comparison of stress responsiveness in lactating and nonlactating female nonhuman primates. Subjects were 53 multiparous female free-ranging rhesus macaques. Approximately half of the females were lactating and half were nonpregnant/nonlactating. Blood samples were obtained after capture and after overnight housing in an individual cage. Lactating females were tested with their infants. Lactating females had significantly higher plasma cortisol levels than nonlactating females on both days. Having or not having an infant was also a better predictor of plasma cortisol levels among all females than their age, dominance rank, group of origin, time of day at which the sample was obtained, and time elapsed since beginning of the sampling procedure or since anesthesia. Plasma cortisol levels of lactating females were not significantly correlated with post-partum stage or with the cortisol levels of their infants. Capture, handling, and individual housing in a cage are powerful psychological stressors for free-ranging primates. We suggest that the higher plasma cortisol levels exhibited by lactating females reflect greater responsiveness to stress associated with perception of risks to infants. Hyporesponsiveness to stress may not be a general characteristic of lactation in all mammalian species, but a short-term effect of infant suckling that is most apparent with stressors unrelated to the offspring.     

Changes in female reproductive condition following male take-overs in a colony of hamadryas and hybrid baboons

This paper describes and discusses events observed in the Madrid colony of hamadryas and hybrid baboons, when a novel group of 3 adult males, 3 adult females and 1 unweaned infant was introduced to the resident colony comprising 12 adult females, 11 juveniles and 6 unweaned infants. Novel males took over resident adult females in any reproductive condition, and all acyclic females (i.e. lactating, pregnant and immature) exhibited a dramatic enhancement of sexual activity. Lactating females shortened their postpartum amenorrhoea periods and resumed oestrous cycles around day 14 following the introduction of the novel males, without infanticide occurring. Their return to breeding condition was not affected by the age of their current infant or the day they were taken over by the males. A female in an early stage of pregnancy aborted spontaneously and resumed oestrus on day 26. The other pregnant female significantly shortened her gestation time, delivered a viable infant on day 13, and resumed breeding activity 39 days post-partum (on day 52), while suckling her infant. A cycling female adopted and suckled a 74-day-old infant, continued showing oestrous cycles and conceived. Immature females reached menarche significantly earlier than expected and only then joined one of the newly established harem units. It is argued that the observed enhancement of sexual activity was not imposed by the males' aggressive behaviour but rather was a spontaneous female response to male novelty. This single causal factor was potent enough to override the role that nutrition and lactation normally play in the control of the females' reproductive activity. Differences in latency until the appearance of the response were probably due to the different constraints imposed by the female's current reproductive state. It was also hypothesized that when (a) sexual swellings are attractive to males, (b) novel males are especially active in the process of bonding with new females, and (c) males are important sources of coalitionary support, females might by developing sexual swellings compete more successfully against other females and attain a higher position in the female hierarchy of the newly established unit. This would have the ultimate effect of increasing their potential reproductive success. In several cases females did gain socially by coming into oestrus, but attained no immediate reproductive advantage.     

Field energetics of free-living, lactating and non-lactating echidnas (Tachyglossus aculeatus)

We measured daily energy expenditure (DEE) and water turnover rates in lactating and non-lactating short beaked echidnas (Tachyglossus aculeatus) using the doubly labelled water technique during the lactation period in spring. Reproductively inactive echidnas were on average significantly heavier (median: 3354 g; range: 2929-3780 g; N=4) than lactating females (median: 2695 g; range: 2690-2715 g; N=3) during the equivalent time period. The median water flux rate of lactating echidnas (152 ml day(-1); range: 120-198 ml day(-1)) did not differ significantly from that of non-lactating females (170 ml day(-1); range: 128-227 ml day(-1)). The median DEE of echidnas that were lactating was 645 kJ day(-1) (range: 581-850 kJ day(-1)), which was not different from the median DEE of non-reproductive control females (763 kJ day(-1); range: 720-766 kJ day(-1)). Lactating females somehow compensate for the energy costs of milk production, resulting in a daily energy budget that is not different from that of non-reproductive females. At least part of their energy minimising strategy could involve the use of moderate heterothermy, allowing a greater proportion of daily energy expenditure to diverted to milk production.     

Dominance and reproductive rates in captive female olive baboons, Papio anubis

The reproductive cycles of 23 captive olive baboons were studied over two successive parturitions. Interbirth intervals of 450 days were reduced by 60% in comparison to wild baboons, and consisted of 145 days of postpartum amenorrhea, 3.5 cycles, and a gestation of 185 days. Dominance rank was found to be one significant factor affecting female fertility. Low-ranking females had longer total intervals between successive births and, in particular, they experienced a longer delay to conception once they had resumed sexual cycles. Mothers of infants who were heavy for age resumed cycling more quickly and had fewer cycles before a subsequent conception. Mothers best able to sustain rapid early infant growth were those of high dominance rank and of high body mass; these females had more rapid reproductive rates. As female energy intake was unrelated to dominance, we suggest that social stresses are important suppressors of the hormonal and lactational competence of subordinate females.     

Dietary energetics of the insectivorous Mexican free-tailed bat (Tadarida brasiliensis) during pregnancy and lactation

Stomach content analysis of 20 pregnant (x body mass=13.4 g) and 18 lactating (x body mass=11.5 g) female Tadarida brasiliensis revealed that the diet, expressed as percent volume, consists largely of lepidopterans, coleopterans, hymenopterans, and dipterans, in decreasing order of importance. We found no significant difference in the diet of pregnant and lactating females when expressed as percent volume. However, when expressed as percent frequency, proportionately more pregnant females fed on lepidopterans, coleopterans, and dipterans than did lactating bats, and proportionately more lactating females fed on hymenopterans. We found no significant differences in the percentages of water, lean dry mass, fat, and energy density in the stomach contents of pregnant and lactating females. Water in stomach contents averaged 62.7% and fat and lean dry mass averaged 22.2% and 15.2%, respectively (expressed as percentage of wet mass); energy density averaged 31.2 kJ g^–1 dry mass. This relatively high energy density of stomach contents, as compared to whole insects, can be attributed to the consumption of insects high in fat (especially flying ants) and the abdomens only of moths and beetles (other body parts being discarded). Estimates of nightly food intake increased markedly from mid- to late pregnancy, stabilized or decreased during late pregnancy, and increased again during early to mid-lactation. Average nightly feeding rate doubled from pregnancy to lactation and increased threefold during the first half of lactation. By adjusting our gravimetric estimates of nightly feeding rate upwards by 40% (based on estimates of field metabolic rate), we estimate that the average nightly energy intake of female T. brasiliensis ranges from 57 kJ day^–1 in early lactation to 104 kJ day^–1 in mid-lactation. These estimates represent nightly feeding rates averaging 39% and 73% of a female's body mass in the period from early to mid-lactation, respectively.     

Habitat choice of Grevy's zebras (Equus grevyi) in Laikipia, Kenya

Characterizing habitat choice is essential for endangered species conservation. For the endangered Grevy's zebra ( Equus grevyi ), as with many widely ranging vertebrates, human activities may be an important factor affecting space use. Grevy's zebras are grazing ungulates inhabiting the savannahs of central-northern Kenya and Ethiopia. Past research on their social organization indicates that reproductive status shapes associations and movements. Here, we examine how habitat use varies across four reproductive classes: lactating and nonlactating females, bachelors and territorial males. We also test whether Grevy's zebra avoid locations close to active livestock corrals, or bomas . We find that forage quality, forage quantity and habitat openness of locations used by Grevy's zebra vary significantly depending on individual reproductive state. Lactating females and bachelors use areas with green, short grass and medium-dense bush more frequently than nonlactating females or territorial males. We hypothesize that lactating females trade off forage quantity and safety to access nutrients in growing grass. Across reproductive classes, Grevy's zebra choose locations further from active bomas than if they used the area randomly. Our results suggest that Grevy's zebra may require a range of vegetation characteristics for different reproductive classes. Further, they may need areas free from competition or disturbance by livestock.     

Foraging decisions in a capital breeder: trade-offs between mass gain and lactation

The high energetic costs of lactation can lead to fundamental trade-offs in life-history traits, particularly in young females that reproduce before completing body growth. We assessed whether lactating female mountain goats (Oreamnos americanus) used behavioural tactics at fine spatio-temporal scales to increase energy intake to compensate for the costs of lactation. Lactating females increased bite rate and chewing rate compared with non-lactating females, but selected similar foraging sites in terms of plant quality and abundance. At peak lactation, forage intake of lactating females was >40% greater than that of non-lactating females. For females that had reached asymptotic body mass (i.e. ≥6 years old), summer mass gain of lactating females was similar to that of non-lactating females. At 4 and 5 years of age, however, daily mass gain of lactating females was about 20% lower than that of non-lactating females. We conclude that increased foraging may allow fully-grown lactating females to compensate for the energetic costs of lactation, but that there is a major trade-off between mass gain and lactation for younger females. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Energy intake, energy expenditure, and reproductive costs of female wild golden lion tamarins (Leontopithecus rosalia)

Callitrichid females are often described as energetically constrained. We examined the energy budgets of 10 female wild golden lion tamarins (GLTs, Leontopithecus rosalia) in an effort to understand how energy intake and expenditure might influence physical condition and therefore reproductive performance. We used focal animal sampling to record behavioral data and conducted energy analyses of foods consumed by GLTs to estimate intake and expenditure. We used two-tailed Wilcoxon signed-rank tests to compare intake in the reproductive vs. nonreproductive period and expenditure in the reproductive vs. nonreproductive period. Energy intake decreased during the reproductive period compared to the nonreproductive period. While total expenditure did not vary significantly across the two periods, females spent more time and therefore expended significantly more energy engaged in energetically inexpensive behaviors (i.e., sleeping or being stationary) during the reproductive period compared to the nonreproductive period. We suggest that reproductive female GLTs may adopt a reproductive strategy that includes high intake prior to pregnancy and lactation, and energy conservation during pregnancy and lactation.     

Microhabitat Variation and Its Effects on Dietary Composition and Intragroup Feeding Interactions Between Adult Female <Emphasis Type="Italic">Lemur catta</Emphasis> During the Dry Season at Beza Mahafaly Special Reserve,Southwestern Madagascar

We compared diets and female feeding agonism in 2 groups of ring-tailed lemurs living in markedly diverse microhabitats in and near the Beza Mahafaly Reserve, Madagascar during mid-to-late gestation periods and height of the dry season to test predictions concerning differences in resource availability, preferred foods, female rank, and degree and frequency of feeding agonism in relation to usurpability and monopolization of food resources. Quadrat sampling in disturbed forest habitat revealed a greater number of plant species than in the gallery forest home range area, but females in both groups consumed nearly equal numbers of actual food plant species. Higher-ranking females in disturbed forest consumed human food scraps from the researchers camp significantly more often than low-ranking females did, while there was no rank effect for consumption of any food type between females in the gallery forest group. Higher rates of female feeding agonism in both groups occurred around usurpable fruit and leaves, as well as over monopolizable human food scraps in the disturbed forest group. There is no association between degree of agonism and food type in either group, and rate of feeding agonism is similar for both groups. The most highly contested food items came in large packages and were high in nutrients: beneficial foods for gestating females in the height of dry season in southwestern Madagascar.     

The effects of lactation and infant care on adult energy budgets in wild siamangs (Symphalangus syndactylus)

In mammals with biparental care of offspring, males and females may bear substantial energetic costs of reproduction. Adult strategies to reduce energetic stress include changes in activity patterns, reduced basal metabolic rates, and storage of energy prior to a reproductive attempt. I quantified patterns of behavior in five groups of wild siamangs (Symphalangus syndactylus) to detect periods of high energetic investment by adults and to examine the relationships between infant care and adult activity patterns. For females, the estimated costs of lactation peaked at around infant age 4–6 months and were low by infant age 1 year, whereas the estimated costs of infant‐carrying peaked between ages 7 and 12 months, and approached zero by age 16 months. There was a transition from primarily female to male care in the second year of life in some groups. Females spent significantly less time feeding during lactation than during the later stages of infant care, suggesting that female siamangs do not use increased food intake to offset the costs of lactation. Female feeding time was highest between infant ages 16 and 21 months, a period of relatively low female investment in the current offspring that coincided with the period of highest male investment in infant care. This suggests that male care may reduce the costs of infant care for females in the later stages of a reproductive attempt. The female energy gain resulting from male care was likely invested in somatic maintenance and future reproduction, rather than the current offspring. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Sex and reproductive stage differences in the growth,metabolism, feed,fecal production,excretion and energy budget of the Amazon River prawn (Macrobrachium amazonicum)

The aim of this study was to evaluate differences in various physiological measures (growth, fecal production, feed intake, nitrogenous excretion, oxygen consumption, energy substrate used, and energy budget) among males, ovigerous females and non-ovigerous females of the freshwater prawn Macrobrachium amazonicum. This species exhibits pronounced sexual dimorphism and different male morphotypes and has the potential for use in aquaculture. Males and non-ovigerous females were studied for 30?days. Ovigerous females were studied for 10?days. Prawns were fed commercial prawn food, and all males were of the Translucent Claw (TC) morphotype. The results demonstrate physiological differences both between males and females and between females of different reproductive stages. Males had higher rates of ingestion, growth and oxygen consumption and less fecal loss than females. We postulate that in the absence of other morphotypes, TC males may exhibit increased growth rates. Males and females used protein as an energy substrate. Males channeled approximately 9% of their energy budget into growth, whereas non-ovigerous and ovigerous females channeled only 1.4?±?0.4 and 0.07?±?0.07%, respectively. Whereas males and non-ovigerous females channeled 9.0?±?9.74 and 61.8?±?3.0%, respectively, of the energy ingested into metabolism, ovigerous females channeled 97.7?±?4.7% into metabolism, likely due to the frequent beating of their pleopods, which oxygenates and cleans the eggs. As reported for marine prawns, males and non-ovigerous females of M. amazonicum lost approximately 5% of their ingested energy in exuviae. The physiological differences observed between the sexes and between females of different reproductive stages might reflect corresponding differences in patterns of activity, growth, and reproduction.     

Severe Aggression Among Female Pan troglodytes schweinfurthii at Gombe National Park, Tanzania

Aggression is generally more severe between males than between females because males gain greater payoffs from escalated aggression. Males that successfully defeat rivals may greatly increase their access to fertile females. Because female reproductive success depends on long-term access to resources, competition between females is often sustained but low key because no single interaction leads to a high payoff. Nonetheless, escalated aggression can sometimes immediately improve a female’s reproductive success. Resisting new immigrants can reduce feeding competition, and infanticide of other females’ young can increase a female’s access to resources. East African chimpanzees live in fission-fusion communities in which females occupy overlapping core areas. Growing evidence indicates that reproductive success correlates with core area quality, and that females compete for long-term access to core areas. Here we document 5 new cases of severe female aggression in the context of such competition: 2 attacks by resident females on an immigrant female, a probable intracommunity infanticide, and 2 attacks on a female and her successive newborn infants by females whose core areas overlapped hers. The cases provide further evidence that females are occasionally as aggressive as males. Factors influencing the likelihood and severity of such attacks include rank and size differences and the presence of dependable allies. Counterstrategies to the threat of female aggression include withdrawing from others around the time of parturition and seeking male protection. We also discuss an unusual case of a female taking the newborn infant of another, possibly to protect it from a potentially infanticidal female.     

Reproductive patterns and birth seasonality in a South-American breeding colony of common marmosets,Callithrix jacchus

We analyzed data on captive-born and wild-caught females housed under natural conditions in a colony located in northeastern Brazil. No differences in reproductive performance were found between captive-born and wild-caught females. Twins were the most frequent litter size, followed by triplets and singletons. No parity effect was observed, with similar infant survival for nulliparous and multiparous females. No significant departures in sex ratio were detected for births and mortality of the male and female infants. The age of the females at the time of pairing showed a negative correlation with pairing-parturition length, but did not affect infant survival. The prolongation in pairing-parturition interval (PPI) and interbirth interval (IBI) was related to birth seasonality. The births were clustered in the second half of the dry season and the beginning of the wet season (November–March), and the time of pairing and the time of infant birth influenced the PPI and IBI, respectively. The use of outdoor cages, which allowed the animals to be aware of the seasonal variations in photo-period and rainfall seems to be sufficient to time the reproductive activity, even when the animals are maintained on a constant food supply.