Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans

Assessment of energetic condition is a critical tool for behavioral and reproductive ecologists. However, accurate quantification of energy intake and expenditure is labor-intensive, and it can be problematic for field scientists to obtain regular data on individual animals. C-peptide, a polypeptide segment of the proinsulin molecule that is secreted along with insulin in an equimolar relationship, can be measured in urine, and thus offers a potential means for the non-invasive assessment of energy balance in wild animals. Here, we validate C-peptide for the quantification of energetic condition, with specific application to wild orangutans (Pongo pygmaeus). We determined that application of urine to filter paper results in significantly lower C-peptide recoveries versus fresh samples. However, concentrations in filter paper samples were significantly correlated with fresh urine and were stable over various storage conditions and durations. We compared the C-peptide concentrations from wild orangutan urine samples with three independent measures of energetic condition: ketone bodies (urinalysis), caloric intake (nutritional biochemistry), and food availability (phenology). As expected, C-peptide concentrations were significantly lower in samples that tested positive for ketones in the field. Monthly average C-peptide concentrations of both male and female orangutans were significantly correlated with monthly determinations of energy intake and food availability. Therefore, we conclude that the collection and preservation of urine samples for C-peptide analysis are feasible under most field conditions and, in this species, presents a useful tool for assessing changes in energy balance.     

Potential applications of urinary C-peptide of insulin for comparative energetics research

The study of comparative energetics offers a valuable way to identify broad ecological principles and assess the functional significance of energetic adaptations during the course of evolution. Yet, the quantification of energetic status for nonhuman primates under natural conditions remains one of the most challenging aspects of comparative energetics research. Here, we report on the development of a noninvasive field method for measuring energetic status in great apes, humans, and possibly other nonhuman primates. Specifically, we have explored measurement of a urinary metabolite of insulin (C-peptide) as a physiological marker of energetic condition in chimpanzees and orangutans. We performed three validation studies and successfully measured C-peptide in urine samples from captive chimpanzees, wild chimpanzees, and wild orangutans. Urinary C-peptide measures gave indications of being a reliable signal of energetic status in both species. For chimpanzees and orangutans in the wild, baseline urinary C-peptide levels were higher during periods of fruit abundance than periods of low fruit availability. Urinary C-peptide levels were also higher for well-fed captive chimpanzees compared with wild chimpanzees. Although sample size was small, top-ranking male chimpanzees showed higher C-peptide levels in the wild than low-ranking males only during the period of fruit abundance. These preliminary results indicate that further development of the urinary C-peptide method could expand opportunities to quantify energetic condition for great apes in the wild and generate new data for comparative research. We highlight specific applications for studying great ape reproduction as well as the nutritional ecology of human foragers.     

Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees

C-peptide of insulin presents a promising new tool for behavioral ecologists that allows for regular, non-invasive assessment of energetic condition in wild animals. C-peptide is produced on an equimolar basis with insulin, thus is indicative of the body's response to available glucose and, with repeated measurement, provides a biomarker of energy balance. As yet, few studies have validated the efficacy of C-peptide for monitoring energy balance in wild animals. Here, we assess seasonal and interindividual variation in urinary C-peptide concentrations of East African chimpanzees (Pan troglodytes schweinfurthii). We assayed 519 urine samples from 13 adult male chimpanzees in the Kanyawara community of Kibale National Park, Uganda. C-peptide levels were significantly predicted by the total amount of fruit and the amount of preferred fruit in the diet. However, chimpanzees had very low C-peptide titers during an epidemic of severe respiratory illness, despite highly favorable feeding conditions. Kanyawara males had significantly lower C-peptide levels than males at Ngogo, a nearby chimpanzee community occupying a more productive habitat. Among Kanyawara males, low-ranking males had consistently higher C-peptide levels than dominant males. While counterintuitive, this result supports previous findings of costs associated with dominance in male chimpanzees. Our preliminary investigations demonstrate that C-peptide has wide applications in field research, providing an accessible tool for evaluating seasonal and individual variation in energetic condition, as well as the costs of processes such as immune function and reproduction.     

Urinary C-peptide measurement as a marker of nutritional status in macaques

Studies of the nutritional status of wild animals are important in a wide range of research areas such as ecology, behavioural ecology and reproductive biology. However, they have so far been strongly limited by the indirect nature of the available non-invasive tools for the measurement of individual energetic status. The measurement of urinary C-peptide (UCP), which in humans and great apes shows a close link to individual nutritional status, may be a more direct, non-invasive tool for such studies in other primates as well and possibly even in non-primate mammals. Here, we test the suitability of UCPs as markers of nutritional status in non-hominid primates, investigating relationships between UCPs and body-mass-index (BMI), skinfold fatness, and plasma C-peptide levels in captive and free-ranging macaques. We also conducted a food reduction experiment, with daily monitoring of body weight and UCP levels. UCP levels showed significant positive correlations with BMI and skinfold fatness in both captive and free-ranging animals and with plasma C-peptide levels in captive ones. In the feeding experiment, UCP levels were positively correlated with changes in body mass and were significantly lower during food reduction than during re-feeding and the pre-experimental control condition. We conclude that UCPs may be used as reliable biomarkers of body condition and nutritional status in studies of free-ranging catarrhines. Our results open exciting opportunities for energetic studies on free-ranging primates and possibly also other mammals.     

Effects of captivity and body condition on plasma corticosterone, locomotor behavior, and plasma metabolites in curve-billed thrashers

The acute stress response involves the secretion of catabolic glucocorticoids, such as corticosterone (CORT) in birds, that mobilize intrinsic energy stores primarily through a gluconeogenic pathway involving fat breakdown, thus linking body condition and stress. We measured changes in CORT and gluconeogenic metabolites (triglycerides, free glycerols, glucose) during handling stress in curve-billed thrashers Toxostoma curvirostre from two habitats (urban vs. desert) that may differ in food abundance in the wild, in captivity, and in response to both food restriction and subsequent recovery. Urban thrashers were heavier and secreted more CORT than desert birds in the field, but differences did not persist in captivity. Decreased access to food resulted in decreased body mass and a diminished ability to elevate plasma CORT in response to handling stress. However, the opposite effect was observed as these birds recovered from food restriction. Plasma levels of glucose and triglycerides did not change with stress. Food restriction also increased locomotor activity, which likely further exacerbated energy loss. These observations suggest that body condition and stress differences between urban and desert birds may be related to differences in their relative energetic states, possibly due to food availability. Body condition may affect the extent to which an individual can elevate CORT and use free glycerol as energy during acute stress.     

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.     

Photoperiod and food restriction differentially affect reproductive and immune responses in Siberian hamsters Phodopus sungorus

1.  Organisms must contend with seasonal fluctuations in energy availability. To maintain a positive energy balance year-round, a number of adaptations have evolved including seasonal changes in reproduction, energetics and immunity. Photoperiod is the primary environmental signal most animals use to predict seasonal events. Despite the established link between energetics and immune function, little is known regarding how changes in energy availability affect immunity.
2.  The goal of the present study was to determine the effects of food restriction on photoperiodic changes in reproduction and immune function in the Siberian hamster ( Phodopus sungorus ). Adult hamsters were housed in long or short days and were food restricted or fed ad libitum . Immune responses were quantified by measuring specific antibody production and bacterial killing capacity.
3.  Food restriction decreased body and relative reproductive masses in long-day animals. Antibody responses, but not bacterial killing ability, were enhanced in food restricted short-day animals as compared with ad libitum fed controls. We also found differential effects of body fat on immune responses depending on the immune measure.
4.  The effects of food restriction on immune function appear to vary based on the restriction regimen, the response measured, and the physiological state of the organism including energy balance, metabolic rate and reproductive status.
5.  In conclusion, these results suggest that a wide range of factors can differentially affect immune function. In addition, these effects may vary based on the specific response examined. Future studies should include a variety of measurements to provide a more integrative and accurate picture of reproductive, energetic, and photoperiodic effects on immune function.     

Hormone changes indicate that winter is a critical period for food shortages in Steller sea lions

Given that many marine mammals display seasonal energetic priorities, it is important to investigate whether the impact of unexpected food restriction differs during the year. Steller sea lions (Eumetopias jubatus) fed restricted diets for up to 9 days during spring, summer, fall, and winter lost an average of 10% of their initial body mass. We tracked changes in the levels of three hormones (cortisol, total thyroxine-TT4, total triiodothyronine-TT3) and one blood metabolite (blood urea nitrogen-BUN) following a food restriction in relation to season, body mass, body composition, and metabolism. Degree of changes in cortisol, TT3, and BUN after food restriction was significantly affected by season. The greatest changes in cortisol (+231%), BUN (+11.4%), TT4 (-23.3%), and TT3 (-35.6%) occurred in the winter (November/December) when rates of body mass loss were also greatest. Changes in cortisol levels were positively related to total body mass loss, while changes in TT3 levels were negatively related. While greater increases in BUN were related to greater rates of mass loss, the use of BUN levels as an indicator of metabolic state is complicated by the type and level of food intake. The observed changes in hormone levels support morphological data suggesting Steller sea lions may be more strongly impacted by short-term, reduced energy intake during winter than at other times of the year.     

Urinary C-peptide levels in male bonobos (Pan paniscus) are related to party size and rank but not to mate competition

Within- and between-species variation in male mating strategies has been attributed to a multitude of factors including male competitive ability and the distribution of fertile females across space and time. Differences in energy balance across and within males allow for the identification of some of the trade-offs associated with certain social and mating strategies. Bonobos live in groups with a high degree of fission–fusion dynamics, there is co-dominance between the sexes and a linear dominance hierarchy among males. Males compete over access to females, breeding is aseasonal, and females exhibit sexual swellings over extended time periods. In this study we use urinary C-peptide (UCP) levels in male bonobos (Pan paniscus) obtained from 260 urine samples from a wild bonobo community, to quantify male energy balance during mate competition and levels of gregariousness in the species. Although high ranking males are more aggressive, spend more time in proximity to maximally tumescent females, and have higher mating frequencies, we found no indication that mate guarding or mate competition affected male energy balance. Our results showed a positive correlation between monthly mean UCP levels and mean party size. When traveling in large parties, high ranking males had higher UCP levels than those of the low ranking males. These results support the hypothesis that patterns of fission–fusion dynamics in bonobos are either linked to energy availability in the environment or to the energetic costs of foraging. The finding of a rank-bias in UCP levels in larger parties could also reflect an increase in contest competition among males over access to food.     

Food restriction affects maternal investment but not neonate phenotypes in a viviparous lizard

Food availability significantly affects an animal's energy metabolism,and thus its phenotype,survival,and reproduction.Maternal and offspring responses to food conditions are critical for understanding population dynamics and life-history evolution of a species.In this study,we conducted food manipulation experiments in field enclosures to identify the effect of food restriction on female reproductive traits and postpartum body condition,as well as on hatchling phenotypes,in a lacertid viviparous lizard from the Inner Mongolian desert steppe of China.Females under low-food availability treatment (LFT) had poorer immune function and body condition compared with those under high-food availability treatment (HFT).The food availability treatments significantly affected the litter size and litter mass of the females,but not their gestation period in captivity or brood success,or the body size,sprint speed,and sex ratio of the neonates.Females from the LFT group had smaller litter sizes and,therefore,lower litter mass than those from the HFT group.These results suggest that female racerunners facing food restriction lay fewer offspring with unchanged body size and locomotor performance,and incur a cost in the form of poor postpartum body condition and immune function.The flexibility of maternal responses to variable food availability represents an important life strategy that could enhance the resistance of lizards to unpredictable environmental change.     

食物限制对雄性大绒鼠能量代谢特征的影响

为探讨横断山区大绒鼠适应食物匮乏的适应对策,将成年雄性大绒鼠随机分为自由取食组和饲喂正常摄食量的80% 限食组。测定了自由取食组和限食组雄性大绒鼠的体重、静止代谢率、非颤抖性产热以及体脂含量、血清瘦素含量、肝脏鲜重、褐色脂肪组织重量和消化道形态。结果显示:限食使雄性大绒鼠的体重、体脂含量、静止代谢率、非颤抖性产热、褐色脂肪组织重量和大肠、小肠长度显著降低,使盲肠内容物重量显著增加。血清瘦素含量与体重、体脂含量呈极显著正相关。在限食条件下,大绒鼠主要通过降低体重、基础代谢和产热的能量支出以及动用体内脂肪以应对食物资源短缺的环境条件,瘦素可能参与了能量代谢和体重的适应性调节。     

随机限食和重喂食小鼠能量收支和生长发育的可塑性

为阐明能量收支和生长发育的可塑性对动物适应食物资源变化的作用和意义,将断乳后的雄性KM小鼠40只随机限食4周,再重喂食4周。采用封闭式流体压力呼吸计测定基础代谢率(BMR)。限食使摄食量显著增加,BMR和活动行为降低,胴体和生殖腺重量显著降低。重喂食后上述指标均恢复到对照组水平,表现出显著的可塑性变化。结果表明,KM小鼠能通过摄食量、BMR、活动行为和身体组成的可塑性调节以适应难以预测的食物资源变化。     

Immune Activity,Body Condition and Human-Associated Environmental Impacts in a Wild Marine Mammal

Within individuals, immunity may compete with other life history traits for resources, such as energy and protein, and the damage caused by immunopathology can sometimes outweigh the protective benefits that immune responses confer. However, our understanding of the costs of immunity in the wild and how they relate to the myriad energetic demands on free-ranging organisms is limited. The endangered Galapagos sea lion (Zalophus wollebaeki) is threatened simultaneously by disease from domestic animals and rapid changes in food availability driven by unpredictable environmental variation. We made use of this unique ecology to investigate the relationship between changes in immune activity and changes in body condition. We found that during the first three months of life, changes in antibody concentration were negatively correlated with changes in mass per unit length, skinfold thickness and serum albumin concentration, but only in a sea lion colony exposed to anthropogenic environmental impacts. It has previously been shown that changes in antibody concentration during early Galapagos sea lion development were higher in a colony exposed to anthropogenic environmental impacts than in a control colony. This study allows for the possibility that these relatively large changes in antibody concentration are associated with negative impacts on fitness through an effect on body condition. Our findings suggest that energy availability and the degree of plasticity in immune investment may influence disease risk in natural populations synergistically, through a trade-off between investment in immunity and resistance to starvation. The relative benefits of such investments may change quickly and unpredictably, which allows for the possibility that individuals fine-tune their investment strategies in response to changes in environmental conditions. In addition, our results suggest that anthropogenic environmental impacts may impose subtle energetic costs on individuals, which could contribute to population declines, especially in times of energy shortage.     

Predicting abundance–body size relationships in functional and taxonomic subsets of food webs

Abundance–body size relationships are widely observed macroecological patterns in complete food webs and in taxonomically or functionally defined subsets of those webs. Observed abundance–body size relationships have frequently been compared with predictions based on the energetic equivalence hypothesis and, more recently, with predictions based on energy availability to different body size classes. Here, we consider the ways in which working with taxonomically or functionally defined subsets of food webs affected the relationship between the predicted and observed scaling of biomass and body mass in sediment dwelling benthic invertebrate communities at three sites in the North Sea. At each site, the energy available to body size classes in the “whole” community (community defined as all animals of 0.03125–32.0 g shell-free wet weight) and in three subsets was predicted from estimates of trophic level based on nitrogen stable isotope analysis. The observed and predicted scalings of biomass and body size were not significantly different for the whole community, and reflected an increase in energy availability with body size. However, the results for subsets showed that energy availability could increase or decrease with body size, and that individuals in the subsets were likely to be competing with individuals outside the subsets for energy. We conclude that the study of abundance–body mass relationships in functionally or taxonomically defined subsets of food webs is unlikely to provide an adequate test of the energetic equivalence hypothesis or other relationships between energy availability and scaling. To consistently and reliably interpret the results of these tests, it is necessary to know about energy availability as a function of body size both within and outside the subset considered.     

Insulin Levels,Physical Activity,and Urinary Catecholamine Excretion of Obese and Non-Obese Rhesus Monkeys

The hypothesis that spontaneous obesity in rhesus monkeys is associated with abnormalities in energy expenditure was tested. Obese (n=7) and non-obese (n=5) monkeys were described in terms of body size and composition, food intake, and physical activity. Additionally, the relationships among fasting and stimulated insulin levels in serum, C-peptide levels in serum and urine, and urinary catecholamines were examined. Obese animals had primarily abdominal deposition of excess body fat, as indicated by markedly elevated abdominal circumferences and skin-fold thicknesses. Food intake did not differ between groups. Physical activity was much lower in the obese group. Obese monkeys had markedly higher serum insulin and C-peptide levels in the fasted state and in response to an intravenous glucose challenge. Urinary excretion of C-peptide and catecholamines was measured during successive 2-day periods of ad libitum feeding, food deprivation, and refeeding in order to examine potential differences between groups in sympathoadrenal activity and their relationship to insulin secretion. C-peptide excretion was greater for obese and decreased for both groups during food deprivation. Urinary dopamine (DA), norepinephrine (NE), and epinephrine (E) levels were significantly greater for obese animals in all conditions. DA excretion was lowest during deprivation and E excretion was lowest during refeeding, whereas NE excretion was relatively unaffected by feeding condition. The overall patterns of C-peptide and catecholamine excretion were qualitatively similar for both groups, and there were no reliable differences between obese and non-obese in their responses to the feeding manipulation. The results suggest that hyperinsulinemia associated with obesity in rhesus monkeys is linked to increased catecholamine secretion and a resistance to cate-cholaminergic action.     

Lipid dynamics in the viperine snake, Natrix maura, from the Ebro Delta (NE Spain)

Body reserves play a major role in several aspects of vertebrate biology. Accurate identification and quantification of body reserves constitute a useful contribution to the better understanding of the energetic costs of reproduction and the implication of food availability in life history traits of organisms. In this study, lipid content in fat bodies, liver and muscle of the viperine snake (Natrix maura) were measured along an active season. Samples were collected monthly from a natural population of the Ebro Delta Natural Park (NE Spain). This methodology pointed out that lipids stored in fat bodies were the main energetic source during reproduction. In addition, lipids stored in liver appeared to be critical for vitellogenesis, while lipids stored in muscle turned out to be a supplementary energetic resource to fuel reproductive effort. Relationships between changes in body reserves and prey availability in canals of the Ebro Delta were also considered. In males, lipid reserves presented a positive correlation with food availability. On the contrary, lipid reserves in female viperine snakes decreased during vitellogenesis even though food availability increased in this period, which suggests a quick transfer of body lipids to clutch. In April, when rice fields of the Ebro Delta were dry and aquatic prey was scarce for viperine snakes, males and females presented a lower lipid content in fat bodies, liver and muscle than they did in other months, showing a clear link between prey availability and body reserves during food shortage. Thus, patterns of variation in fat levels indicated that Natrix maura is a capital breeder since it acquires resources in advance and stores them until they are invested during the reproductive period. Nevertheless, the shortage in April forces Natrix maura to turn into a facultative income breeder to fuel vitellogenesis. Finally, fat reserves in body components were compared with an estimate of body condition calculated by the residuals from the regression of body mass on body length. In male viperine snakes, the estimate of body condition was correlated with fat levels, revealing that this index is useful to measure condition in living individuals. On the contrary, body condition in females was not correlated with fat levels, which suggests that it is not appropriate to infer condition in female viperine snakes since it depends on the reproductive status of the individuals.     

Examining the potential for nutritional stress in young Steller sea lions: physiological effects of prey composition

The effects of high- and low-lipid prey on the body mass, body condition, and metabolic rates of young captive Steller sea lions (Eumetopias jubatus) were examined to better understand how changes in prey composition might impact the physiology and health of wild sea lions and contribute to their population decline. Results of three feeding experiments suggest that prey lipid content did not significantly affect body mass or relative body condition (lipid mass as a percent of total mass) when sea lions could consume sufficient prey to meet their energy needs. However, when energy intake was insufficient to meet daily requirements, sea lions lost more lipid mass (9.16±1.80 kg±SE) consuming low-lipid prey compared with eating high-lipid prey (6.52±1.65 kg). Similarly, the sea lions lost 2.7±0.9 kg of lipid mass while consuming oil-supplemented pollock at maintenance energy levels but gained 5.2±2.7 kg lipid mass while consuming identical energetic levels of herring. Contrary to expectations, there was a 9.7±1.8% increase in metabolism during mass loss on submaintenance diets. Relative body condition decreased only 3.7±3.8% during periods of imposed nutritional stress, despite a 10.4±4.8% decrease in body mass. These findings raise questions regarding the efficacy of measures of relative body condition to detect such changes in nutritional status among wild animals. The results of these three experiments suggest that prey composition can have additional effects on sea lion energy stores beyond the direct effects of insufficient energy intake.     

Experimental manipulation of food availability leads to short‐term intra‐clutch adjustment in egg mass but not in yolk androgen or thyroid hormones

In birds, mothers can affect their offspring's phenotype and thereby survival via egg composition. It is not well known to what extent and time‐scales environmental variation in resource availability, either via resource constrains or adaptive adjustment to predicted rearing conditions, influences maternal effects. We experimentally studied whether egg and yolk mass and yolk hormone levels respond to short‐term changes in food availability during laying in wild great tits Parus major. Our treatment groups were: 1) food supplementation (mealworms) from the 1st until the last egg; 2) food supplementation from the 1st until the 5th egg, where the effect of cessation of the supplementary food treatment could also be studied; 3) no food supplementation (controls). We analysed both nutritional resources (egg, yolk and albumen mass), and the important developmental signals, yolk androgens (testosterone and androstenedione), and for the first time in a wild population, yolk thyroid hormones (thyroxine and 3,5,3′‐triiodothyronine). Egg mass is a costly resource for females, androgens most likely non‐costly signals, whereas thyroid hormones may be costly signals, requiring environmental iodine. In the food supplemented group egg, yolk and albumen mass increased rapidly relative to controls and when food supplementation was halted, egg and albumen mass decreased, indicating rapid responses to resource availability. Yolk androgen and thyroid hormone levels were not affected by food supplementation during laying. Thyroxine showed an increase over the laying sequence and its biological meaning needs further study. The rapid changes in egg mass to variation in within‐clutch food availability suggest energetic/protein/nutrient constrains on egg formation. The lack of a response in yolk hormones suggest that perhaps in this species the short‐term changes in resource availability during egg laying do not predict offspring rearing conditions, or (for thyroid hormones) do not cause systemic changes in circulating hormones, and hence do not affect maternal signaling.     

Resource allocation in Wilson's storm-petrels<Emphasis Type="Italic"> Oceanites oceanicus</Emphasis> determined by measurement of glucocorticoid excretion

When resources are limited, life-history theory predicts that long-lived animals should allocate available resources to body maintenance rather than to reproduction in order to maximise their lifetime reproductive success. In the present study, we estimated physiological stress in a small procellariiform seabird, the Wilson's storm-petrel Oceanites oceanicus, as a means of understanding how limited resources are partitioned between provisioning parents and their chicks. We analysed adrenocortical activity of Wilson's storm-petrels during the breeding season by measuring glucocorticoid (GC) excretion, using an enzyme immunoassay measuring tetrahydrocorticosterone concentrations in extracts of faeces and urine of chicks and adults. Faecal GC measures were negatively correlated with chick body condition, suggesting that measures of tetrahydrocorticosterone in faeces and urine can be used to assess adrenal activity characteristic for physiological stress in Wilson's storm-petrels. In the breeding season of 1999, the colony was subject to low food availability, and the faecal and urine GC levels of chicks were elevated during these months of chronic starvation. In contrast, adults did not show elevated GC levels. The data thus suggest that Wilson's storm-petrels respond to unfavourable conditions by maintaining their own body condition and reducing provisioning of food to their chicks. Communicated by R.F. Oliviera     

Testosterone and energetics in wild chimpanzees (Pan troglodytes schweinfurthii)

Ovarian function in female hominoids is sensitive to both energy flux and energy balance, resulting in a reduced probability of conception during periods when a successful reproductive outcome is less likely. However, the extent to which energetic factors constrain gonadal function in male hominoids is not clear. We examined the effects of both acute and chronic variation in energy availability on urinary testosterone (T) levels in adult male chimpanzees. Acute changes in energy availability, which were assayed by means of observational data on feeding behavior, did not result in decreased T production for 11 individuals at Kibale National Park, Uganda. Chronic energy shortages, on the other hand, may be associated with lower T levels in this population. Adult males in Kibale (n=11), who maintain suboptimal access to energy, exhibit significantly lower urinary T levels than males in captivity (n=11), who are more sedentary and better fed. These results suggest that data on hormonal function in captive chimpanzees should be interpreted with caution because individuals may produce T at levels well above those that are typical in the wild. They also suggest that short-term variations in T levels in male hominoids are more likely to be explained by social factors than by energetic ones.