Balancing contest competition,scramble competition,and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus)

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within‐group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as “single female dominance,” with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.     

Relation of Food Intake Behaviors and Obesity Development in Young Common Marmoset Monkeys

Objective : Increasing prevalence of childhood obesity and associated risks of adult type disease have led to worldwide concern. It remains unclear how genetic predisposition, environmental exposure to obesogenic food, and developmental programming interact to lead to overweight and obese children. The development of a nonhuman primate model of obesity, and particularly juvenile obesity, is an important step to elucidating the factors associated with obesity and evaluating intervention strategies. Design and Methods : Infant marmosets were followed from birth to 12 months of age. Feeding phenotypes were determined through the use of behavioral observation, solid food intake trials, and liquid feeding trials monitored via lickometer. Results : Marmosets found to be obese at 12 months of age (more than 14%body fat) start consuming solid food sooner and initiate more time off of care givers. These individuals developed stable feeding phenotypes that included being more efficient consumers during liquid intake trials, drinking more grams of diet per contact with the licksit. Conclusions : The weaning process appears to be particularly important in the development of feeding phenotypes and the development of juvenile obesity for the marmosets, and thus this is the time that should be focused upon for intervention testing in both nonhuman primates and children.     

Spatial Distribution and Exploitation of Trees Gouged by Common Marmosets (Callithrix jacchus)

Resource distribution shapes many aspects of primate behavioral ecology. Though the spatial patterning of fruits, leaves, and insects has been explored among primate foods, comparatively less is known about exudate distributions. Tree exudates are a renewable resource, provide long-term evidence of exploitation, and may be selectively exploited to manipulate spatial distribution. We assessed the spatial patterning of trees gouged by common marmosets (Callithrix jacchus) to determine if they exhibit a uniform, random, or clumped distribution. We also asked whether marmosets selectively gouge trees in home range centers, which may afford them exclusive access to exudates. We explored whether spatial or physical characteristics of trees predict how intensely gouged trees were exploited. The mean nearest neighbor distance of gouged trees was significantly closer than expected for a random distribution and Ripley’s K-function showed that gouged trees were clumped across all spatial scales in our study area. Clumping may enable marmosets to reduce day and home ranges and facilitate repeated gouging of trees. Gouged trees were not closer to marmosets’ home range centers than peripheries, nor were centrally located trees more intensely gouged. Increased gouging intensity was associated with larger tree circumferences, although this effect was primarily driven by interspecific differences in circumference. Although marmosets may benefit from exploiting clumped exudates, they do not concentrate gouging in areas where they are more likely to gain exclusive access. Species-specific tree characteristics such as exudate quality and/or bark properties may play a larger role in determining gouging patterns than intergroup feeding competition.     

The GLP-1 agonist exendin-4 reduces food intake in nonhuman primates through changes in meal size

Exendin-4 (Ex4), a long-acting glucagon-like peptide-1 (GLP-1) receptor agonist, has been shown to reduce food intake and suppress gastric emptying in rodents and humans. In this study we investigated the effects of peripheral administration of Ex4 on food intake and meal patterns in adult male rhesus macaques. Rhesus macaques (n = 4) that had been trained to lever press for food pellets were injected intramuscularly 15 min before the start of their 6-h daily feeding period. Ex4 was given at doses of 0.10, 0.32, 0.56, 1.0, and 3.0 microg/kg. Ex4 suppressed food intake in a dose-dependent manner, with the 3.0 microg/kg dose completely preventing feeding during the 6-h period and the 0.10 microg/kg dose suppressing intake by 17%. Doses of 0.32, 0.56, 1.0, and 3.0 microg/kg caused significant reductions in cumulative intake at all six hourly time points. Ex4 inhibited food intake through a specific effect on meal size. Meal size was significantly reduced in a dose-dependent manner with significant reductions at the 0.32 and 1.0 microg/kg doses (P < 0.05). Day 2 and 3 intakes returned to baseline levels with no compensation for Ex4-induced feeding suppression. Administration of doses of 0.32 and 0.56 microg/kg Ex4 over 5 consecutive days led to sustained reductions in intake with no evidence of compensation. Again, these reductions were due to specific effects on meal size. These results demonstrate that activation of GLP-1 pathways has potent effects on the controls of meal size and overall food intake in a nonhuman primate model.     

What smells? Developing in‐field methods to characterize the chemical composition of wild mammalian scent cues

Olfactory cues play an important role in mammalian biology, but have been challenging to assess in the field. Current methods pose problematic issues with sample storage and transportation, limiting our ability to connect chemical variation in scents with relevant ecological and behavioral contexts. Real‐time, in‐field analysis via portable gas chromatography–mass spectrometry (GC‐MS) has the potential to overcome these issues, but with trade‐offs of reduced sensitivity and compound mass range. We field‐tested the ability of portable GC‐MS to support two representative applications of chemical ecology research with a wild arboreal primate, common marmoset monkeys (Callithrix jacchus). We developed methods to (a) evaluate the chemical composition of marmoset scent marks deposited at feeding sites and (b) characterize the scent profiles of exudates eaten by marmosets. We successfully collected marmoset scent marks across several canopy heights, with the portable GC‐MS detecting known components of marmoset glandular secretions and differentiating these from in‐field controls. Likewise, variation in the chemical profile of scent marks demonstrated a significant correlation with marmoset feeding behavior, indicating these scents’ biological relevance. The portable GC‐MS also delineated species‐specific olfactory signatures of exudates fed on by marmosets. Despite the trade‐offs, portable GC‐MS represents a viable option for characterizing olfactory compounds used by wild mammals, yielding biologically relevant data. While the decision to adopt portable GC‐MS will likely depend on site‐ and project‐specific needs, our ability to conduct two example applications under relatively challenging field conditions bodes well for the versatility of in‐field GC‐MS.     

Peptide YY(3-36) inhibits gastric emptying and produces acute reductions in food intake in rhesus monkeys

Peptide YY3-36 [PYY(3-36)], a gastrointestinal peptide that is released into the circulation in response to ingesting a meal, has recently been suggested to play a role in controlling food intake. PYY(3-36) has been reported to inhibit food intake following peripheral administration in rodents and in human subjects. To more fully characterize the potential feeding actions of PYY(3-36), we examined the ability of a dose range of PYY(3-36) (0.3-3.0 nmol/kg) to affect liquid gastric emptying and daily 6-h food intake in male rhesus monkeys. Intramuscular PYY(3-36) produced a dose-related inhibition of saline gastric emptying that was maximal at a dose of 3 nmol/kg. Intramuscular PYY(3-36) administered before daily 6-h food access produced significant feeding reductions at doses of 1 and 3 nmol/kg. Analyses of the patterns of food intake across the 6-h period of food access revealed that PYY(3-36) increased the latency to the first meal and reduced average meal size without altering meal number. Although single doses of PYY(3-36) reduced intake, a suppressive effect on food intake was not sustained over multiple administrations across successive days. Together, these data suggest that PYY(3-36) has the ability to reduce food intake in acute test situations in nonhuman primates. Whether this is a physiological action of the endogenous peptide remains to be determined.     

Cage use and feeding height preferences of captive common marmosets (Callithrix j. jacchus) in two-tier cages

Determining appropriate feeding regimes has important welfare implications for captive primates. This study examined the preference of food bowl heights in 6 pairs of common marmosets (Callithrix jacchus) housed in a 2-tier cage system. Given that marmosets are arboreal and spend most of their time in the upper half of their cages, we predicted that the marmosets would prefer a food bowl positioned at the top of the cage over one positioned at the bottom. We further predicted that this would be more apparent for the marmosets housed in lower tier than upper tier cages. Given a choice regarding where to feed, marmosets did prefer the top bowl to the bottom bowl; however, when only 1 food bowl was presented, its position had no significant effect on the marmosets' feeding behavior. In addition, contrary to the prediction, there were few differences in the marmosets' feeding behavior in the upper and lower tier cages. Feeding the marmosets in a bowl at the bottom of their cage did not result in greater cage use. On the basis of this study, we recommend positioning captive marmosets' food bowls high in the cage.     

Feeding rate as valuable information in primate feeding ecology

In this review I outline studies on wild non-human primates using information on feeding rate, which is defined as the food intake per minute on a dry-weight basis; further, I summarize the significance of feeding rate in primate feeding ecology. The optimal foraging theory has addressed three aspects of animal feeding: (1) optimal food patch choice, (2) optimal time allocation to different patches, and (3) optimal food choice. In order to gain a better understanding of these three aspects, the feeding rate itself or its relevance indices (e.g., rates of calorie and protein intake) could be appropriate measures to assess the quality of food and food patches. Moreover, the feeding rate plays an essential role in estimation of total food intake, because it varies greatly for different food items and the feeding time is not a precise measure. The feeding rate could also vary across individuals who simultaneously feed on the same food items in the same food patch. Body size-dependent and rank-dependent differences in the feeding rate sometimes cause individuals to take strategic behavioral options. In the closing remarks, I discuss the usefulness of even limited data on feeding rate obtained under adverse observational conditions in understanding primate feeding ecology.     

Cage Use and Feeding Height Preferences of Captive Common Marmosets (Callithrix j. jacchus) in Two-Tier Cages

Determining appropriate feeding regimes has important welfare implications for captive primates. This study examined the preference of food bowl heights in 6 pairs of common marmosets (Callithrix jacchus) housed in a 2-tier cage system. Given that marmosets are arboreal and spend most of their time in the upper half of their cages, we predicted that the marmosets would prefer a food bowl positioned at the top of the cage over one positioned at the bottom. We further predicted that this would be more apparent for the marmosets housed in lower tier than upper tier cages. Given a choice regarding where to feed, marmosets did prefer the top bowl to the bottom bowl; however, when only 1 food bowl was presented, its position had no significant effect on the marmosets' feeding behavior. In addition, contrary to the prediction, there were few differences in the marmosets' feeding behavior in the upper and lower tier cages. Feeding the marmosets in a bowl at the bottom of their cage did not result in greater cage use. On the basis of this study, we recommend positioning captive marmosets' food bowls high in the cage.     

Human speech reduces pygmy marmoset (Cebuella pygmaea) feeding and resting at a Peruvian tourist site,with louder volumes decreasing visibility

Although potentially beneficial in terms of raising awareness and conservation funding, tourist visitation of wild primates can have negative impacts on visited groups. Tourism‐generated noise is a relatively understudied facet of ecotourism research, and the effects of tourist‐generated speech on free‐ranging, wild primates has never been explored previously. This study investigates the behavioral responses of 10 groups of pygmy marmosets (Cebuella pygmaea) to human speech. Through the use of an experimental playback study using recorded human speech, we show that pygmy marmosets within the Tamshiyacu‐Tahuayo Reserve, Peru, are significantly less visible, and often move completely out of sight after louder playbacks. Although no consistent differences were found in other behaviors with playback duration and volume, playbacks of human speech tended to increase the amount of time individuals were alert and decrease feeding and resting behaviors. Our results demonstrate that human speech can alter the behavior of visited primates, and identifies a decrease in primate visibility within the increasing volume. As all trials in this study took place near a marmoset group's feeding tree, moving out of sight from the visible study area is a particularly energetically costly behavior, and also has a negative effect on visitor enjoyment as it limits the time that they are able to view the target species. This response was not observed (nor was any other consistent behavior change) in control trials where the marmosets were exposed to human presence but not to speech, suggesting that negative tourist impacts can be reduced by encouraging tourists to refrain from speaking in the presence of visited primate groups.     

Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia

Local variations in fruit- and leaf-eating have been reported for some primate species; however, similar variations in exudate-feeding of pygmy marmosets, one of the most specialized neotropical primate species, have not been studied. In our 3-year study of four populations of pygmy marmosets in northeastern Ecuador, we characterized their exudate-feeding behavior by describing the use of exudate sources. We tested whether the use of exudate species was related to ecological factors such as the availability of exudate species in an area. We estimated the daily activity budgets of the groups with 1-hr scan samples and found significant interpopulation differences in the time spent on exudate feeding. We recorded a total of 18 exudate species used in the four populations; however, the populations differed in the total number of species used and in the preferred species. The most commonly used plant species were Sterculia apetala at San Pablo, Cedrela odorata at Sacha, Inga marginata at Amazoonico, and Parkia balslevii at Zancudo. We recorded the presence and abundance of the 18 exudate species in 90-m transects in the home range of each group and in one additional control area that contained no marmosets, for each population. Differences in the most-used exudate species among populations did not appear to be related to the availability of these species in each population, i.e., the marmosets did not use at random the exudate species available within their range, nor did they use more often the exudate species that were more abundant in their home ranges. One implication of our results for conservation is that protecting exudate resources based on data from only one area will not be sufficient to preserve pygmy marmosets in all populations.     

The temporal pattern of feeding over the oestrous cycle of the mouse.

The detailed temporal pattern of feeding in female mice was measured by an automated method over the oestrous cycle whilst feeding on either of two foods differing in stimulus characteristics, but of similar calorific value. The total time spent feeding varied systematically over the cycle, being increased for sweet food and decreased for laboratory chow at the time of sexual receptivity. and increased for both foods towards the end of the cycle. The temporal pattern is analysed into a number of variables, which are seen to alter in different ways over the oestrous cycle. The pro-oestrus disturbance is due to alterations in meal size brought about solely by changes in mean bout length, themselves products of variations in the initial bouts of the meal. Inter-meal interval is unrelated to changes in meal size at this time, allowing the latter to affect food intake. The changes towards the end of the cycle are produced by alterations of meal frequency at constant meal size. It is argued that separable 'phasic' and 'tonic' effects of reproductive condition on feeding may therefore be identified, and that they might possibly have different functions.     

An analysis of feeding patterns in the adult pig

Feeding behavior has been analyzed in Large-White and Chinese pig breeds. Maximally automatized apparatuses, especially adapted to animal size, were used. Besides the usual parameters measured such as food intake, meal size, meal duration, meal frequency, intermeal intervals and postprandial correlation, these apparatuses also permitted us to measure the rate of intake during the meal. This rate was constant throughout the meal in ad libitum conditions and after 24-hour deprivation. A positive correlation between meal size and length of the postmeal interval was found in only half of the animals. During this work, we began to study the mechanisms initiating food intake.     

Body mass growth in common marmosets: Toward a model of pediatric obesity

While much is known about adult obesity in nonhuman primates, very little is known regarding development of childhood adiposity. As small monkeys that are easy to handle and have a relatively fast life history, common marmoset monkeys (Callithrix jacchus) offer interesting opportunities to examine the question of fat versus lean mass growth in a nonhuman primate. This article provides an overview of our understanding of early life growth in mass in marmoset monkeys, based primarily upon our past 20 years of research, culminating in our recent findings on early life obesity in this species. Common marmosets display variance in early life growth patterns that is related to both pre‐ and postnatal factors and the marmoset uterine environment is exquisitely designed to reflect resources available for the gestation of multiple offspring, making them an interesting model of developmental programming. We have demonstrated that obesity can be generated in very early life in captive marmosets, with excess adiposity evident by one month of age, making this species a potentially valuable model in which to study pediatric obesity and its sequelae. Birth weight is associated with adiposity in animals vulnerable to obesity. Early life exposure to higher fat diets enhances the chances of postweaning obesity development. However, overall higher food consumption is also associated with obesity development at later ages. One unexpected finding in our studies has been the relatively high body fat percentage of neonatal (12–18%) marmosets suggesting that hypotheses regarding the uniqueness of high human neonatal adiposity merit further examination. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Expression of taste signal transduction molecules in the caecum of common marmosets

The extraoral presence of taste signal transduction proteins has recently been reported in rodents and humans. Here, we report for the first time the presence of these signal transduction proteins in the caecum of a non-human primate, the common marmoset. Quantitative RT-PCR data on the gene expression of taste signal transduction molecules (gustducin and TRPM5) in common marmosets suggested high expression in the caecum, which was not observed in other non-human primates. Immunohistochemical analysis confirmed the specific presence of gustducin and taste receptors in marmoset caecal cells. These results may relate to the specific feeding behaviour of marmosets, which consume plant exudates, primarily gums.     

Primate socioecology at the crossroads: Past, present, and future

Attempts to explain differences in the size and structure of primate groups have argued that they are a consequence of variation in the intensity of feeding competition caused by contrasts in food distribution. However, although feeding competition can limit the size of female groups, many other factors affect the costs and the benefits of sociality to females and contribute to differences in group size. Moreover, interspecific differences in social relationships between females, in female philopatry, and in kinship between group members appear to be more closely associated with variation in life‐history parameters, reproductive strategies, and phylogeny than with contrasts in food distribution or feeding competition. The mismatch between predictions of socioecological theory and observed variation in primate social behavior has led to protracted arguments about the future of primate socioecology. We argue that future attempts to understand the diversity of primate societies need to be based on an approach that explores separate explanations for different components of social organization, combines ecological and phylogenetic information, and integrates research on primates with similar studies of other groups of mammals. © 2012 Wiley Periodicals, Inc.     

Homeostatic regulation of protein intake: in search of a mechanism

Free-living organisms must procure adequate nutrition by negotiating an environment in which both the quality and quantity of food vary markedly. Recent decades have seen marked progress in our understanding of neural regulation of feeding behavior. However, this progress has occurred largely in the context of energy intake, despite the fact that food intake is influenced by more than just the energy content of the diet. A large number of behavioral studies indicate that both the quantity and quality of dietary protein can markedly influence food intake. High-protein diets tend to reduce intake, low-protein diets tend to increase intake, and rodent models seem to self-select between diets in order to meet protein requirements and avoid diets that are imbalanced in amino acids. Recent work suggests that the amino acid leucine regulates food intake by altering mTOR and AMPK signaling in the hypothalamus, while activation of GCN2 within the anterior piriform cortex contributes to the detection and avoidance of amino acid-imbalanced diets. This review focuses on the role that these and other signaling systems may play in mediating the homeostatic regulation of protein balance, and in doing so, highlights our lack of knowledge regarding the physiological and neurobiological mechanisms that might underpin such a regulatory phenomenon.     

A novel feeding behavior index integrating several components of the feeding behavior of finishing pigs

Describing the feeding behavior of pigs is difficult given the large day-to-day variations observed for a given animal. The objectives of this study were to create an index that integrates the information from several components of feeding behavior in order to account for intra-animal variation within a day and between days, and to evaluate the capability of this index to study the impact of relevant nutritional factors affecting feeding behavior. Feed intake information from 160 pigs during the last 28 d of the growing phase from three studies was used. For each pig, the sum of the absolute values of the deviation areas between the regression line of the relative cumulative feed intake and the observed cumulative feed intake was used to calculate the weekly index measuring the irregularity of feed intake (IIFI). Spearman’s correlations of IIFI with the number of daily meals (r = −0.42; P < 0.001), meal duration (r = 0.38; P < 0.01), and feed intake per meal (r = 0.41; P < 0.01) indicate that pigs with high IIFI have fewer meals of longer duration and higher feed intake compared to pigs with low IIFI. This shows that IIFI captures information from several components of feeding behavior. Analysis of variance showed no effect of treatment on feeding behavior for datasets 1 and 2. However, the correlation between IIFI and dietary levels of CP (r = 0.34) indicates that diets high in CP were associated with pigs having more irregular meals. In dataset 3, pig feeding behavior was more regular in control diets than in pigs fed fibrous diets (IIFI; 164 vs. 197, respectively; P < 0.05). Additionally, IIFI was smaller in pigs fed canola by-product diets than in pigs fed wheat by-product diets, indicating that the source of fiber may also influence the feeding behavior of pigs. In most cases, IIFI was more effective at identifying differences in feeding behavior between dietary treatments than conventional feeding behavior variables. These results show the ability of IIFI to integrate information from several conventional components of the feeding behavior of pigs and its potential to successfully evaluate the effect of nutritional factors on feeding behavior.     

Meal Pattern Analysis of Macronutrient Intake Aafter PVN Norepinephrine and Peripheral Clonidine Administration

Norepinephrine (NE) injected into the paraventricular nucleus (PVN) of the hypothalamus of rats is a potent stimulant of food intake, more specifically ingestion of the carbohydrate nutrient. In 2 experiments of the present study, this effect was found to be dose-dependent, and the effectiveness of NE in potentiating total food consumption was greatly reduced when the carbohydrate diet was removed. In addition, experiments using a computer-automated data acquisition apparatus were performed to characterize, in detail, the impact of PVN injection of NE and peripheral administration of the α2-nor-adrenergic agonist clonidine (CLON) on the macrostructure of feeding behavior in animals given 3 pure macronutrient diets. These 2 compounds, injected at the onset of the nocturnal feeding cycle, had very similar effects on meal patterns, with both affecting nutrient intake by increasing meal size and duration rather than by increasing meal frequency. They both affected primarily the first meal of the dark cycle, selectively enhancing carbohydrate ingestion by increasing Kcal intake, percent composition in the total diet and feeding time, and also by decreasing the satiating impact of this macronutrient. These stimulatory effects of NE and CLON on carbohydrate ingestion during the first meal were followed by complete recovery over the next 1 to 2 hours after injection. In addition to these predominant effects on carbohydrate intake, PVN NE at the highest doses tested (10 and 20 nmoles) produced a small increase in fat intake, whereas peripheral CLON actually decreased intake of fat and protein over the 12-hour cycle. The similarities in the impact of NE and CLON on carbohydrate feeding patterns support the hypothesis that both agonists may be acting via the same PVN α2-noradrenergic system controlling ingestion of the carbohydrate-rich meals which predominate at dark onset.     

Nicotine's attenuation of body weight involves the perifornical hypothalamus

Previously we showed that intermittent administration of nicotine (NIC) in the dark phase decreased food intake and body weight and this could be blocked when the NIC receptor antagonist mecamylamine was infused into the fourth ventricle. Catecholaminergic neurons adjacent to the fourth ventricle contain NIC receptors and directly innervate the perifornical hypothalamus (PFH) which has been shown to be involved in regulation of feeding. This study explored whether NIC regulates feeding behavior by modulating catecholaminergic input to the PFH. Epinephrine and norepinephrine neuronal input was ablated within the PFH by infusion of 6-hydroxydopamine hydrobromide (6-OHDA), while bupropion was infused to protect dopaminergic neurons. After recovery of body weights to pre-surgery levels, food intake, meal size, meal number and body weight were measured after intermittent NIC injections. The results showed the PFH lesioned animals did not exhibit the typical prolonged drop in food intake, meal size and body weight normally associated with NIC administration. High performance liquid chromatography analyses demonstrated that compared to control rats, 6-OHDA administration significantly reduced PFH norepinephrine and epinephrine levels, but not dopamine levels. These results are consistent with NIC reducing food intake in part by acting through catecholaminergic neurons within or extending through the PFH.