The effect of dominance on food hoarding: a game theoretical model

Many food hoarding animals live in small groups structured by rank. The presence of conspecifics in the hoarding area increases the risk of losing stored supplies. The possibility of stealing from others depends on a forager's rank in the group. Highly ranked individuals can steal from subordinates and also protect their own caches. Since storing incurs both costs and benefits, the optimal hoarding investment will differ between individuals of different rank. In a game theoretical model, we investigate how dominant and subordinate individuals should optimize their hoarding effort. Our model imagines animals that are large-scale hoarders in autumn and dependent on stored supplies for winter survival. Many examples can be found in the bird families Paridae and Corvidae, but the model can be used for any hoarding species that forage in groups. Predictions from the model are as follows: First, subordinates should store more than dominants, but in a predictable environment, this difference will decrease as the environment gets harsher. Under harsh conditions, dominants should store almost as much as subordinates and, later, spend almost as much time retrieving their own caches as subordinates. Second, if on the other hand, bad winter conditions were not expected when storing, dominants should spend more time pilfering caches from subordinates. Third, in populations that are highly dependent on stored supplies, dominants should store relatively more than in populations that are less dependent on stored supplies. Fourth, harsher environments will favor hoarding. And finally, if dominant individuals store, it implies that hoarders have a selfish recovery advantage over conspecific pilferers.     

Social influences on food caching in willow tits: a field experiment

We studied the food hoarding behavior of willow tits (Parusmontanus), a scatter-hoarding passerine wintering in dominance-structuredflocks. We examined social influences on microhabitat selectionand spatial cache distribution at temporary feeders. Dominantadult males stored food closer to die feeder and at a greaterrate than did subordinates. When alone, the birds stored foodcloser to the feeder than when accompanied by conspecifics.Conifers were preferred over deciduous trees as cache trees.The subordinates cached more in die outer parts of branchesthan dominants. There were no significant differences in dierelative or absolute heights of die caches, nor in the verticalor horizontal hoarding niche breadths between dominants andsubordinates. We experimentally removed die dominants from dieflock for 90 min and recorded the behavior of die remainingsubordinates immediately after die removal. The removal resultedin a decrease in die hoarding distance of die remaining birds,indicating that die presence of dominants directly affecteddie behavior of subordinates and suggesting that kleptopar-asitismby dominants may be prevented by rarhing farther away. Withdie dominants removed, die subordinates cached at a greaterrate than before die removal. The decrease in die hoarding distanceand increase in die hoarding rate were die only significanteffects of die experiment, perhaps suggesting that, during ashort absence of dominants, die subordinates do not benefitfrom changing dieir caching microhabitat They might be excludedfrom those new, possibly safer, microhabitats after die dominantbird rejoins die flock.     

The effect of social dominance on fattening and food-caching behaviour in Carolina chickadees, Poecile carolinensis

Subordinates often have to wait for dominants to obtain food. As a result, their foraging success should be less predictable and they should therefore maintain a higher level of energy reserves compared with dominants. A corollary of this prediction is that subordinates should gain mass earlier in the day and maintain higher mass than dominants. We tested these predictions with captive Carolina chickadees. In two different experiments (one where birds were given ad libitum access to food and the other with food access limited to 60 min/day), we formed social flocks of two previously unfamiliar birds and compared their energy management (body fat and food caches) while they were in the flock with energy management when housed alone. Results from both experiments failed to support the predictions. Of all the parameters of body mass and food caching we measured only the following results were significant: (1) On the ad libitum food schedule, both subordinates and dominants accumulated more mass over the day when in a flock compared with when they were solitary, and there were no differences in mass gain between dominants and subordinates. (2) When analysed separately, dominants showed a higher evening mass in the flock compared with the solitary condition, a trend that runs opposite to the prediction. Our results suggest that when in favourable foraging conditions, social interactions might cause dominant and subordinate birds to accumulate more energy reserves as a result of competition. On the other hand, if food supply is limited, both dominants and subordinates may be forced to maintain similar fat reserves as an insurance against increased risk of starvation. Copyright 2000 The Association for the Study of Animal Behaviour.     

Dominance, competition, and energetic reserves in the European starling, Sturnus vulgaris

We investigated the relationships between social dominance,competition for food, and strategies of body mass and fat regulationin the European starling (Sturnus vulgaris). In birds housedin groups of three, subdominant birds stored more fat than dominants.A removal experiment established a causal link between socialdominance and fat reserves; in groups that had the dominantindividual removed, the remaining birds reduced body mass andfat, relative to control groups that had the subordinate removed.In a second experiment, we investigated the influences of degreeof competition for food and dominance on body mass and fat reserves.Birds under high competition increased fat reserves and tendedto have higher body mass than birds under low competition. Theincrease in fat reserves was higher in the subdominants thanin the dominants. These results are consistent with hypothesesconcerning dominance-dependent access to food; subdominant birds,or birds under increased competition, may store more fat asan insurance against periods when food cannot be obtained. However,relations between dominance, body mass, and fat reserves mayalso arise through other proximate factors relating to dominance-dependentcosts and benefits of fat storage, such as predation risk andenergetic expenditure.     

Using priority to food access: fattening strategies in dominance-structured willow tit (Parus montanus) flocks

We studied changes in body mass in response to priority to foodaccess by repeatedly weighing free-living willow tits in dominance-structuredflocks. Priority to food access did not correlate to eitheracquisition rate or net turnover of body reserves, but subordinateswith low food availability had larger body reserves than dominants.Removal experiments suggest a causal relationship between rankand the size of reserves. Body reserves of subordinates decreasedwhen their access to food increased after the dominant was removed.Low variability in body mass of subordinates shows that theydo not maintain large reserves in response to uncertain acquisitionof food. Rather, large reserves of low-rank individuals couldserve as insurance for conditions with increasing requirements.Under such conditions, dominants are more likely to claim theirpriority to food, and subordinates would not be able to increasetheir body reserves by feeding.     

Why do hoarding birds gain fat in winter in the wrong way? Suggestions from a dynamic model

In winter, small birds should be fat to avoid starvation andlean and agile to escape predators. This means that they facea trade-off between the costs and benefits of carrying fat reserves.Every day they must gain enough fat to survive the coming night.Food-hoarding species can afford to carry less fat than nonhoardersbecause they can store energy outside the body. Furthermore, hoardersshould avoid carrying excessive fat during the day because theycan gain fat fast by retrieving food late in the afternoon.With no stored supplies, nonhoarders face more unpredictableaccess to food, and they should start gaining fat earlier inthe day. The predicted pattern is then that nonhoarders gainfat early and that hoarders gain fat late in the day. Recent fielddata show the opposite pattern: hoarders gain relatively morefat reserves in the morning than nonhoarders do. Using a dynamicmodel that mimics the conditions in a boreal winter forest,I investigated under which conditions this pattern will arise.The only assumption of those investigated that produced thispattern was to relax the effect of mass-dependent predation risk.I did this by introducing a limit under which fat reserves didnot affect predation risk. Hoarders then started the day bygaining fat in the morning. Later, when they had reached a safer(but still not risky) level, they switched to hoarding. Thepattern I searched would only occur if either not all food waspossible to store, or if retrieval gave less energy than foragingin good weather conditions. If I assumed that low levels ofbody fat also increased predation risk, hoarders would cachein the morning when they carried least fat. I discuss empiricalevidence for how body fat affects predation risk. In summary,the factors that produced the pattern I searched were a changein the predation-mortality function combined with restrictions onhoarding.     

Daily body mass regulation in dominance-structured coal tit (Parus ater) flocks in response to variable food access: a laboratory study

In a dominance-structured flock, social status may determinepriority of access to food. Birds of low social status mayperceive present and future access to food as less predictable,and so have a higher risk of starvation, than birds of highsocial rank. Theoretical models predict that subordinate birdsshould carry larger fat reserves and incur higher mass-dependentcosts than dominants. However, empirical tests of the assumptionsof these models are still scarce and controversial. We investigatedthe effect of dominance rank on daily mass gain under conditionsof fluctuating food availability in a laboratory experimentusing four flocks of four coal tits (Parus ater) each. Thesame amount of food was delivered in two treatments, but inone treatment the food was offered at a constant rate betweendays (fixed treatment), while in the other treatment the dailyfood supply varied in an unpredictable sequence between days(variable treatment). All birds showed greater variance inbody mass in the variable treatment than in the fixed treatment.Body mass within birds showed the same variability at dawn thanat dusk in the fixed treatment, but less variability at dawnthan at dusk in the variable treatment. This may be a mechanismto reduce the immediate risk of starvation at the beginningof the day, when fat reserves are at their lowest and the aggressionbetween flock members when feeding highest. Subordinate birdswere excluded from the feeders by dominants more often in theearly morning than in the rest of the day, and they showedmore variability in daily mass gain and body mass at dawn thandominant birds. These results support the hypothesis that subordinatebirds have a reduced probability of surviving when food availabilitychanges unexpectedly compared to dominants.     

The relationship between dominance, corticosterone, memory, and food caching in mountain chickadees (Poecile gambeli)

It has been hypothesized that in avian social groups subordinate individuals should maintain more energy reserves than dominants, as an insurance against increased perceived risk of starvation. Subordinates might also have elevated baseline corticosterone levels because corticosterone is known to facilitate fattening in birds. Recent experiments showed that moderately elevated corticosterone levels resulting from unpredictable food supply are correlated with enhanced cache retrieval efficiency and more accurate performance on a spatial memory task. Given the correlation between corticosterone and memory, a further prediction is that subordinates might be more efficient at cache retrieval and show more accurate performance on spatial memory tasks. We tested these predictions in dominant-subordinate pairs of mountain chickadees (Poecile gambeli). Each pair was housed in the same cage but caching behavior was tested individually in an adjacent aviary to avoid the confounding effects of small spaces in which birds could unnaturally and directly influence each other's behavior. In sharp contrast to our hypothesis, we found that subordinate chickadees cached less food, showed less efficient cache retrieval, and performed significantly worse on the spatial memory task than dominants. Although the behavioral differences could have resulted from social stress of subordination, and dominant birds reached significantly higher levels of corticosterone during their response to acute stress compared to subordinates, there were no significant differences between dominants and subordinates in baseline levels or in the pattern of adrenocortical stress response. We find no evidence, therefore, to support the hypothesis that subordinate mountain chickadees maintain elevated baseline corticosterone levels whereas lower caching rates and inferior cache retrieval efficiency might contribute to reduced survival of subordinates commonly found in food-caching parids.     

Do chimpanzees know what conspecifics know?

We conducted three experiments on social problem solving by chimpanzees, Pan troglodytes. In each experiment a subordinate and a dominant individual competed for food, which was placed in various ways on the subordinate's side of two opaque barriers. In some conditions dominants had not seen the food hidden, or food they had seen hidden was moved elsewhere when they were not watching (whereas in control conditions they saw the food being hidden or moved). At the same time, subordinates always saw the entire baiting procedure and could monitor the visual access of their dominant competitor as well. If subordinates were sensitive to what dominants did or did not see during baiting, they should have preferentially approached and retrieved the food that dominants had not seen hidden or moved. This is what they did in experiment 1 when dominants were either uninformed or misinformed about the food's location. In experiment 2 subordinates recognized, and adjusted their behaviour accordingly, when the dominant individual who witnessed the hiding was replaced with another dominant individual who had not witnessed it, thus demonstrating their ability to keep track of precisely who has witnessed what. In experiment 3 subordinates did not choose consistently between two pieces of hidden food, one of which dominants had seen hidden and one of which they had not seen hidden. However, their failure in this experiment was likely to be due to the changed nature of the competition under these circumstances and not to a failure of social-cognitive skills. These findings suggest that at least in some situations (i.e. competition with conspecifics) chimpanzees know what conspecifics have and have not seen (do and do not know), and that they use this information to devise effective social-cognitive strategies. Copyright 2001 The Association for the Study of Animal Behaviour.     

Effect of the Presence of Subordinates on Dominant Female Behaviour and Fitness in Hierarchies of the Dwarf Angelfish Centropyge bicolor

In many hierarchical animal societies, dominant individuals control group membership owing to their power to evict subordinates. In such groups, the presence of subordinates, and therefore group stability, is continually dependent on subordinates being tolerated by dominants. The dominant decision to tolerate or evict is, in turn, dependent on the costs and benefits to dominants of subordinate presence. We investigated the effect of subordinate presence on dominants in the female dominance hierarchy of the dwarf angelfish Centropyge bicolor, using both observations of natural groups and experimental removals of subordinates. We found that the presence of subordinates had no effect on dominant access to resources, as measured by dominant foraging rates and home range areas, nor on dominant fitness, as measured by growth rates and spawning frequencies. Our results suggest that the presence of subordinates has a neutral effect on the current fitness of dominants, so that dominants have no great incentive to evict subordinates. We discuss the possibility that tolerance of subordinates might be further explained by considering future fitness, as dominant females in these haremic protogynous angelfish stand to inherit the male position, whereupon subordinate females change from potential competition to useful mates.     

Growth depensation and aggression in laboratory reared coho salmon: the effect of food distribution and ration size

Groups of recently emerged coho salmon fry Oncorhynchus kisutch were reared for 3 months on food that appeared either asynchronously at a single location (localized) or synchronously and spatially dispersed (dispersed). Groups were further subdivided into those receiving low (1%) or high (3% body weight per day) rations, with five replicate groups for each treatment combination. At low ration there was greater growth depensation, i.e. growth variation, in groups receiving localized as compared to dispersed food. At high ration there was no difference. There was no effect of food distribution upon mean fish weight, but groups receiving high rations had greater mean fish weights than groups receiving low rations. There was no overall difference in the frequency of chasing between any of the treatment combinations. However, in localized food groups, dominants defended positions close to where food entered the tank, giving them greater access than subordinates. In dispersed food groups, while dominants also defended particular areas, this did not result in greater access to food. These results demonstrate that although feeding methodology may not directly influence the frequency of aggressive interactions, feeding methods which facilitate food monopolization by dominants can accelerate the growth of these individuals at the expense of subordinates. In aquacultural applications where greater size is desirable, or otherwise selected for, this may result in the unintentional selection for increased aggressiveness.     

Pheromone, juvenile hormone, and social status in the male lobster cockroach Nauphoeta cinerea

In this study, the major pheromone component, 3‐hydroxy‐2‐butanone (3H‐2B), released by dominants was measured during early scotophase. Both the JH III titer in the hemolymph and the 3H‐2B content of the sternal glands of the dominants and subordinates were then measured during late scotophase and late photophase. These investigations were performed on encounter days 1, 2, 3, 5, 7, 9, 12, and 20. The results showed that, for non‐aggressive posture (AP)‐adopting socially naïve males (SNMs), both the 3H‐2B release and the hemolymph JH III titer were maintained at a low level. Once a fight occurred, 3H‐2B release was raised significantly in the AP‐adopting dominants, but not in non‐AP‐adopting subordinates, and remained raised throughout the entire experimental period. At 30 min after the first encounter, the hemolymph JH III titer was significantly increased in dominants, but not in subordinates. A significantly higher hemolymph JH III titer was observed in dominants during late scotophase on days 3, 5, 12, and 20 and during late photophase on days 3, 5, and 20. After fighting, the sternal gland 3H‐2B content of the dominants or subordinates was significantly lower than in SNMs. In dominants, the sternal gland 3H‐2B content during late scotophase was significantly lower than that during late photophase in the first 9 domination days, while, in the subordinates, the 3H‐2B content during late scotophase was either similar to, or significantly higher than, that in late photophase. In the dominants, 3H‐2B release and JH III titer were positively correlated. In rank switchers, the switched social status was positively correlated with both 3H‐2B release and JH III titer. Comparison of 3H‐2B release and JH III titer in 1‐time, 3‐time, or 5‐time dominants showed that, although winning significantly increased both 3H‐2B release and JH III titer, there is no significant difference in 3H‐2B release between 3‐ and 5‐time winners, while the JH III titer was most significantly increased in the 3‐time winners. The possible relationship between pheromone release, JH III titer, and social status is discussed. Arch. Insect Biochem. Physiol. 2008. © 2008 Wiley‐Liss, Inc.     

Acquisition of dominance status affects maze learning in mice

Learning is likely to be costly and thus subject to trade-off with other components of life history. An obvious prediction, therefore, is that investment in learning, and thus learning performance, will vary with individual life history strategy and the reproductive value of the learning outcome. We tested this idea in the context of social dominance in male laboratory mice, using a simple radial maze paradigm to compare the ability of high- and low-ranking male mice to track changing food location. We tested animals in randomly selected pairs before and after establishing aggressive rank relationships to distinguish intrinsic differences in learning ability from those attributable to acquiring high or low rank. There was no difference in learning between later dominants and subordinates prior to establishing rank relationships. After pairing, however, dominants showed a significantly greater percentage of correct responses, with the difference being greatest earlier in a sequence of trials. The percentage of correct responses also increased with the amount of aggression initiated during pairing. The results thus appeared to reflect a state-dependent change in learning associated with the aggressive social relationships formed during pairing.     

Allostatic load, social status and stress hormones: the costs of social status matter

Cooperation and social support are the major advantages of living in social groups. However, there are also disadvantages arising from social conflict and competition. Social conflicts may increase allostatic load, which is reflected in increased concentrations of glucocorticoids. We applied the emerging concept of allostasis to investigate the relation between social status and glucocorticoid concentrations. Animals in a society experience different levels of allostatic load and these differences may predict relative glucocorticoid concentrations of dominant and subordinate individuals. We reviewed the available data from free-ranging animals and generated, for each sex separately, phylogenetic independent contrasts of allostatic load and relative glucocorticoid concentrations. Our results suggest that the relative allostatic load of social status predicts whether dominants or subordinates express higher or lower concentrations of glucocorticoids. There was a significant correlation between allostatic load of dominance and relative glucocorticoid concentrations in both females and males. When allostatic load was higher in dominants than in subordinates, dominants expressed higher levels of glucocorticoids; when allostatic load was similar in dominants and subordinates, there were only minor differences in glucocorticoid concentrations; and when allostatic load was lower in dominants than in subordinates, subordinates expressed higher levels of glucocorticoids than dominants. To our knowledge, this is the first model that consistently explains rank differences in glucocorticoid concentrations of different species and sexes. The heuristic concept of allostasis thus provides a testable framework for future studies of how social status is reflected in glucocorticoid concentrations.     

Winter survival and breeding success of dominant and subordinate Willow Tits Parus montanus

We studied the effect of winter rank on survival rate and reproductive success in Willow Tits Parus montanus, a resident passerine living in dominance-structured flocks during the nonbreeding season, in 6 years. Winter survival was dependent on both the birds' age and rank. Adults survived better than first-year birds, and within first-year males, dominants survived better than subordinates. In other sex and age classes, rank did not contribute to survival. Although first-year males were in excess among nonbreeders, no connection existed between breeding status and rank. Female rank did not explain the variation in the start of laying, clutch size, number of fledglings or recruit production. We conclude that social status in Willow Tits affects individual fitness mainly through rank-dependent survival. Acquiring a high rank position seems to be most important for first-year birds, especially first-year males.     

Helping effort and future fitness in cooperation animal societies

Little attention has been paid to a conspicuous and universal feature of animal societies: the variation between individuals in helping effort. Here, we develop a multiplayer kin-selection model that assumes that subordinates face a trade-off because current investment in help reduces their own future reproductive success. The model makes two predictions: (i) subordinates will work less hard the closer they are to inheriting breeding status; and (ii) for a given dominance rank, subordinates will work less hard in larger groups. The second prediction reflects the larger pay-off from inheriting a larger group. Both predictions were tested through a field experiment on the paper wasp Polistes dominulus. First, we measured an index of helping effort among subordinates, then we removed successive dominants to reveal the inheritance ranks of the subordinates: their positions in the queue to inherit dominance. We found that both inheritance rank and group size had significant effects on helping effort, in the manner predicted by our model. The close match between our theoretical and empirical results suggests that individuals adjust their helping effort according to their expected future reproductive success. This relationship has probably remained hidden in previous studies that have focused on variation in genetic relatedness.     

Dominance and feeding competition in captive rhesus monkeys

The feeding behavior of 16 adult female rhesus monkeys living in three captive social groups was observed. Estimates of relative food intake, feeding rate, and location of feeding in relation to food sources were compared between females of different dominance ranks. Higher-ranking females had greater access to feeding sites and were supplanted or threatened less frequently while feeding than subordinates. However, no consistent differences in estimates of total intake were found between females of high and females of low rank. The effects of dominance on feeding behavior were most pronounced in the group receiving the least food relative to estimates of overall group nutritional requirements. Higher-ranking females, both over the long term and during the study period, tended to produce more surviving offspring. The effects of dominance on reproductive performance appeared to be less related to food intake than to competitive and aggressive interactions, potentially resulting in higher levels of stress for subordinates.     

Liver size reveals social status in the African cichlid Neolamprologus pulcher

Wild groups ( n = 167) of the cooperatively breeding Lake Tanganyika cichlid, Neolamprologus pulcher , were used to investigate how social status and sex influence liver investment. In contrast to expectations, males and females (controlling for body size) had similar liver investment and subordinates (both sexes) had relatively larger livers compared with dominants. Three hypotheses were considered for why social status results in liver size disparity: liver mass might reflect status-dependent differences in (1) energy expenditure, (2) energy storage and (3) energy acquisition. First, dominants performed more energetically costly behaviours ( e.g . social policing and care) compared with subordinates, supporting the notion that energy expenditure drives liver investment. Moreover, dominants in large groups (with many subordinates to monitor) and those holding multiple territories (with large areas to patrol), tended to have smaller livers. Second, subordinates did not appear to use the liver as a strategic energy storage organ. In laboratory and field experiments, subordinates ascending in rank had similar or larger livers during periods of rapid growth compared with non-ascending controls. Third, although subordinates fed more frequently than dominants, a negative relationship was found between feeding rates and liver size. Hence, these results contrast with previous liver studies and suggest that liver investment patterns were linked to status-driven differences in energy expenditure but not to energy intake or storage in N. pulcher .     

Size dominance affecting the social interactions and growth of juvenile Japanese flounder,Paralichthys olivaceus

Juvenile flounder Paralichthys olivaceus were size‐graded into three groups (small, large and mixing of small and large) and social interactions (feeding, aggressive attacking and activity) and growth of the fish were investigated. Growth of the subordinates (small flounder) was markedly suppressed by the presence of the dominants (large flounder). Dominants did not significantly suppress the overall food intake of the subordinates, but exhibited high aggressive attacking on the subordinates and consequently inhibited their activity. Size dominant interactions had little influence on the aggressive behaviour, feeding, activity and growth of the dominants. Results substantiated the hypothesis that the retardation in the growth of the subordinate flounder was attributed to the physiological costs of ‘stress’ by the aggression of the dominants. Individual differences in aggressive behaviour, feeding and activity were at least partly responsible for the growth depensation of the juvenile flounder. The dominants could not effectively defend the food in excess and disproportional food acquisition of the subordinates and dominants was not the primary mechanism responsible for the size hierarchy effect. In culture, size grading of the early juvenile flounder could markedly improve the growth and survival and thus possibly increase the overall biomass production of the flounder.     

Function and variability of male sex traits in a blenniid fish, Parablennius tentacularis

Juvenile flounder Paralichthys olivaceus were size‐graded into three groups (small, large and mixing of small and large) and social interactions (feeding, aggressive attacking and activity) and growth of the fish were investigated. Growth of the subordinates (small flounder) was markedly suppressed by the presence of the dominants (large flounder). Dominants did not significantly suppress the overall food intake of the subordinates, but exhibited high aggressive attacking on the subordinates and consequently inhibited their activity. Size dominant interactions had little influence on the aggressive behaviour, feeding, activity and growth of the dominants. Results substantiated the hypothesis that the retardation in the growth of the subordinate flounder was attributed to the physiological costs of 'stress' by the aggression of the dominants. Individual differences in aggressive behaviour, feeding and activity were at least partly responsible for the growth depensation of the juvenile flounder. The dominants could not effectively defend the food in excess and disproportional food acquisition of the subordinates and dominants was not the primary mechanism responsible for the size hierarchy effect. In culture, size grading of the early juvenile flounder could markedly improve the growth and survival and thus possibly increase the overall biomass production of the flounder.