Effect of Daily Body Mass Variation on the Foraging Behaviour of Tit Species (Parus spp.)

We studied the effect of daily body mass increase on the foraging preferences of two tit species, crested tit, Parus cristatus and blue tit, P. caeruleus, contrasting in morphology and behaviour. We found that both species show a diurnal increase in body mass during winter. Using an experiment with feeders we show that in the crested tit, the proportion of time spent foraging while hanging decreased as body mass increased. In contrast, in the blue tit, foraging behaviour did not change with mass gain. We propose that the species with a morphological design providing a high ecological plasticity in terms of foraging postures can counteract the negative effect of body mass on the ecological options (foraging niche) more than species with a morphological design providing a low ecological plasticity in terms of foraging postures. Our results suggest that blue tits had the advantage of being able to choose to feed on different patches in the habitat throughout the day, which makes resources more predictable for them. In contrast, crested tits might be more restricted in their foraging options as their body mass increases, and this might explain why they hoard food.     

Avian daily foraging patterns: Effects of digestive constraints and variability

Summary Birds show a typical daily pattern of heavy morning and secondary afternoon feeding. We investigate the pattern of foraging by a bird that results in the lowest long-term rate of mortality. We assume the following: mortality is the sum of starvation and predation. The bird is characterized by two state variables, its energy reserves and the amount of food in its stomach. Starvation occurs during the day if the bird's reserves fall to zero. The bird starves during the night if the total energy stored in reserves and the stomach is less than a critical amount. The probability that the bird is killed by a predator is higher if the bird is foraging than if it is resting. Furthermore, the predation risk while foraging increases with the bird's mass. From these assumptions, we use dynamic programming techniques to find the daily foraging routine that minimizes mortality. The principal results are (1) Variability in food finding leads to routines with feeding concentrated early in the day, (2) digestive constraints cause feeding to be spread more evenly through the day, (3) even under fairly severe digestive constraints, the stomach is generally not full and (4) optimal fat reserve levels are higher in more variable environments and under digestive constraints. This model suggests that the characteristic daily feeding pattern of small birds is not due to digestive constraints but is greatly influenced by environmental variability.     

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.     

啮齿动物的分散贮食行为

食物贮藏是许多动物重要的适应性行为,分散贮藏的食物以植物种子为主。每个贮藏点贮藏数量不等的食物项目。啮齿动物分散贮藏食物之后,可降低食物被其他个体获取的机率,提高对食物资源的控制能力,最终有利于自身的生存和繁殖成功。植物种子被贮藏之后,可减少非贮食鼠类对种子的取食。同时,合适的微生境和埋藏有利于种子萌发、幼苗建成和植物的更新;使植物的分布区得以扩展。探讨啮齿动物的分散贮食行为,能够更好地理解食物贮藏在啮齿动物生活史中的作用,进一步认识鼠类和植物的相互关系以及不同啮齿动物在群落形成中的潜在作用。本综述了啮齿动物分散贮食的研究进展,并提出今后工作中的几点建议。     

Individual food-hoarding decisions in a nonterritorial coal tit population: the role of social context

Among the Paridae, food hoarding is thought to be strongly associated with the exclusive use of territories by winter groups, although it has also been described in populations with loose social systems. However, detailed data on such populations are scarce. To identify the mechanisms underlying individual storing decisions, I studied hoarding behaviour in a nonterritorial, high-density coal tit, Parus ater, population in a subalpine forest. The presence of close neighbours (within 5 m) had the strongest, negative influence on caching probability, whereas more distant neighbours foraging in the same flock did not affect the probability of caching. Adults concentrated their stores in the centre of their home ranges. Caching location, but not caching intensity, was affected by the time of day. Coal tits took longer, and travelled further, to cache food in the inner parts of trees than in the outer parts. Resident adults stored in inner, safer caching locations more often than juvenile residents and transients. Differences in hoarding effort according to the storing substrate, and the daily storing location pattern of juvenile residents and transients, suggest that stores have a different use depending on where they are located. Therefore, my results show that hoarding is compatible with a nonterritorial, nonbreeding social system; hoarding could thus have originated in an ancient, nonterritorial, but sedentary, tit species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Neural and hormonal control of food hoarding

Many animals hoard food, including humans, but despite its pervasiveness, little is known about the physiological mechanisms underlying this appetitive behavior. We summarize studies of food hoarding in humans and rodents with an emphasis on mechanistic laboratory studies of species where this behavior importantly impacts their energy balance (hamsters), but include laboratory rat studies although their wild counterparts do not hoard food. The photoperiod and cold can affect food hoarding, but food availability is the most significant environmental factor affecting food hoarding. Food-deprived/restricted hamsters and humans exhibit large increases in food hoarding compared with their fed counterparts, both doing so without overeating. Some of the peripheral and central peptides involved in food intake also affect food hoarding, although many have not been tested. Ad libitum-fed hamsters given systemic injections of ghrelin, the peripheral orexigenic hormone that increases with fasting, mimics food deprivation-induced increases in food hoarding. Neuropeptide Y or agouti-related protein, brain peptides stimulated by ghrelin, given centrally to ad libitum-fed hamsters, duplicates the early and prolonged postfood deprivation increases in food hoarding, whereas central melanocortin receptor agonism tends to inhibit food deprivation and ghrelin stimulation of hoarding. Central or peripheral leptin injection or peripheral cholecystokinin-33, known satiety peptides, inhibit food hoarding. Food hoarding markedly increases with pregnancy and lactation. Because fasted and/or obese humans hoard more food in general, and more high-density/high-fat foods specifically, than nonfasted and/or nonobese humans, understanding the mechanisms underlying food hoarding could provide another target for behavioral/pharmacological approaches to curb obesity.     

Daily accumulation of body reserves under increased predation risk in captive Greenfinches Carduelis chloris

The effect of increased perceived risk of predation on the trajectory describing the daily gain in body mass of captive Greenfinches Carduelis chloris was tested. Theoretically, increased risk of predation is expected to shift the gain in body mass towards the latter part of the day and reduce body mass. The perceived risk of predation was increased with a stuffed flying hawk three times per day. Following each presentation of the predator, foraging stopped and the birds lost mass. When feeding resumed, the birds compensated for the mass loss by increasing the rate of body mass gain, in line with theoretical predictions. In the presence of the predator, the daily accumulation of body reserves was lower compared with risk-free situations. However, on the days following presentation of the hawk, when the birds were presumably aware of an increased risk of predation, Greenfinches did not exhibit the predicted change in reserve accumulation, but rather maintained their usual pattern of body mass gain.     

Effects of foraging effort on body fat and food hoarding in Siberian hamsters

Food hoard size varies inversely with body fat levels in Siberian hamsters. If food hoarding only increases when body fat decreases, then hamsters foraging for their food should only increase food hoarding when foraging efforts decrease body fat ("lipostatic hypothesis"); however, if food hoarding increases whenever there is an energy flux away from fat storage, then it should increase regardless of significant body fat decreases ("metabolic hypothesis"). Female Siberian hamsters (Phodopus sungorus) earned food pellets after completion of a programmed number of wheel revolutions (Immobilized Wheel [free access to food], Free Wheel [wheel active, free food], and 10, 50, 100, and 200 revolutions/pellet). Hamsters were killed after 19 days and inguinal, retroperitoneal, and parametrial white adipose tissue (WAT) pads (IWAT, RWAT, and PWAT, respectively) were harvested and carcass composition determined. Food hoard size increased fourfold with the availability of running wheels alone (Free Wheel), increased threefold with low foraging levels (10 and 50 revolutions/pellet), but was nearly abolished at the highest foraging level (200 revolutions/pellet). Surplus food (earned, not eaten or hoarded) was significantly greatest at the lowest level of foraging. As foraging effort increased, PWAT mass decreased the most (<10 revolutions/pellet), while RWAT and IWAT mass only were decreased at the highest foraging effort. Carcass lipid content only was significantly decreased at the highest foraging effort, yet food hoarding was nearly abolished at that level. Collectively, these results demonstrate that body fat levels and food hoarding can be uncoupled with increases in foraging effort. J. Exp. Zool. 289:162-171, 2001.     

Hyper-dispersed cache distributions reduce pilferage: a laboratory study

Many animals use hoarding as a long-term strategy to ensure a food supply at times of shortage. We suggest that long-term scatter hoarders, whose caches are vulnerable to potentially high pilferage, should hoard in ways to reduce cache loss. This could be achieved by manipulating the density and dispersal patterns of caches to reduce the foraging efficiency of pilferers. This study explores the effect of distribution patterns on cache loss in the laboratory. We recorded the discovery of food items in different dispersal patterns by two bird species: coal tits Periparus ater (a hoarder) and great tits Parus major (a non-hoarder). Hyper-dispersed distributions reduced foraging efficiency because both species used systematic local search patterns. This study shows that hyper-dispersed distributions would be advantageous to hoarding animals to reduce cache loss.     

Strategic diel regulation of body mass in European robins

Stochastic dynamic programming (SDP) is a computational technique that has been used to model daily routines of foraging in small birds. A diurnal bird must build up its fat reserves towards dusk in order to avoid starvation during the night, when it cannot feed. However, as well as the benefits of avoiding starvation, storing fat imposes costs such as an increased predation risk and higher flight and metabolic costs. There is therefore an optimal level of fat reserves for a bird to reach at dusk in order to survive overnight without being left with excessive fat reserves at dawn. I tested a prediction common to all SDP models of daily foraging routines, that a bird will attempt to reach this level at dusk, regardless of its fat reserves the previous dawn. I provided supplementary food to manipulate the fat reserves at dawn of free-living European robins, Erithacus rubecula. Diurnal changes in body mass (a reliable estimate of fat reserves) were then monitored remotely. Robins provided with an ad libitum food supply reached almost exactly the same body mass at dusk, regardless of their body mass at dawn, supporting the prediction that birds attempt to reach a target level of reserves at dusk. Copyright 2000 The Association for the Study of Animal Behaviour.     

Fat pad-specific effects of lipectomy on foraging, food hoarding, and food intake

Unlike most species, after food deprivation, Siberian hamsters increase foraging and food hoarding, two appetitive ingestive behaviors, but not food intake, a consummatory ingestive behavior. We previously demonstrated (Wood AD, Bartness TJ, Am J Physiol Regul Integr Comp Physiol 272: R783-R792, 1997) that increases in food hoarding are triggered by directly decreasing body fat levels through partial surgical lipectomy; however, we did not test if lipectomy affected foraging, nor if the magnitude of the lipid deficit affected food hoard size. Therefore, we tested whether varying the size of the lipectomy-induced lipid deficit and/or foraging effort affected foraging, food hoarding, or food intake. This was accomplished by housing adult male Siberian hamsters in a foraging/hoarding system and removing (x) both epididymal white adipose tissue (EWATx) pads, both inguinal white adipose tissue (IWATx) pads, or both EWAT and IWAT pads (EWATx + IWATx) and measuring foraging, food hoarding, and food intake for 12 wk. The lipectomy-induced lipid deficit triggered different patterns of white adipose tissue mass compensation that varied with foraging effort. Foraging for food (10 wheel revolutions to earn a food pellet) abolished the EWATx-induced compensation in IWAT pad mass. The magnitude of the lipid deficit did not engender a proportional change in any of the appetitive or consummatory ingestive behaviors. EWATx caused the greatest increase in food hoarding compared with IWATx or EWATx + IWATx, when animals were required to forage for their food. Collectively, it appears that the magnitude of a lipid deficit does not affect appetitive or consummatory behaviors; rather, when energy (foraging) demands are increased, loss of specific (gonadal) fat pads can preferentially stimulate increases in food hoarding.     

Strategic Regulation of Body Mass and Singing Behavior in New Zealand Robins

The ‘small bird in winter’ paradigm states that body mass is a balance between the conflicting demands of carrying enough energy to survive nightly fasts while minimizing the risk of predation associated with carrying additional fat reserves. We conducted a short‐term food‐supplementation experiment during which New Zealand robins (Petroica australis) were provided with food on the second day of a 3‐d trial. This allowed us to test two predictions from models of strategic mass regulation in small birds: (1) individual birds reach the same end‐of‐day mass despite differences in their initial morning mass while, (2) using surplus energy for increased singing. As expected, robins gained mass at a higher rate early in the morning on the fed day than they did on either of the two control days, but there was no significant difference in their evening masses across the 3 d of the experiment despite birds on day 3 starting at higher initial masses than birds on day 1. Robins displayed a significantly higher rate of singing when receiving food supplements on day 2, supporting a link between energetic reserves and behavior. Our results suggest that potentially energetically costly behaviors, such as song production, are sensitive to short‐term changes in energy reserves, and that both state and behavioral predictions can be successfully integrated to provide tests of state‐based models of behavior.     

Coal Tit fat-storing patterns during the non-breeding season: the role of residence status

According to the optimal body mass hypothesis, resident individuals, having priority of resource access and better knowledge of food availability in an area, should carry smaller fat reserves than transients whose resource predictability is lower. We tested this prediction in a free-living population of Coal Tits Parus ater in sub-alpine coniferous forest during three winters. We examined the role of residence status in determining the daily patterns of fat accumulation of individuals using time of day, temperature, season, year and body size as covariates. Only time of day, residence status and temperature significantly affected daily variation of fat score in Coal Tits. Fat scores were higher in transients than residents, although within residents, juveniles did not carry significantly more fat than adults. Our results show that fattening strategies are associated with residence status in the Coal Tit, in support of the hypothesis that transient individuals facing lower food predictability carry larger body fat reserves. The finding that within residents, patterns of fat accumulation did not differ between adults and juveniles, suggests that residence per se , involving higher food predictability, rather than age-related dominance or hoarding behaviour, determines fattening strategies in wild Coal Tits.     

Food supplementation and predation risk in harsh climate: interactive effects on abundance and body condition of tit species

Food availability and predation risk can have drastic impacts on animal behaviour and populations. The tradeoff between foraging and predator avoidance is crucial for animal survival and will strongly affect individual body mass, since large fat reserves are beneficial to reduce starvation but may increase predation risk. However, two‐factor experiments simultaneously investigating the interactive effects of food and predation risk, are still rare. We studied the effects of food supplementation and natural predation risk imposed by pygmy owls Glaucidium passerinum on the abundance and fat reserves of tit species in boreal forests of north Europe, from January to March in 2012 and in 2013. Food supplementation increased the number of individuals present in a given forest patch, whereas the level of predation risk had no clear impact on the abundance of tit species. The stronger impact of food supply respect to predation risk could be the consequence of the harsh winter conditions in north Europe, with constant below‐zero temperatures and only few (5–7 h) daylight hours available for foraging. Predation risk did not have obvious effects on tit abundance but influenced food consumption and, together with food supplementation, affected the deposition of subcutaneous fat in great tits Parus major. High owl predation risk had detrimental effects on body fat reserves, which may reduce over‐winter survival, but the costs imposed by pygmy owl risk were compensated when food was supplemented. The starvation–predation tradeoff faced by great tits in winter may thus be mediated through variation in body fat reserves. In small species living in harsh environment, this tradeoff appeared thus to be biased towards avoidance of starvation, at the cost of increasing predation risk.     

Patterns of feeding and food pellet retrieval by Norway rats during food deprivation

This study examined whether, for Norway rats suffering a body weight deficit of sufficient magnitude, food hoarding is prepotent over feeding. Rats food-deprived to 85% ad lib weight were videotaped during hoarding sessions that lasted until they ceased to hoard or eat to obtain complete records of retrieval and feeding. During the early minutes of a trial, feeding was the predominant activity, and food pellet retrieval occurred singly or in short bouts. This gave way over time to diminished eating and extended bouts of retrieval (hoarding). Closer analysis suggested that retrieval and feeding were aroused together and at the beginning of such arousal retrieval was momentarily prepotent over feeding. But once retrieval had occurred, there was a shift in favor of feeding. After the rat had consumed a sufficient amount of food, feeding was no longer aroused to the same degree, so bouts of retrieval occurred without feeding. Electronic Publication     

围栏条件下社鼠的食物贮藏行为

在北京东灵山地区, 用活捕笼从野外捕获社鼠, 并在野外建造围栏, 以山杏种子和辽东栎坚果为备选食物, 对围栏条件下社鼠的食物贮藏行为进行了研究。数据的统计分析采用SPSS for Windows (version 1010) 进行。结果表明: 1) 社鼠主要表现出食物的集中贮藏方式; 2) 贮藏食物被模拟盗窃使社鼠的食物贮藏活动加强; 3)社鼠倾向于选择山杏种子进行贮藏, 而对辽东栎坚果则取食较多。文中还讨论了食物类型、模拟盗窃等因素对社鼠食物贮藏行为的影响。     

Mass gained during breeding positively correlates with adult survival because both reflect life history adaptation to seasonal food availability

Both mass (as a measure of body reserves) during breeding and adult survival should reflect variation in food availability. Those species that are adapted to less seasonally variable foraging niches and so where competition dominates during breeding, will tend to have a higher mass increase via an interrupted foraging response, because their foraging demands increase and so become more unpredictable. They will then produce few offspring per breeding attempt, but trade this off with higher adult survival. In contrast, those species that occupy a more seasonal niche will not gain mass because foraging remains predictable, as resources become superabundant during breeding. They can also produce more offspring per breeding attempt, but with a trade-off with reduced adult survival. We tested whether the then predicted positive correlation between levels of mass gained during seasonal breeding and adult survival was present across 40 species of tropical bird measured over a 10-year period in a West African savannah. We showed that species with a greater seasonal mass increase had higher adult survival, controlling for annual mass variation (i.e. annual variation in absolute food availability) and variation in the timing of peak mass (i.e. annual predictability of food availability), clutch size, body size, migratory status and phylogeny. Our results support the hypothesis that the degree of seasonal mass variation in birds is probably an indication of life history adaptation: across tropical bird species it may therefore be possible to use mass gain during breeding as an index of adult survival.     

The predator-prey size hypothesis in three assemblages of forest birds

I investigated morphological pattern and preysize preference of three bird assemblages (14 species altogether) in a Hungarian oak forest, during the breeding seasons of 1979–1986. To assess the occurrence of competition for food among forest birds I performed a 5-year removal experiment with two hole-nesting passerines, the great tit and the blue tit. Prey preference of both species was affected by the presence of the other species. The results of both the removal experiment and the estimation of available food supply indicated food limitation, at least for foliage-gleaning birds. However, I found neither a regular size ratio among species nor a strong relationship between predator size and prey size. Other phenomena such as foraging strategies may affect preysize preference. Therefore, a competition model including only morphological ratios and predator-prey size relationships is too simplified.     

Vulnerability to severe weather and regulation of body mass of Icelandic and British Redshank Tringa totanus

During severe weather, Redshanks suffer the heaviest mortality amongst all the shorebird species wintering around the North Sea coasts of the British Isles. An earlier study had suggested that this resulted from a failure to accumulate sufficient body fat reserves before mid-winter. Detailed field studies in northeast England between 1993 and 1995 of seasonal changes in body mass, and in estimated lean and fat masses, of two races of Redshank, both of which winter in the same estuary, were accompanied by similar studies of small numbers held in captivity with unlimited food. After differences in body size were allowed for, there were no differences in body composition and its seasonal pattern of change in birds of the Icelandic and British races. Body mass changes in wild birds paralleled those in captives between November and March, and mid-winter levels were not limited by food supply; indeed they were slightly higher in a winter with lower prey densities. It is concluded that Redshanks regulate body mass and, indirectly, fat reserves at levels set by a trade-off between the risks of predation and starvation. Unlike most other shorebird species, they take very small prey in relation to their body size and hence must feed for long periods during each tidal cycle to achieve their daily energy intake needs. Thus they have little scope to extend their feeding time during severe weather, which also forces them to feed on ice-free exposed coastal habitats where wind chill cannot be avoided. Both factors lead to more rapid depletion of fat reserves than in other species which have higher energy intake rates or lower total daily requirements.     

Management of fat reserves and food caches in tufted titmice (Parus bicolor) in relation to unpredictable food supply

In the temperate zone, permanent-resident birds and mammalsthat do not hibernate must survive harsh winter conditions oflow ambient temperature, long nights, and reduced food levels.To understand the energy management strategy of food-hoardingbirds, it has been hypothesized that such birds respond to increasedstarvation risk by increasing the number of their hoards ratherthan by increasing their fat reserves and that they cache earlyin the day and retrieve their caches later to achieve fat reservesnecessary to survive the night We tested these hypotheses byobserving the responses in captivity of a caching bird, thetufted titmouse (Parus bicolor), to the combined influencesof reduced predictability of food and naturally occurring ambienttemperature and photoperiod. When the food supply was unpredictable,birds significantly increased both internal fat reserves atdusk and external food caches. Initially leaner birds tendedto increase their fat reserves to a greater extent and initiallyfatter birds tended to cache more food and to fly significantlyless. Half the birds also increased their dawn and mean dailybody mass. All birds tended to forage, gain body mass, and cachefood at significantly lower rates in the morning and at significantlyhigher rates in the evening. Cache retrieval showed the oppositetrend, with birds retrieving most of their caches in the morning.Our results do not support the hypothesis that caching birdsincrease caching rate but not body mass under an unpredictablefood regime. Instead fat reserves and food caches are both importantcomplementary sources of energy in food-hoarding birds. Energymanagement by wintering birds occurs in response to a numberof biotic and abiotic factors acting simultaneously; thus futuremodels must incorporate independent variables in addition tothe state of the food supply and time of day