Fine-scale food hoarding decisions in New Zealand Robins ( Petroica australis ): is inter-sexual competition important?

Competition for cache retrieval is hypothesised to influence food hoarding intensity. Previous work has tested this hypothesis by evaluating food hoarding rates during foraging bouts when animals are exposed to different levels of competition for cache retrieval. Little is known about how competition might influence fine-scale food hoarding decisions within foraging bouts. I evaluated fine-scale food hoarding decisions of New Zealand Robins (Petroica australis) by offering mealworms to competitively dominant males and subordinate females, both when they were alone and when they foraged together. I then compared food hoarding rates of sequentially handled prey between sexes and social conditions by assessing how the total number of prey cached increased with the total number of prey handled. Relationships for solitary females, solitary males and paired males were non-linear, indicating that they were more likely to consume initially handled prey, and increasingly likely to cache subsequently handled prey items. Non-linear rates of food hoarding may result from declines in the energetic value of prey that are consumed and stored internally as birds become satiated. Somewhat differently, the relationship for paired females was linear, indicating that paired females make a single food hoarding decision based on bout-level foraging conditions, which results in constant fine-scale food hoarding rates. Constant food hoarding rates in paired females, which experience the strongest competitive effects of any treatment, suggest that food consumption is consistently more advantageous than food hoarding under these conditions, regardless of satiation level. Overall results from this study indicate that New Zealand Robins continuously update food hoarding decisions according to their competitive environment and satiation levels, resulting in scale-dependent patterns in food hoarding intensity.     

Food hoarding,but not food intake,is attenuated by acute diazepam treatment in female Mongolian gerbils (Meriones unguiculatus)

This article is part of a Special Issue “Energy Balance”. Effects of γ-aminobutyric acid (GABA) on food hoarding are unknown in rodents, and the effects of energy balance and GABA have not been evaluated in females. To evaluate the role of food deprivation and GABA on food hoarding, female Mongolian gerbils were given i.p. injection of diazepam (1 mg/kg and 3 mg/kg, respectively), a GABA_A receptor agonist. Among food-deprived females, there was a bimodal pattern in the frequency of gerbils with different levels of food hoarding. High food hoarding (HFH) and low food hoarding (LFH) gerbils were analyzed. Diazepam blocked food deprivation-induced food hoarding in HFH gerbils, but not in LFH gerbils. This blockade was associated with increased cellular activation in selected brain areas, such as the nucleus accumbens (NAcc), caudate putamen (CP) and ventral tegmental area (VTA), which suggested that direct activation of GABA in the brain reward circuitry decreased food hoarding in HFH females. Moreover, diazepam increased Fos expression in field CA₂ and CA₃ of the hippocampus, but had no significant effect on Fos expression in field CA₁ and dentate gyrus (DG) of the hippocampus, indicating that the hippocampus has area-specific effects on food hoarding in HFH gerbils. Diazepam did not alter food intake in both HFH and LFH gerbils. In addition, serum corticosterone concentrations were higher in the HFH than in the LFH ones. Together, these data indicated that food deprivation increased food hoarding in female gerbils, diazepam reduced food deprivation-induced food hoarding in HFH gerbils, and that GABA might influence food hoarding via classical reward circuitry via the mesolimbic dopamine system and specific hippocampal areas.     

An influence of hormones on hoarding behavior in the Mongolian gerbil (Meriones unguiculatus)

Three experiments on food hoarding behavior in the Mongolian gerbil (Meriones unguiculatus) demonstrated (1) that females hoarded more than males, (2) that castration increased food hoarding in males, and (3) that administration of testosterone propionate to castrate males inhibited hoarding. The adaptive value of these relationships and their implications for a physiological model of food hoarding in the rodent are discussed.     

Energetic challenges unmask the role of ovarian hormones in orchestrating ingestive and sex behaviors

Effects of ovarian hormones on sex and ingestive behavior are well studied, and yet, their role in diverting attention from food to sex has not been examined directly, possibly because these functions are masked under conditions of excessive food abundance typical of the laboratory. Female Syrian hamsters were either fed ad libitum or food-restricted to 75% of their ad libitum intake for 8 days and then tested every day of the estrous cycle for their preference for males versus food, food hoarding and food intake in an apparatus designed to mimic aspects of their natural habitat. The food-restricted, but not the fed females, varied significantly over the estrous cycle in appetitive behaviors, which included their preference for males versus food and in the amount of food hoarded, with low food hoarding and high male preference on the night of ovulation. In contrast, there were no significant differences between restricted and ad libitum-fed females in the consummatory behaviors, namely, food intake or lordosis duration. In ovariectomized females, estradiol plus progesterone treatment delayed food restriction-stimulated hoarding and hastened feeding-inhibited hoarding without affecting food intake or lordosis duration. In summary, energy restriction and the presence of males unmasked an effect that was obscured in the normal laboratory conditions characterized by isolation and an over abundance of readily available food. These results are consistent with the idea that ovarian hormones orchestrate appetites for food and sex to optimize reproductive success under fluctuating energetic conditions.     

Climate change and perishable food hoards of an avian predator: Is the freezer still working?

Changing climate can modify predator–prey interactions and induce declines or local extinctions of species due to reductions in food availability. Species hoarding perishable food for overwinter survival, like predators, are predicted to be particularly susceptible to increasing temperatures. We analysed the influence of autumn and winter weather, and abundance of main prey (voles), on the food‐hoarding behaviour of a generalist predator, the Eurasian pygmy owl (Glaucidium passerinum), across 16 years in Finland. Fewer freeze–thaw events in early autumn delayed the initiation of food hoarding. Pygmy owls consumed more hoarded food with more frequent freeze–thaw events and deeper snow cover in autumn and in winter, and lower precipitation in winter. In autumn, the rotting of food hoards increased with precipitation. Hoards already present in early autumn were much more likely to rot than the ones initiated in late autumn. Rotten food hoards were used more in years of low food abundance than in years of high food abundance. Having rotten food hoards in autumn resulted in a lower future recapture probability of female owls. These results indicate that pygmy owls might be partly able to adapt to climate change by delaying food hoarding, but changes in the snow cover, precipitation and frequency of freeze–thaw events might impair their foraging and ultimately decrease local overwinter survival. Long‐term trends and future predictions, therefore, suggest that impacts of climate change on wintering food‐hoarding species could be substantial, because their ‘freezers’ may no longer work properly. Altered usability and poorer quality of hoarded food may further modify the foraging needs of food‐hoarding predators and thus their overall predation pressure on prey species. This raises concerns about the impacts of climate change on boreal food webs, in which ecological interactions have evolved under cold winter conditions.     

A comparative analysis of feeding and hoarding in hamsters and gerbils

Male and female hamsters and gerbils were randomly assigned to one of three groups. The animals were tested under ad lib feeding conditions or food deprived until they had lost either 10% or 20% of their predeprivation body weight. They were given a 30-min. hoarding test for three consecutive days. The results indicated that although food-deprived gerbils ate more than control gerbils, deprivation had no significant effect on the food intake of hamsters. A sex difference was also evident in the food intake of gerbils; males ate more than did females. Although there was a sex and species difference in the amount of hoarding, deprivation had no significant effect on the amount of hoarding. The implications of these results for of different models of hoarding are discussed. These models contrast hoarding as a defensive response in the regulation of body weight or as an anticipatory activity that is influenced by other selection pressures.     

剥夺食物对雄性长爪沙鼠贮食行为的影响

禁食导致一些啮齿动物的贮食量增加,但禁食处理后雄性长爪沙鼠贮食行为的变化则不一致。每天禁食22 h,长爪沙鼠的一些个体表现出高水平的贮食行为(禁食贮食组),而另一些个体则没有表现出贮食行为(禁食无贮食组)。延长禁食(22 h)持续的时间(连续重复3 d 和20 d)和增加禁食时间(禁食48 h),都没有使禁食无贮食组的动物表现出贮食行为。同样在自由取食条件下,长爪沙鼠的贮食行为也表现为二型性。在自由取食和禁食条件下,贮食量与体重、体脂含量和瘦素的浓度之间无明显相关关系。研究结果表明,禁食是诱导雄性长爪沙鼠贮食行为发生的一个重要条件,但增加禁食的程度并不改变其贮食行为的表现。     

Experimentally induced sickness decreases food intake, but not hoarding, in Siberian hamsters (Phodopus sungorus)

A wide range of physiological and behavioral alterations occur in response to sickness. Sickness behaviors, rather than incidental by-products or side-effects of acute illness, serve as adaptive functional responses that allow animals to cope with a pathogenic challenge. Among the more salient sickness behaviors is a reduction in food intake; virtually all sick animals display marked decreases in this behavior. Food intake, however, is only one component of the food-related behavioral repertoire. For many mammalian species, food hoarding represents a substantial portion of the total energetic budget. Here we tested the effects of experimental sickness on food hoarding and food intake in a naturally food hoarding species, Siberian hamsters (Phodopus sungorus). Adult male and female hamsters received injections of lipopolysaccharide (LPS) to induce sickness or control injections. LPS-induced sickness resulted in a marked decrease in food intake in both males and females, but did not decrease hoarding in either sex. These results support previous findings suggesting that food hoarding and food intake appear to be differentially regulated at the physiological level.     

Food hoarding behaviour of large field mouseApodemus peninsulae

An important behavioural adaptation for animal species with variable or unpredictable food availability is storing food. Food availability for large field mouseApodemus peninsulae (Thomas, 1907) is not reliable. We conducted a series of tests with the large field mouse to determine food hoarding behaviour, response when their hoarded food was removed, and whether perishable foods were treated different than non perishable foods. The study was conducted in four semi-natural enclosures (4 × 3 × 1 m), established on the Donglingshan Mountain near Beijing, China. Thirteen large field mice were placed in enclosures and offered wild apricotPrunus armeniaca seeds and Liaodong oakQuercus liaotungensis acorns. Our results indicated that although large field mice hoarded seeds in larder and scatter patterns, they more frequently exhibited larder hoarding. Liadong oak acorns were generally consumed near the feeder, whereas apricot seeds were more frequently transported to the nest box. Only apricot seeds were scattered among hoard sites. When seeds were removed from hoarding sites the mice responded by taking increased amounts of seeds to their nest for larder and scatter hoarding. Hoarding sites were not randomly distributed throughout the enclosure.     

Seasonal changes in neuron numbers in the hippocampal formation of a food‐hoarding bird: The black‐capped chickadee

The volume of the hippocampal formation (HF) in black‐capped chickadees (Poecile atricapillus) varies across the seasons, in parallel with the seasonal cycle in food hoarding. In this study, we estimate cell density and total cell number in the HF across seasons in both juveniles and adults. We find that the seasonal variation in volume is due to an increase in the number of small and large cells (principally neurons) in the fall. Adults also have lower neuron densities than juveniles. Both juveniles and adults show an increase in cell density in the rostral part of the HF in August and a subsequent decrease toward October. This suggests that the net cell addition to the HF may already start in August. We discuss the implications of this early start with respect to the possibility that the seasonal change in HF volume is driven by the experience of food hoarding. We also speculate on the functional significance of the addition of neurons to the HF in the fall. © 2000 John Wiley & Sons, Inc. J Neurobiol 44: 414–422, 2000     

Food hoarding is increased by food deprivation and decreased by leptin treatment in Syrian hamsters

Compensatory increases in food intake are commonly observed after a period of food deprivation in many species, including laboratory rats and mice. Thus it is interesting that Syrian hamsters fail to increase food intake after a period of food deprivation, despite a fall in plasma leptin concentrations similar to those seen in food-deprived rats and mice. In previous laboratory studies, food-deprived Syrian hamsters increased the amount of food hoarded. We hypothesized that leptin treatment during food deprivation would attenuate food-deprivation-induced increases in hoarding. Baseline levels of hoarding were bimodally distributed, with no hamsters showing intermediate levels of hoarding. Both high (HH) and low hoarding (LH) hamsters were included in each experimental group. Fifty-six male hamsters were either food deprived or given ad libitum access to food for 48 h. One-half of each group received intraperitoneal injections of leptin (4 mg/kg) or vehicle every 12 h during the food-deprivation period. Within the HH group, the hoarding score increased significantly in food-deprived but not fed hamsters (P < 0.05). Leptin treatment significantly decreased hoarding in the food-deprived HH hamsters (P < 0.05). The LH hamsters did not increase hoarding regardless of whether they were food deprived or had ad libitum access to food. These results are consistent with the idea that HH hamsters respond to energetic challenges at least in part by changing their hoarding behavior and that leptin might be one factor that mediates this response.     

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.     

NPY Y1 receptor is involved in ghrelin- and fasting-induced increases in foraging, food hoarding, and food intake

Fasting triggers a constellation of physiological and behavioral changes, including increases in peripherally produced ghrelin and centrally produced hypothalamic neuropeptide Y (NPY). Refeeding stimulates food intake in most species; however, hamsters primarily increase foraging and food hoarding with smaller increases in food intake. Fasting-induced increases in foraging and food hoarding in Siberian hamsters are mimicked by peripheral ghrelin, central NPY, and NPY Y1 receptor agonist injections. Because fasting stimulates ghrelin and subsequently NPY synthesis/release, it may be that fasting-induced increased hoarding is mediated by NPY Y1 receptor activation. Therefore, we asked: Can an Y1 receptor antagonist block fasting- or ghrelin-induced increases in foraging, food hoarding, and food intake? This was accomplished by injecting the NPY Y1 receptor antagonist 1229U91 intracerebroventricularly in hamsters fasted, fed, or given peripheral ghrelin injections and housed in a running wheel-based food delivery foraging system coupled with simulated-burrow housing. Three foraging conditions were used: 1) no running wheel access, free food, 2) running wheel access, free food, or 3) foraging requirement (10 revolutions/pellet) for food. Fasting was a more potent stimulator of foraging and food hoarding than ghrelin. Concurrent injections of 1229U91 completely blocked fasting- and ghrelin-induced increased foraging and food intake and attenuated, but did not always completely block, fasting- and ghrelin-induced increases in food hoarding. Collectively, these data suggest that the NPY Y1 receptor is important for the effects of ghrelin- and fasting-induced increases in foraging and food intake, but other NPY receptors and/or other neurochemical systems are involved in increases in food hoarding.     

Hoarding behavior by ship rats (Rattus rattus) in captivity and its relevance to the effectiveness of pest control operations

Hoarding of food items is well known among muroid rodents, but evidence for hoarding behavior among ship rats (Rattus rattus) is scant. Here, we characterize hoarding behavior in ship rats maintained in captivity after capture from the wild. After acclimatization to captivity, 40 ship rats (21 females, 19 males) were presented with baits in experiments designed to emulate a typical poison control operation for vertebrate pests in New Zealand: this involved first offering rats nontoxic cereal baits (of 2- or 6-g size) as a prefeed for three nights consecutively, followed by 6- or 12-g cereal baits laden with 0.15% 1080 on the fourth night. Seventy-eight percent of rats (31/40) hoarded food in distinct cache sites when presented with nontoxic baits although there was no significant effect of bait size or type on hoarding behavior and nor did hoarding behavior vary according to rat gender. When rats were presented with 1080-laden baits, the incidence of hoarding was reduced to 40%, due to the onset of toxicosis. This study indicates that R. rattus will show hoarding behavior analogous to other rat species when presented with an excess of cereal-based baits, at least under conditions of captivity and free from competition. This finding may have practical relevance: since 1080 is the principal toxin used against the major vertebrate pest species in New Zealand (the brushtail possum, Trichosurus vulpecula), ship rats have the potential to deplete supplies of prefeed and/or toxic baits intended for possum control. However, based on typical rat densities recorded in New Zealand native forest (c. 5 rats/ha), the degree of removal and manipulation of toxic baits observed by ship rats here is unlikely to impact adversely on the efficacy of possum control operations.     

Feeding and hoarding behaviour of the Eurasian red squirrelSciurus vulgaris during autumn in Hokkaido, Japan

The feeding habits and hoarding behaviour of the Eurasian red squirrelSciurus vulgaris Linnaeus, 1758 were examined during autumn in Nopporo Forest Park (43°20’N, 141°30’E), in western Hokkaido, Japan. The diet consisted of 32 plant species. Twelve species were both eaten and hoarded (the two most common of which wereAbies sachalinensis andPinus koraiensis), and 20 species were eaten but not hoarded. The distance from where a food item was found to the hoarding spot averaged 50 m and differed significantly according to food type. WalnutsJuglans regia were transported farthest, and chestnutsCastanea crenata to the second farthest from the site of origin. Most food was hoarded beneath the ground surface (95%), but some were hoarded in forks of trees and in small tree holes. Squirrels selected food items of high energy content for hoarding, in preparation for winter and the breeding season.     

Spacing Behavior of a Non‐Larder‐Hoarding Tamiasciurus: A Study of Mearns's Squirrels in Xeric Coniferous Forests

In ecosystems with seasonal fluctuations in food supply many species use two strategies to store food: larder hoarding and scatter hoarding. However, because species at different geographic locations may experience distinct environmental conditions, differences in hoarding behavior may occur. Tree squirrels in the genus Tamiasciurus display variation in hoarding behavior. Whereas red (Tamiasciurus hudsonicus) and Douglas's (Tamiasciurus douglasii) squirrels in mesic coniferous forests defend territories centered around larder hoards maintaining non‐overlapping home ranges, red squirrels in deciduous forests defend small scatter‐hoarded caches of cones maintaining overlapping home ranges. As in other rodent species, variation in hoarding behavior appears to influence the spacing behavior of red and Douglas's squirrels. In contrast, Mearns's squirrels (Tamiasciurus mearnsi) in xeric coniferous forests neither rely on larder hoards nor appear to display territorial behavior. Unfortunately, little is known about the ecology of this southernmost Tamiasciurus. Using radiotelemetry, we estimated home‐range size, overlap, and maximum distance traveled from nest to examine the spacing behavior of Mearns's squirrels. Similar to scatter‐hoarding rodents, maximum distance traveled from nest was greater for males during mating season, whereas those of females were similar year round. Although no seasonal differences were detected, male home ranges were three times larger during mating season, whereas those of females were smaller and displayed a minor variation between seasons. Home ranges were overlapped year round but contrary to our expectations, overlap was greater during mating season for both sexes, with no detectable relationship between male home‐range size and the number of females overlapped during mating season. Overall, the results appear to support our hypothesis that in the absence of larder hoards, the spacing behavior of Mearns's squirrels should be different from larder‐hoarding congeners and more similar to scatter‐hoarding rodents.     

布氏田鼠合作贮食行为及其影响因素

合作贮食是社会性动物应对食物匮乏的重要对策,但其内在的生态学机制尚未阐明。本文以布氏田鼠为研究对象,根据亲缘关系划分为亲缘组和非亲缘组。在人工实验箱中录像统计不同组别合作贮食行为占用时间的差异,探究亲缘关系对合作贮食行为的影响,并利用相关性分析探究亲缘组个体对贮食的贡献—收益关系以及与贮食行为相关的个体特征因素。结果表明,在组间水平上,与非亲缘组相比,亲缘组的布氏田鼠表现更多的合作贮食。在亲缘组个体水平上,不同个体对贮食的参与度和贡献度存在很大差异。个体对合作贮食的付出与其取食的收益呈显著负相关关系,并且个体合作贮食贡献越大,其睾丸指数和睾酮含量降低越显著。研究结果说明,亲缘关系的存在有利于布氏田鼠的合作贮食,但合作贮食贡献大的个体,其繁殖受到了抑制。     

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.     

Hoarding versus the immediate consumption of food among hamsters and gerbils

This project dealt with a comparative analysis of the effects of food deprivation on feeding and hoarding in hamsters and gerbils. The animals were given food in their home cage and their food intake was measured during a 30-min period after which they were transferred to an apparatus in which hoarding behaviour was assessed. The results indicated interesting species differences in the animals' reactions in the test situations. Whereas food-deprived gerbils ate more food than nondeprived gerbils, the food intake of hamsters was not significantly enhanced by deprivation. In the hoarding test, although significant differences were observed between deprived and nondeprived gerbils, the absolute level of hoarding in gerbils was very low in comparison to that of hamsters tested under the same conditions. These results suggest that hamsters and gerbils respond to challenges to their food reserves with different strategies.     

Effects of burrow condition and seed handling time on hoarding strategies of Edward's long-tailed rat (Leopoldamys edwardsi)

Many hoarding rodents use burrows not only for dwelling and protection from natural enemies, but also for food storage. However, little is known how burrows used by scatter-hoarding animals influence their foraging behaviors. In addition, handling time for a given food item has a fundamental impact on hoarding strategies of these hoarding animals: food items with longer handling time are more likely to be hoarded due to increasing predation risk because the animals spend more time outside their burrows if they consumed such food. By providing with two types of artificial burrows (aboveground vs. underground) and two types of food items (i.e. seeds) with contrasting handling times, we investigated how burrow condition and handling time co-influence hoarding strategies of a key scatter-hoarding rodent, Edward's long-tailed rat (Leopoldamys edwardsi) in large enclosures in southwest China. We found that only a few animals larder-hoarded fewer seeds when only aboveground burrows were available, while over 80% of the animals preferred to use the underground burrows and hoard significantly more seeds in the burrows when both aboveground and underground burrows were provided simultaneously. We also found that seed handling time significantly affected hoarding strategies of the animals: they consumed and/or scatter-hoarded more Camellia oleifera seeds with shorter handling time outside the burrow, but consumed and larder-hoarded more Lithocarpus harlandii seeds with longer handling time in underground burrows. Our study indicates that both burrow types and seed handling time have important impacts on hoarding strategies of scatter-hoarding animals.