Mechanisms of Cache Retrieval in the Group Nesting Southern Flying Squirrel (Glaucomys volans)

We examined the proximate mechanisms of cache retrieval in the group‐living, southern flying squirrel, Glaucomys volans, through a series of behavioral experiments conducted in a large indoor arena. The effectiveness of several retrieval mechanisms was determined including spatial memory, olfaction, random searching and a heuristic under different environmental conditions. Our goal was to elucidate the hoarding strategy of individuals in a nest group and to address whether food storing individuals possess a retrieval advantage over pilfering nestmates. A storer's retrieval advantage is necessary for scatter hoarding to be an evolutionarily stable strategy (ESS) within aggregations of unrelated individuals. Our previous work has shown that, G. volans lives in such groups, and consequently it was important to address the storer's retrieval advantage under a range of environmental conditions. Initially in our baseline experiment, we developed methods to eliminate olfactory‐based retrieval and to control for random searching. Subsequently, we experimentally determined the effectiveness of cache retrieval via spatial memory, a heuristic and olfaction. We examined the mechanisms of cache retrieval in three additional experiments using two independent subject populations and found that under dry, odorless conditions spatial memory was the most effective retrieval mechanism in support of a storer's retrieval advantage. In a fifth experiment we examined cache retrieval under wet environmental conditions and showed that olfactory‐based retrieval was effective and the storer's advantage was reduced. We interpret these laboratory results based on considerations of natural environmental conditions and game theory. We propose a conditional ESS strategy where animals store and retrieve their own caches as the primary food hoarding tactic and opportunistically pilfer caches as a secondary tactic.     

Memory for food caches: not just for retrieval

Many animals use hoarding as a long-term strategy to ensurea food supply at times of shortage. Hoarders employ strategiesthat enhance their ability to relocate caches such as rememberingwhere caches are located. Long-term scatterhoarders, whose cacheshave potentially high pilferage rates, should also hoard ina way to reduce potential cache pilferers' ability to find caches.Previous studies have demonstrated that this could be achievedby hyperdispersing caches to reduce the foraging efficiencyof pilferers. This study investigates whether coal tits (Parusater) indeed place their caches away from existing ones. Inour experiment, birds hoarded food in 3 conditions: when cachesfrom a previous storage session were still present, when cachesfrom a previous storage session were not present anymore becausethe bird had retrieved them, and when caches from a previousstorage session had been removed by the experimenter. We showthat coal tits hoard away from existing caches and that theydo not use cues from extant caches to do this. This evidenceis consistent with the use of memory for the locations of previouscaches when deciding where to place new caches. This findinghas important implications for our understanding of the selectivepressures that have shaped spatial memory in food-hoarding birds.     

Social context hinders humans but not ravens in a short-term memory task

Using resources shared within a social group—either in a cooperative or a competitive way—requires keeping track of own and others’ actions, which, in turn, requires well-developed short-term memory. Although short-term memory has been tested in social mammal species, little is known about this capacity in highly social birds, such as ravens. We compared ravens (Corvus corax) with humans in spatial tasks based on caching, which required short-term memory of one's own and of others’ actions. Human short-term memory has been most extensively tested of all social mammal species, hence providing an informative benchmark for the ravens. A recent study on another corvid species (Corvus corone) suggests their capacity to be similar to the humans’, but short-term memory skills have, to date, not been compared in a social setting. We used spatial setups based on caches of foods or objects, divided into individual and social conditions with two different spatial arrangements of caches (in a row or a 3 × 3 matrix). In each trial, a set of three up to nine caches was presented to an individual that was thereafter allowed to retrieve all items. Humans performed better on average across trials, but their performance dropped, when they had to keep track of partner's actions. This differed in ravens, as keeping track of such actions did not impair their performance. However, both humans and ravens demonstrated more memory-related mistakes in the social than in the individual conditions. Therefore, whereas both the ravens’ and the humans’ memory suffered in the social conditions, the ravens seemed to deal better with the demands of these conditions. The social conditions had a competitive element, and one might speculate that ravens’ memory strategies are more attuned to such situations, in particular in caching contexts, than is the case for humans.     

Long-term hoarding in the Paridae: a dynamic model

Using stochastic dynamic programming we modeled the hoardingand foraging behavior of tits and chickadees, Pandas, that areresident in the boreal forest at high latitudes. Here autumnshave a rich supply of seeds and temperatures are relativelymild, while winters are cold with short days and a low foodsupply. We assumed that parids have a memory of limited durationand that forgotten seeds accumulate in a bank that adds to thegeneral food supply in the hoarder's territory. Our model predictsthat birds should start "high-intensity" hoarding in early autumn,but not before that. Because of mass-dependent costs the birdswill keep their fat levels low during the autumn. When winterarrives they will carry more body fat, both for the long winternights and to hedge against the large effects of weather variationsin winter. After increasing the fat level at the start of winter,fat should gradually increase even more, to compensate for thediminishing food supply. Most hoarding occurs in autumn as away of building up the supply of long-term stores. Remembered,or short-term caches, may hedge against stochastic events inthe environment. Even though conditions are not beneficial forhoarding in winter, the birds still stored in winter to maintainlarger short and long-term hoards if environmental variationincreased. Almost all time in winter that not was spent foragingwas spent perching, mainly to avoid predation     

Common ravens raid arctic fox food caches

Cache recovery is critical for evolution of hoarding behaviour, because the energy invested in caching may be lost if consumers other than the hoarders benefit from the cached food. By raiding food caches, animals may exploit the caching habits of others, that should respond by actively defending their caches. The arctic fox (Alopex lagopus) is the main predator of lemmings and goose eggs in the Canadian High Arctic and stores much of its prey in the ground. Common ravens (Corvus corax) are not as successful as foxes in taking eggs from goose nests. This generalist avian predator regularly uses innovation and opportunism to survive in many environments. Here, we provide the first report that ravens can successfully raid food cached by foxes, and that foxes may defend their caches from ravens.     

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.     

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.     

Effects of habitat and season on removal and hoarding of seeds of wild apricot (Prunus armeniaca) by small rodents

The wild apricot (Prunus armeniaca) is widely distributed in the Donglingshan Mountains of Mentougou District of Beijing, China, where its seeds may be an important food resource for rodents. Predation, removal and hoarding of seeds by rodents will inevitably affect the spatio-temporal pattern of seed fate of wild apricot in this area. By marking and releasing tagged seeds of wild apricot, we investigated seeds survival, scatter-hoarding, cache size and seedling establishment, and the preference of micro-habitats used by rodents to store seeds. The results showed that: (1) rodents in this area hoarded food intensively in autumn, as well as in spring and summer. (2) There were significant effects of habitat and season on removal rate of tagged seeds at releasing plots. In both two types of habitats, Low and High shrub, tagged seeds were removed most rapidly by rodents in autumn, at intermediate rates in spring and least rapidly in summer. (3) During three seasons, mean dispersal distance of scatter-hoarded seeds in Low shrub habitat was greater than that in High shrub. Most removed seeds were buried within 21.0 m of the releasing plots. (4) In both two types of habitats, Low and High shrub, rodents tended to carry seeds to US (Under shrub) and SE (Shrub edge) microhabitats for scatter-hoarding or predation. (5) Among the caches made by rodents, most caches contained only one seed, but up to three seeds were observed; caches of 2–3 seeds were common in autumn. (6) By comparing dental marks, we determined that large field mice (Apodemus peninsulae) and David’s rock squirrels (Sciurotamias davidianus) contributed to removal and predation of released tagged seeds. However, only the large field mice exerted a pivotal and positive role on the burial of dispersed seeds. (7) Establishment of three seedlings originated from seeds buried by rodents was documented in High shrub habitat.     

Scatter Hoarding of Seeds Confers Survival Advantages and Disadvantages to Large-Seeded Tropical Plants at Different Life Stages

Scatter hoarding of seeds by animals contributes significantly to forest-level processes, including plant recruitment and forest community composition. However, the potential positive and negative effects of caching on seed survival, germination success, and seedling survival have rarely been assessed through experimental studies. Here, I tested the hypothesis that seed burial mimicking caches made by scatter hoarding Central American agoutis (Dasyprocta punctate) enhances seed survival, germination, and growth by protecting seeds from seed predators and providing favorable microhabitats for germination. In a series of experiments, I used simulated agouti seed caches to assess how hoarding affects seed predation by ground-dwelling invertebrates and vertebrates for four plant species. I tracked germination and seedling growth of intact and beetle-infested seeds and, using exclosures, monitored the effects of mammals on seedling survival through time. All experiments were conducted over three years in a lowland wet forest in Costa Rica. The majority of hoarded palm seeds escaped predation by both invertebrates and vertebrates while exposed seeds suffered high levels of infestation and removal. Hoarding had no effect on infestation rates of D. panamensis, but burial negatively affected germination success by preventing endocarp dehiscence. Non-infested palm seeds had higher germination success and produced larger seedlings than infested seeds. Seedlings of A. alatum and I. deltoidea suffered high mortality by seed-eating mammals. Hoarding protected most seeds from predators and enhanced germination success (except for D. panamensis) and seedling growth, although mammals killed many seedlings of two plant species; all seedling deaths were due to seed removal from the plant base. Using experimental caches, this study shows that scatter hoarding is beneficial to most seeds and may positively affect plant propagation in tropical forests, although tradeoffs in seed survival do exist.     

Is hippocampal volume affected by specialization for food hoarding in birds?

The hypothesis that spatial-memory specialization affects the size of the hippocampus has become widely accepted among scientists. The hypothesis comes from studies on birds primarily in two families, the Paridae (tits, titmice and chickadees) and the Corvidae (crows, nutcrackers, jays, etc.). Many species in these families store food and rely on spatial memory to relocate the cached items. The hippocampus is a brain structure that is thought to be important for memory. Several studies report that hoarding species in these families possess larger hippocampi than non-hoarding relatives, and that species classified as large-scale hoarders have larger hippocampi than less specialized hoarders. We have investigated the largest dataset on hippocampus size and food-hoarding behaviour in these families so far but did not find a significant correlation between food-hoarding specialization and hippocampal volume. The occurrence of such an effect in earlier studies may depend on differences in the estimation of hippocampal volumes or difficulties in categorizing the degree of specialization for hoarding or both. To control for discrepancies in measurement methods we made our own estimates of hippocampal volumes in 16 individuals of four species that have been included in previous studies. Our estimates agreed closely with previous ones, suggesting that measurement methods are sufficiently consistent. Instead, the main reasons that previous studies have found an effect where we did not are difficulties in assessing the degree of hoarding specialization and the fact that smaller subsets of species were compared than in our study. Our results show that a correlation between food-hoarding specialization and hippocampal volume cannot be claimed on the basis of present data in these families.