Michael A. Steele

DETERMINANTS OF SEED REMOVAL DISTANCE BY SCATTER-HOARDING RODENTS IN DECIDUOUS FORESTS

Scatter-hoarding rodents should space food caches to maximize cache recovery rate (to minimize loss to pilferers) relative to the energetic cost of carrying food items greater distances. Optimization models of cache spacing make two predictions. First, spacing of caches should be greater for food items with greater energy content. Second, the mean distance between caches should increase with food abundance. However, the latter prediction fails to account for the effect of food abundance on the behavior of potential pilferers or on the ability of caching individuals to acquire food by means other than recovering their own caches. When considering these factors, shorter cache distances may be predicted in conditions of higher food abundance. We predicted that seed caching distances would be greater for food items of higher energy content and during lower ambient food abundance and that the effect of seed type on cache distance variation would be lower during higher food abundance. We recorded distances moved for 8636 seeds of five seed types at 15 locations in three forested sites in Pennsylvania, USA, and 29 forest fragments in Indiana, U.S.A., across five different years. Seed production was poor in three years and high in two years. Consistent with previous studies, seeds with greater energy content were moved farther than less profitable food items. Seeds were dispersed less far in seed-rich years than in seed-poor years, contrary to predictions of conventional models. Interactions were important, with seed type effects more evident in seed-poor years. These results suggest that, when food is superabundant, optimal cache distances are more strongly determined by minimizing energy cost of caching than by minimizing pilfering rates and that cache loss rates may be more strongly density-dependent in times of low seed abundance.

The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels

The dentate gyrus is one of two areas in the mammalian brain that produces neurons in adulthood. Neurogenesis (proliferation, survival, and differentiation of new neurons) is regulated by experience, and increased neurogenesis appears to be correlated with improved spatial learning in mammals and birds. We tested the hypothesis that in long‐lived mammals that scatter‐hoard food, seasonal variations in spatial memory processing (i.e. increased processing during caching season in the autumn) might correlate with changes in neurogenesis and neuron number in the granule cell layer of the dentate gyrus (gcl DG). We investigated the rate of cell proliferation and the total number of neurons in the granule cell layer of wild adult eastern grey squirrels (Sciurus carolinensis) at three different times of the year (October, January and June). We found no seasonal differences in cell proliferation rate or in total neuron number in the granule cell layer. Our findings are in agreement with those of previous studies in laboratory mice and rats, and in free‐ranging, food‐caching, black‐capped chickadees, as well as with current hypotheses regarding the relationship between neurogenesis and learning. Our results, however, are also in agreement with the hypothesis that neurogenesis in the dentate gyrus represents a maintenance system that may be regulated by environmental factors, and that changes in total neuron number previously reported in rodents represent developmental changes rather than adult plasticity. The patterns observed in mature wild rodents, such as free‐ranging squirrels, may represent more accurately the extent of hippocampal plasticity in adult mammals.

Caching and Feeding Decisions by Sciurus carolinensis: Responses to Weevil-Infested Acorns

We tested the caching and feeding responses of gray squirrels ( Sciurus carolinensis ) to acorns of three species of oaks ( Quercus alba, Q. palustris , and Q. rubra ) infested with weevil larvae ( Curculio ). Experiments were designed to test the primary hypothesis that squirrels selectively cache sound acorns and the secondary hypothesis that such response may be due to increased perishability resulting from infestation. In an open, suburban oak ( Quercus ) forest in northeastern Pennsylvania, we presented free-ranging animals with whole, infested acorns, whole, noninfested acorns, and noninfested acorns from which the pericarp (shell) was removed to increase perishability. Squirrels cached significantly (20–35%) more of whole, intact acorns of red oak, dispersed these acorns significantly greater distances before caching them, and consumed shelled and infested acorns. Squirrels showed a similar response to acorns of pin oak, but ate significantly more of both infested and noninfested acorns of white oak. Squirrels also were observed to consume weevil larvae in >76% of all trials with infested acorns. These results indicate that squirrels can distinguish between infested and noninfested acorns, that they often selectively cache sound acorns, and that weevils represent a significant dietary supplement for squirrels. We also suggest that gray squirrels may exert a strong influence on the dispersal of oaks by selecting viable seeds for storage.

CACHE MANAGEMENT BY SMALL MAMMALS: EXPERIMENTAL EVIDENCE FOR THE SIGNIFICANCE OF ACORN-EMBRYO EXCISION

Abstract We conducted 2 field experiments to assess relative importance of acorn-embryo excision in the caching decisions of small mammals. In the 1st, we selectively provisioned small mammals with metal-tagged acorns of red oak (Quercus rubra) and white oak (Q. alba) at 40 point locations in 8 sites in an oak forest in northeastern Pennsylvania. We then followed the fate of cached seeds by relocating acorns with metal detectors soon after they were cached and again in spring after seeds began to germinate. At least 1 species of small mammal excised embryos of >70% of the cached acorns of white oak and <4% of those of red oak. Animals also were observed to revisit caches in spring and excise embryos of germinating acorns. More excised acorns of white oak were found intact in spring than those of red oak, indicating that the behavior is important for long-term storage of these seeds. In a 2nd experiment, we presented free-ranging Mexican gray squirrels (Sciurus aureogaster) with pairs of acorns of 5 native white oak and 5 native red oak species and recorded caching events and whether or not cached seeds had their embryos removed. Squirrels cached significantly more acorns of white oak species, frequently excised embryos of these seeds, and only excised embryos of red oaks when they were germinating. These results support our previous hypothesis that the behavior of embryo excision is geographically widespread and has important implications for cache-management strategies of some diurnal tree squirrels and their effect on dispersal of oaks.

Sex differences, but no seasonal variations in the hippocampus of food-caching squirrels: A stereological study

Recent studies have described sex differences in the relative size of the hippocampus that are associated with sex differences in space use in birds and short‐lived mammals. A correlation between spatial learning and increased hippocampal volume has also been demonstrated in food‐caching animals. Such results suggest that sexually dimorphic spatial learning (sex differences in space use during the breeding season) and seasonal variations in food‐caching behavior (spatial memory for cache locations) might correlate with morphological changes in the hippocampus of adult long‐lived mammals. We used modern stereological techniques to examine the volume and neuron number of the structures forming the hippocampal complex ( dentate gyrus , CA3, and CA1) of wild adult eastern gray squirrels (Sciurus carolinensis) throughout the year. We observed differences in brain size between samples collected at different times of the year (October, January, and June). Our analysis showed sex differences, but no seasonal variations, in the volume of CA1 stratum oriens and stratum radiatum. There were no sex differences or seasonal variations in the relative volume or the number of neurons of any other layer of the structures forming the hippocampal complex. These results confirm the existence of sex differences in the structure of the hippocampus; however, this sexual dimorphism does not vary seasonally in adulthood and is likely to result from developmental processes. These results do not support the hypothesis that seasonal variations in food‐caching behavior might correlate with morphological changes, such as variations in volume or neuron number, in the hippocampal complex of adult long‐lived mammals. J. Comp. Neurol. 425:152–166, 2000.

The innate basis of food-hoarding decisions in grey squirrels: evidence for behavioural adaptations to the oaks

Rodents selectively cache acorns of red oak species (subgenus Erythrobalanus; RO) over those of white oaks (subgenus Quercus; WO) because of perishability of early-germinating WO acorns. On occasion, at least three species of tree squirrels also will cache white oak acorns, but only after they excise acorn embryos, thereby preventing germination. Failure to observe embryo excision of acorns in several other mammal species led us to hypothesize that tree squirrels may have an innate tendency to perform embryo excision and possibly the differential caching of RO and WO acorns. To test this, we evaluated the hoarding decisions of eight captive-reared (naive) eastern grey squirrels, Sciurus carolinensis, with no previous experience with acorns and four wild-caught squirrels. Squirrels were presented individually with pairs of dormant RO and nondormant WO acorns (two species) and pairs of dormant and nondormant RO acorns over a 2-month period. Both naive and wild-caught squirrels selectively cached dormant RO acorns more often than those of one WO species (Quercus alba), but showed a much weaker response to other pairs of dormant and nondormant acorns. Naive squirrels also removed the radicles of germinating acorns, and on occasion, attempted to excise embryos of germinating acorns. We conclude that there is a strong innate basis for some of the hoarding decisions made by tree squirrels, strengthening an emerging argument that tree squirrels show specific behavioural adaptations to the oaks.

Cache protection strategies of a scatter-hoarding rodent: do tree squirrels engage in behavioural deception?

Behavioural deception has been studied experimentally primarily in captive-raised primates and corvids, and only in a laboratory setting. Here we show that free-living eastern grey squirrels, Sciurus carolinensis, caching food in the presence of conspecifics perform behavioural deception by covering additional empty sites where nothing has been cached. Such deceptive caching (1) occurred in two distinct populations, (2) occurred more often in the close presence of conspecifics and (3) reduced the probability of cache pilferage by surrogate (human) cache pilferers. In an additional experiment, in which we attempted to elicit deceptive behaviour by pilfering caches, deceptive caching appeared as one behaviour in a suite of pilferage-avoidance responses. To our knowledge, this is the first study to show evidence of behavioural deception by a rodent, and the first to use an experimental approach to studying deceptive behaviour in the wild.

Seed fate and decision-making processes in scatter-hoarding rodents

A mechanistic understanding of seed movement and survival is important both for the development of theoretical models of plant population dynamics, spatial spread, and community assembly, and for the conservation and management of plant communities under global change. While models of wind‐borne seed dispersal have advanced rapidly over the past two decades, models for animal‐mediated dispersal have failed to make similar progress due to their dependence on interspecific interactions and complex, context‐dependent behaviours. In this review, we synthesize the literature on seed dispersal and consumption by scatter‐hoarding, granivorous rodents and outline a strategy for development of a general mechanistic seed‐fate model in these systems. Our review decomposes seed dispersal and survival into six distinct sub‐processes (exposure, harvest, allocation, preparation, placement, and recovery), and identifies nine intermediate (latent) variables that link physical state variables (e.g. seed and animal traits, habitat structure) to decisions regarding seed allocation to hoarding or consumption, cache placement and management, and deployment of radicle‐pruning or embryo excision behaviours. We also highlight specific areas where research on these intermediate relationships is needed to improve our mechanistic understanding of scatter‐hoarder behaviour. Finally, we outline a strategy to combine detailed studies on individual functional relationships with seed‐tracking experiments in an iterative, hierarchical Bayesian framework to construct, refine, and test mechanistic models for context‐dependent, scatter‐hoarder‐mediated seed fate.

Scatterhoarding rodents favor higher predation risks for cache sites: The potential for predators to influence the seed dispersal process.

Scatterhoarding rodents often place caches in the open where pilferage rates are reduced, suggesting that they tradeoff higher risks of predation for more secure cache sites. We tested this hypothesis in two study systems by measuring predation risks inferred from measures of giving-up densities (GUDs) at known cache sites and other sites for comparison. Rodent GUDs were measured with small trays containing 3 L of fine sand mixed with sunflower seeds. In the first experiment, we relied on a 2-year seed dispersal study in a natural forest to identify caches of eastern gray squirrels (Sciurus carolinensis) and then measured GUDs at: (i) these caches; (ii) comparable points along logs and rocks where rodent activity was assumed highest; and (iii) a set of random points. We found that GUDs and, presumably, predation risks, were higher at both cache and random points than those with cover. At the second site, we measured GUDs of eastern gray squirrels in an open park system and found that GUDs were consistently lowest at the base of the tree compared to more open sites, where previous studies show caching by squirrels to be highest and pilferage rates by naïve competitors to be lowest. These results confirm that predation risks can influence scatterhoarding decisions but that they are also highly context dependent, and that the landscape of fear, now so well documented in the literature, could potentially shape the temporal and spatial patterns of seedling establishment and forest regeneration in systems where scatterhoarding is common.

Alternative strategies of seed predator escape by early-germinating oaks in Asia and North America

Early germination of white oaks is widely viewed as an evolutionary strategy to escape rodent predation; yet, the mechanism by which this is accomplished is poorly understood. We report that chestnut oak Quercus montana (CO) and white oak Q. alba (WO) (from North America), and oriental cork oak Q. variabilis (OO) and Mongolian oak Q. mongolica (MO) (from Asia) can escape predation and successfully establish from only taproots. During germination in autumn, cotyledonary petioles of acorns of CO and WO elongate and push the plumule out of the cotyledons, whereas OO and MO extend only the hypocotyls and retain the plumule within the cotyledons. Experiments showed that the pruned taproots (>6 cm) of CO and WO acorns containing the plumule successfully germinated and survived, and the pruned taproots (≥12 cm) of OO and MO acorns without the plumule successfully regenerated along with the detached acorns, thus producing two seedlings. We argue that these two distinct regeneration morphologies reflect alternative strategies for escaping seed predation.