Scatter-hoarding Rodents Research Articles

Proteomic evidence for seed odor modifying olfaction and spatial memory in a scatter-hoarding animal

Seed odor plays a crucial role in affecting the scatter-hoarding behavior of small rodents that rely on spatial memory and olfaction to cache and recover. However, evidence of how seed odor modifies olfaction function and spatial memory is still lacking. Here, we coated seeds with waterproof glue to test how seed odor intensity alters the proteome of both the olfactory bulbs and hippocampus of a dominant scatter-hoarding rodent, Leopoldamys edwardsi, in Southwest China. We showed that animals repeatedly caching and recovering weak odor seeds exhibited greater olfactory ability and spatial memory, as indicated by alterations in the protein profiles of the olfactory bulbs and hippocampus. The upregulation of proteins closely related to neural connections between the olfactory bulb and hippocampus is highly responsible for improved olfactory function and spatial memory. Our study provides new insights into how scatter-hoarding rodents manage and respond to cached seeds differing in odor intensity from a neurobiological perspective, which is of significant importance for better understanding the parallel evolution of the olfactory and hippocampal systems.

Tree isolation enhances seed dispersal behavior by scatter-hoarding rodents

Tree isolation enhances seed dispersal behavior by scatter-hoarding rodents

Effects of subtle variation in forest canopy openness on cache pilferage and its implications for forest regeneration.

Scatter-hoarding rodents play important roles in plant regeneration and species coexistence in many forest ecosystems. Cache pilferage, the behavior of rodents seeking or relocating seeds cached by other individuals, is ubiquitous during the scatter-hoarding process. The effects of canopy openness on cache pilferage have received considerable attention, most of which have focused on the comparison between full canopy cover and completely open areas, such as forest gaps. However, little attention has been given to whether the subtle variation in forest canopy openness affects cache pilferage, although subtle variation in light environments exists in many forests, especially tropical and subtropical forests, where the overall canopy is large and the forest window is relatively small. Here, we directly tested these questions by simulating 400 artificial caches, each containing one seed from four selected tree species, in a subtropical forest in southwestern China. The overall canopy openness of the forest was relatively small (with a mean value of 11.1%), but subtle spatial variation still existed (ranging from 5.7% to 19.5%). Overall, caches with lower canopy openness were more likely to be pilfered and removed faster, although not all species showed the same pattern. Our study highlights that subtle variation in forest canopy openness, even in a closed primary forest, has significant effects on cache pilferage by rodents, which may influence the following seed germination and forest regeneration processes. Additionally, seedling species composition may further be altered because the canopy effects on cache pilferage are species-specific.

Scatter-hoarding rodents are important seed dispersers in pine plantations

The caching behavior of rodents is widely considered to facilitate plant seed dispersal and seedling regeneration in forest ecosystems. Studies supporting this theory have been based mainly on experimental results from natural forests; however, whether scatter-hoarding rodents play an important role in seed dispersal and seedling regeneration in tree plantations remains unclear. In this study, we tracked 4000 seeds over 2 years in a Pinus armandii plantation in southwest China to investigate their fate from seed removal to survival after hoarding. We found that rodents removed more than 30.0% of the released seeds in both years, 9.9% to 29.1% of the seeds were scatter-hoarded under the leaf litter or on the soil surface, and a few seeds were removed two to three times. The dispersal distance of scatter-hoarded seeds ranged from 0.4 to 14.5 m with a mean of 3.55 m, and re-caching processes increased the dispersal distance of cached seeds. Additionally, 18.9% of the removed seeds survived in the cache until the end of the observation period. Our results suggested that scatter-hoarding rodents play an important role in seed dispersal in planted forests.

Use of logging roads by terrestrial mammals in a responsibly managed neotropical rainforest in Guyana

Selective logging is the most widespread use of tropical forests. Building logging roads facilitates access to previously remote rainforests, and so proper management is essential for ensuring biodiversity retention in logged landscapes. Terrestrial mammals often directly use logging roads (via movement corridors, hunting or foraging), making them vulnerable to poorly managed roads. Here we explore how the presence, arrangement and use of logging roads influence terrestrial mammal occupancy and detection within a Forest Stewardship Council (FSC) certified logged forest in Guyana. We compared camera trap data from20 natural ‘game’ trails in an unlogged area, with camera trap data from 23 sites set near to or on logging roads within the Iwokrama forest. Our findings showed high occupancy within logged areas with no statistically significant difference to unlogged areas. Higher detections were noted along secondary and feeder roads compared to skid trails and the natural trails in control areas. Additionally, our data showed a negative correlation between occupancy and distance to village for a scatter hoarding rodent, most likely driven by subsistence hunting by local communities. Our results indicate that proper road management geared towards the monitoring and guarded access of logging roads, can have a positive effect on terrestrial mammal occurrence within responsibly managed rainforests.

Impacts of human forest management on seed dispersal patterns by scatter-hoarding rodents

Abstract Scatter-hoarding rodents play a central role in seed dispersal, predating and dispersing seeds that affect many plant species’ population dynamics and influence forest regeneration. Anthropogenic changes in forest structure, such as clear-cutting in dense forests, may alter the ecological interactions between seeds and dispersers. This study compared predation and dispersal patterns of holm oak (Quercus ilex L.) acorns by wood mouse (Apodemus sylvaticus L.) in original dense forest [less managed forest (MF)] vs open MF (more MF) in north-eastern Spain. Results showed variations in the patterns of acorn predation and dispersal by wood mouse between forest types. In the MF, a greater fraction of acorns was harvested, and the acorns were being dispersed further than in the original forest. Despite the greater fraction of acorns dispersed in the MF, the proportion of acorns that survived and had the potential to grow was reduced in the MF because of increased predation. This shows that forest management has a significant influence on seed dispersal by rodents and thereby influences the natural regeneration potential of forests.

Behavioral adaptation of sympatric rodents to early germination of oak acorns: radicle pruning and embryo excision.

The seed germination schedule is a key factor affecting the food-hoarding behavior of animals and the seedling regeneration of plants. However, little is known about the behavioral adaptation of rodents to the rapid germination of acorns. In this study, we provided Quercus variabilis acorns to several rodent species to investigate how food-hoarding animals respond to seed germination. We found that only Apodemus peninsulae adopted embryo excision behavior to counteract seed germination, which is the first report of embryo excision in nonsquirrel rodents. We speculated that this species may be at an early stage of the evolutionary response to seed perishability in rodents, given the low rate of embryo excision in this species. On the contrary, all rodent species preferred to prune the radicles of germinating acorns before caching, suggesting that radicle pruning is a stable and more general foraging behavior strategy for food-hoarding rodents. Furthermore, scatter-hoarding rodents preferred to scatter-hoard and prune more germinating acorns, whereas they consumed more nongerminating acorns. Acorns with embryos excised rather than radicles pruned were much less likely to germinate than intact acorns, suggesting a behavioral adaptation strategy by rodents to the rapid germination of recalcitrant seeds. This study provides insight into the impact of early seed germination on plant-animal interactions.

Contrasting seed traits of co-existing seeds lead to a complex neighbor effect in a seed-rodent interaction.

Scatter-hoarding rodents play important roles in seed dispersal and predation in many forest ecosystems. Existing studies have shown that the seed foraging preference of rodents is directly affected by seed traits and indirectly affected by the traits of other co-existing seeds nearby (i.e., neighbor effect). Plant seeds exhibit a combination of diverse seed traits, including seed size, chemical defense, and nutrient content. Therefore, it is difficult to evaluate the influence of each single seed trait on such neighbor effects. Here, by using artificial seeds, we investigated the impacts of contrasts in seed size, tannin content, and nutrient content on neighbor effects. We tracked 9000 tagged artificial seeds from 30 seed-seed paired treatments in a subtropical forest in southwest China. The contrast in seed size between paired seeds created obvious neighbor effects measured through three seed dispersal related indicators: the proportion of seeds being removed, the proportion of seeds cached, and the distance transported by rodents. However, the magnitudes and the signs of the neighbor effects differed among pairs, including both apparent mutualism and apparent competition, depending on the contrast in seed size between paired seeds. The contrasts of tannin and nutrient content between paired seeds showed relatively few neighbor effects. Our results suggest that the contrast in seed traits between the target seed and its neighboring seeds should be considered when studying rodent-seed interactions. Furthermore, we expect that similar complex neighbor effects may also exist in other plant-animal interactions, such as pollination and herbivory.

The morphological and ecological variation of Arctostaphylos (Ericaceae) fruit: A link between plant ecology and animal foraging behavior.

Persistent soil seed banks are characteristic of Arctostaphylos (Ericaceae) species in the Mediterranean-climate California Floristic Province. While most species are obligate seeders, regeneration of stands of all Arctostaphylos species ultimately depends on post-fire seedling recruitment. Arctostaphylos seed banks are created, in large part, by scatter-hoarding rodents. Variation in fruit morphology, therefore, is expected to impact the Arctostaphylos-rodent interaction. Seeds produce sufficient rewards (nutritious mature embryo) to entice rodents to disperse and ultimately bury seeds in the soil. Hard seed coats increase the time required to extract the embryo, encouraging rodents to choose storage over immediate predation, and nutlets are frequently empty. We assessed the variation of fruit nutlet fusion and seed viability among 38 Arctostaphylos taxa. Factors such as latitude, elevation, life history, ploidy, and phylogenetic position were also analyzed. Generalized mixed-effects models were used to determine the factors contributing to variation in fruit nutlet fusion and seed viability. Our results indicate that fruit volume and shape are the most important variables affecting nutlet fusion and seed viability. Additionally, other potential influences only show a weak correlation and are not predicted to significantly impact nutlet fusion or seed viability. These findings provide insights into evolved strategies used by plants to increase reproductive success via scatter-hoarding rodents. Our study benefits the conservation and restoration of Arctostaphylos stands by emphasizing the importance of animal-mediated dispersal and providing estimates of seed viability for different species. With the anticipated effects of climate change, such as departures from historic fire regimes, the preservation of the relationship between plants and animal foragers is crucial for the continued survival of Arctostaphylos and California's evergreen chaparral.

Tree density-dependence effects on seed dispersal of a large-seeded tropical tree

Abstract One of the biggest issues in plant ecology is determining the interaction outcome between seeds and scatter-hoarding rodents because the latter has a dual role as dispersers and predators of seeds. Density-dependence contexts involving resource abundance largely influence the outcome of this interaction. Here, we investigated how the variation in the density of a large-seeded tropical tree (Joannesia princeps Vell) affects its probability of seed removal, consumption, dispersal, and burial by a neotropical rodent (Dasyprocta azarae Lichtenstein). We tested whether the elevated resource availability in high tree density areas would cause scatter hoarder’s satiation by decreasing seed removal and consumption (predator satiation hypothesis) or increasing seed dispersal and burial (predator dispersal hypothesis). We tracked the fate of 461 seeds in 14 plots with distinct J. princeps abundances inside a large Atlantic Forest fragment. We used spool-and-line tracking and camera trappings to determine seed fate and identify interacting animals. Agouti was the only species removing J. princeps seeds. Tree density benefitted J. princeps by increasing seed dispersal through buried seed but not affecting seed removal and consumption. This result shows how density-dependent contexts, such as tree density, may alter seed fate in seed–rodent interactions supporting future studies aiming to reestablishing seed dispersal functions in Atlantic Forest fragments.

Potential seed dispersal mechanism of Kigelia africana (Lam.) Benth. in an urban habitat

ABSTRACT Kigelia africana is known to exhibit megafaunal syndrome. Many mega faunal taxa having become extinct with time, the species seems to have adapted to its changing environment by ensuring the dispersal of its seeds by alternative dispersers. The present investigation reports the mechanism of seed dispersal adopted by individuals of K. africana grown in India, outside the species natural environment. The massive – ~2.0 kg – indehiscent and unattractive fruits retain the wingless seeds. Of more than 300 seeds present in a fruit in average, approximately 92% remained viable at maturity, and the viability decreased over time after 1 year. We observed that numerous termites (Coptotermes formosanus) initiated the disintegration of the fallen fruits particularly during monsoon. Three-striped squirrels (Funambulus palmarum), classified as scatter hoarding rodents, then accessed these fruits and their seeds, and actively carried about 48% seeds with broken coats to a distance of 40 m away from the mother trees. The coordinated activity of these two dynamic vectors ensured successful seed dispersal in K. africana at the study site, suggesting that the species may have developed a way to adapt to its new environment.

Seed size-seed number trade-offs: influence of seed size on the density of fire-stimulated persistent soil seed banks.

Does the seed size-seed number allocation trade-off model apply to long-term persistent soil seed banks? This trade-off between seed size versus number of seeds produced is usually applied at a single population on an annual basis. Our question is how this model might apply to close relatives that produce dormant seed forming long-term persistent soil seed banks. These two criteria allow a focus on divergent evolution of conspecifics and permits us to isolate seed size in the spectrum of life history traits that may be influencing seed traits, and on how seed size influences accumulation and persistence in the soil. In California, Arctostaphylos species only produce physiologically dormant seed that are fire-stimulated and that vary in seed size permitting seed size-seed bank density relationship as a test of the seed size-seed number allocation model. Soil seed banks of 10 species of Arctostaphylos were sampled with fruit volumes ranging from 21-1063 mm3 . Seed bank density was determined by hand extraction from soil samples. We found that seed bank densities were significantly negatively related to fruit or seed size. Rather than an issue of allocational trade-off between size and number, we interpret these results as reflecting seed predation and postfire seedling establishment. Seed bank densities, even after decades, generally were less than one or two-year's seed production, suggesting intense seed predation. Burial by scatter-hoarding rodents provided sufficient seeds deep enough for survival of fire. Variation on seed size suggests seedling establishment constraints, but it needs further research.

Ecology of fear and its effect on seed dispersal by a neotropical rodent

Abstract Predators exert negative effects on prey, besides the act of killing, generating behavioral and physiological costs, a concept known as the ecology of fear. Studies in scatter-hoarding rodents in temperate zones suggests that prey use habitat structure to perceive predation risk. Less is known about how tropical forest rodents perceive predation risk. Here, we investigated whether the Central American agouti perceive predation risk by ocelots through olfactory cues and whether it influences the foraging behavior for Attalea butyracea seeds, one of its main food sources. By monitoring tagged seeds, we found that seed dispersal and pilferage was lower in sites with high density of ocelots, in line with the predictions of ecology of fear proposing that scared animals eat less. We also found that pilferage rates in high ocelot density sites seem to be lower during the rainy—transition period but not during dry season when food availability is generally low. However, we did not find evidence that agoutis adjust their cache spacing behavior in response to ocelot density. In an additional experiment to corroborate that agoutis’ responses were caused by ocelots’ cues, we found lower dispersal rates for seeds placed next to samples of urine and feces of ocelots as compared to controls, during the first seven days. Moreover, agoutis spent less time handling the seeds with ocelots’ cues. Here, we discuss potential cascading effects linked to the behavior of agoutis towards predation risk.

Seed size affects rodent-seed interaction consistently across plant species but not within species: evidence from a seed tracking experiment of 41 tree species.

Scatter-hoarding rodents play a crucial role in seed survival and seed dispersal. As one of the most important seed traits, seed size and its effect on rodent-seed interaction attract lots of attention. Current studies usually target one or a few species and show inconsistent patterns; however, few experiments include a large number of species although many plant species usually coexist in natural forest and overlap in fruiting time. Here, we tracked the dispersal and predation of 26100 seeds belonging to 41 tree species in a subtropical forest for 2 years. Most species showed no relationships between seed size and rodent foraging preference, while the remaining species displayed diverse of patterns: monotonic decrease and increase trends, and hump-shaped and U-shaped patterns, indicating that a one-off study with a few species might give misleading information. However, the seed size effect across species was consistent in both years, indicating that including a large number of species that hold a sufficient range of seed size may avoid the aforementioned bias. Interestingly, seed size effect differed among rodent foraging processes: a negative effect on seed harvest, a hump-shaped effect on seed removal and removal distance, while a positive effect on overwinter survival of cached seeds, indicating that rodents may make trade-offs between large and small seeds both among foraging processes and within a single process, thus lead to a parabolic relationship between seed size and seed dispersal success, that is medium-sized seeds were more likely to be removed and cached, and transported with a further distance.

Canopy openness of individual tree promotes seed dispersal by scatter-hoarding rodents

Scatter-hoarding rodents are important seed predators and dispersers in various forest ecosystems and significantly influence the seed fate and seedling regeneration of many tree species. Canopy openness is believed to have an important influence on the foraging behavior of scatter-hoarding rodents, mainly because of the variation in predation risk between open and canopy microsites. Most of the current studies have mainly focused on the spatial variation in canopy openness within a forest or on comparisons among forests; however, the question of how variation in canopy openness at the individual tree scale affects seed-rodent interaction has received little attention, although tree-to-tree variation in canopy openness is ubiquitous. In this study, we measured the individual canopy openness of 45 trees belonging to three species in a subtropical forest, and compared seed dispersal and predation by rodents under the selected trees by labeling and tracking 4,500 seeds. Our results showed that canopy openness differed among individual trees both within and across species. More importantly, our results proved that individual tree variation in canopy openness significantly affected seed dispersal and predation by rodents, although not all species followed a consistent pattern. Seeds under trees with larger canopy openness were more likely to be removed rather than eaten in situ and dispersed farther. Our study highlights the pattern that individual tree characteristics (e.g., canopy openness) have profound effects on rodent-mediated seed dispersal services, which may further lead to tree-to-tree variation in seed fate and seedling regeneration. Our results also provide important implications for forest conservation and management: crown pruning can promote seed dispersal by rodents and natural seedling regeneration.

Multiple Anthropogenic Pressures Lead to Seed Dispersal Collapse of the Southernmost Palm Jubaea chilensis

Seed dispersal is a critical process for plant reproduction and regeneration. Successful recruitment depends on pre- and post-dispersal processes that complete a seed’s journey until becoming a new plant. However, anthropogenic stressors may disrupt the seed dispersal process at some stages, collapsing plant regeneration and hampering its long-term persistence. The Chilean palm tree Jubaea chilensis is the southernmost and the only non-tropical palm species, which currently relies on the scatter-hoarding rodent Octodon degus for seed dispersal. We assessed seed fate by measuring predation and dispersal rates through experimental fieldwork in the Palmar de Ocoa site (located within La Campana National Park) and the Palmar El Salto. We also used previous reports on seed harvest and seedling herbivory to depict the whole J. chilensis seed dispersal process and assess the relative importance of different anthropogenic pressures. We asked the following questions: (1) What is the effect of human harvesting on J. chilensis recruitment? (2) Do native and exotic rodents predate J. chilensis seeds in the same way? and (3) Does post-dispersal herbivory matter? We found that J. chilensis fruits are harvested for human consumption, reducing pre-dispersal available seeds by removing about 23 tons per season. Then, post-dispersal seeds at the Ocoa palm grove are heavily predated by exotic (Rattus rattus) and native (Octodon spp.) rodents; only 8.7% of the seeds are effectively dispersed by Octodon degus. At Palmar El Salto, 100% of the seeds were predated by Rattus rattus, precluding further analysis. Finally, 70% of the seedlings were consumed by exotic herbivores (mainly rabbits), resulting in a success rate of 1.81%. Only 7.9% of the surviving seedlings become infantile plants (4 year-old). Our assessment suggests that J. chilensis has aging populations with very few young individuals in disturbed sites to replace the old ones. For those reasons, we suggest increasing its conservation category to critically endangered as land-use change is rapidly fragmenting and shrinking the extant J. chilensis populations. We urge to take urgent actions to protect this relict palm, which otherwise may go extinct in the next decades.

Dual ecological functions of scatter-hoarding rodents: pollinators and seed dispersers of Mucuna sempervirens (Fabaceae).

Double mutualism, that is, pollination and seed dispersal of the same plant species mediated by the same animal partners, is important but remains elusive in nature. Recently, rodent species were found as key pollinators (i.e. explosive openers) for some Mucuna species in (sub)tropical Asia, but no evidence has shown whether and how these rodents could also act as legitimate seed dispersers via scatter-hoarding for those producing large seeds. Here, my aim was to test the hypothesis that scatter-hoarding rodents could act as double mutualists for both pollination and seed dispersal of the same Mucuna species, that is, Mucuna sempervirens (Fabaceae). Based on camera-trapping survey at 2 locations with or without squirrel presence in the Dujiangyan subtropical forests, Southwest China, 7 mammals and birds were identified as explosive openers for M. sempervirens flowers, but Leopoldamys edwardsi (rats) and Paguma larvata (civets) were the main pollinators at the squirrel-absent site, while Callosciurus erythraeus (squirrels) were the main pollinators at the squirrel-present site. By tracking the fate of individually-tagged seeds over 5 years at each site, I provide the first evidence for seed-eating rodents as legitimate seed dispersers via scatter-hoarding of seeds in this world-wide plant genus, although dispersal services were slightly reduced at squirrel-absent site. More importantly, the dual roles of scatter-hoarding rodents as key pollinators and seed dispersers for the same Mucuna species have shown a clear relationship of double mutualism, and their key services may be essential for population conservation of these Mucuna species in human-disturbed landscapes.

High-valued seeds are remembered better: evidence for item-based spatial memory of scatter-hoarding rodents

Episodic memory of scatter-hoarding animals involves encoding and storage of memories of cached food items, in conjunction with subsequent retrieval or recovery. Although the reward values mediate the interaction of item memory and source memory, whether nonhuman animals divide their spatial memory resources between cached items of different values has never been tested. Here, we used a unique scatter-hoarder/seed system to test our ‘cache value hypothesis’, which proposes that scatter-hoarding animals will preferentially allocate spatial memory resources towards higher-valued caches. By making Edwards's long-tailed rats, Leopoldamys edwardsi , anosmic, using Triton X-100, we showed that L. edwardsi recovered more caches containing large nuts than those containing small ones, although the two kinds of nuts were equivalently cached. Our results therefore support the hypothesis that scatter-hoarding animals allocate more spatial memory resources to caches containing high-valued items. This is one of the few studies to investigate how item memory regulates source memory (order information) in the context of food storing and recovery by animals, especially by scatter-hoarding rodents. That high-valued items were remembered better than low-valued ones in our study suggests that item memory appears to be contextually associated with order information of items in animal memory processes, which is not in agreement with a previous suggestion that order information is independent of content or item information. • We used a scatter-hoarding rodent to test episodic memory. • Edward's long-tailed rats allocated more memory on high-valued caches. • High-valued items were remembered better than low-valued ones. • The rats know ‘what food’ was cached ‘where’ or ‘when’.

Pilfering of western juniper seed caches by scatter-hoarding rodents varies by microsite and canopy type.

Scatter-hoarding rodents store seeds throughout their home ranges in superficially buried caches which, unlike seeds larder-hoarded in burrows, are difficult to defend. Cached seeds are often pilfered by other scatter-hoarders and either re-cached, eaten or larder-hoarded. Such seed movements can influence seedling recruitment, because only seeds remaining in caches are likely to germinate. Although the importance of scatter-hoarding rodents in the dispersal of western juniper seeds has recently been revealed, the level of pilfering that occurs after initial burial is unknown. Seed traits, soil moisture, and substrate can influence pilfering processes, but less is known about how pilfering varies among caches placed in open versus canopy microsites, or how cache discovery and removal varies among different canopy-types, tree versus shrub. We compared the removal of artificial caches between open and canopy microsites and between tree and shrub canopies at two sites in northeastern California during late spring and fall. We also used trail cameras at one site to monitor artificial cache removal, identify potential pilferers, and illuminate microsite use by scatter-hoarders. Removal of artificial caches was faster in open microsites at both sites during both seasons, and more caches were removed from shrub than tree canopies. California kangaroo rats were the species observed most on cameras, foraging most often in open microsites, which could explain the observed pilfering patterns. This is the first study to document pilfering of western juniper seeds, providing further evidence of the importance of scatter-hoarding rodent foraging behavior in understanding seedling recruitment processes in juniper woodlands.

The intermediate dispersal hypothesis: seed dispersal is maximized in areas with intermediate usage by hoarders

Seed dispersal and predation are paramount for tropical plant diversity. When encountered by scatter-hoarding frugivores, seeds can be either eaten, dispersed or ignored. But even after dispersal, seed caches are still subjected to predation. Many factors are known to influence these dynamics; however, how frequently hoarders use certain patches has seldom been related to cache predation rates. We used the interaction between agoutis (Dasyprocta leporina), a scatter-hoarding rodent, and Joannesia princeps, a tropical tree, as a model to investigate how the number of visits by hoarders in certain areas influences cache predation and seed fate. Camera-traps were used for 30 days in twenty different locations in Tijuca National Park to assess number of visits by agoutis. Thereafter, we placed seed piles on the same areas and determined their fate using the spool-and-line method to track seeds for over one hundred days. We found a non-linear relationship between how often an area is used by hoarders and the final proportion of dispersed seeds. At areas with a low number of visits, proportion of dispersed seeds was low due to low removal. As frequency of visits by hoarders increased, seed removal and the number of dispersal events increased but so did cache predation. Thus, in areas intensively used by hoarders, high cache predation resulted in a low number of dispersed seeds that remained alive in caches. As a result, dispersal was maximized in areas with intermediate use by scatter-hoarders, where there was a balance between primary seed dispersal and cache predation.