Hongmao Zhang

Effects of seed abundance on seed scatter-hoarding of Edward’s rat (Leopoldamys edwardsi Muridae) at the individual level

Mast seeding is a common phenomenon, and has important effects on seed dispersal and hoarding by animals. At population level, the predator satiation hypothesis proposes that the satiating effect of a large amount of seeds on a relatively small number of predators benefits seed survival in mast-seeding years. However, the effect of mast seeding on the scatter-hoarding of rodents at the individual level is largely unknown. In this study, we investigated the effects of seed abundance (by simulating mast seeding and non-mast seeding) on the removal, consumption and scatter-hoarding of seeds of Camellia oleifera (Theaceae) by Edward’s rat Leopoldamys edwardsi (Muridae) in seminatural enclosures in southwest China. We wanted to test the masting-enhanced hoarding hypothesis, which suggests that rodents tend to scatter-hoard more seeds in mast-seeding years in order to occupy more food resources. Our results indicate that L. edwardsi tended to disperse and scatter-hoard more seeds of C. oleifera per night with increasing seed abundance, and to eat less seeds per night when there was a high level of seed abundance in the enclosure experiments. These results support the masting-enhanced hoarding hypothesis. This capacity of rodents may be an evolutionary adaptation to the mast-seeding phenomenon. Our results suggest that mast seeding benefits forest regeneration not only through the predator satiation effect at the population level, but also through increased hoarding by animals at the individual level.

Trade-off between seed defensive traits and impacts on interaction patterns between seeds and rodents in forest ecosystems

Plants often have two kinds of defensive traits against animal predation: physical and chemical defenses, but the trade-off between them is heavily debated, and their impacts on relationship between plants and animals are largely unknown. We investigated seed traits of 23 tree species and their impacts on seed fates or hoarding behaviors under predation from 16 rodent species in four forest types in China. We provide clear evidence that there is a strong nonlinear trade-off between physical (as measured by seed coat thickness) and chemical (as measured by tannin content) defensive traits in seeds. This trade-off was closely associated with nutritional traits, resulting in coordinated defense syndromes in seeds. The seed fate and hoarding behavior patterns were largely determined by the trade-off-related seed traits and the body mass of rodents, respectively, not by the phylogenetic relations of species. Tree species showed more conservative evolution in seed traits of high starch content, high tannin content, and thin seed coat, but they showed more convergent/divergent evolution in seed traits of high protein content, high fat content, and thick seed coat under rodent predation. Our results suggest that trade-off-related seed traits may play a predominant role in shaping the relationship between plants and animals.

Responses of seed-hoarding behaviour to conspecific audiences in scatter- and/or larder-hoarding rodents

In rodents, the presence of conspecifics may trigger changes in food-hoarding behaviour when the risk of pilferage is perceived to be high. It is not clear how hoarding intensity and hoarding patterns (scatter- or larder-hoarding) of rodents change in the presence of conspecific audiences or if the nature of the change is different between sexes, or influenced by body size. We investigated these questions in Korean field mice (Apodemus peninsulae) (KFM, showing both scatter- and larder-hoarding behaviours) and Chinese white-bellied rats (Niviventer confucianus) (CWBR, showing larder-hoarding behaviours only) through carefully controlled experiments in outdoor enclosures. We observed the seed-hoarding behaviour of focal females and males of each species in the presence of a conspecific audience of the opposite sex, same sex, and alone (control treatment). We found both rodent species increased hoarding efforts when faced with an increased pilferage risk (presence of audiences), supporting the pilferage tolerance hypotheses or forage competition hypotheses. In contrast with previous studies, we found potential pilferage risk can result in a KFM shift from scatterhoarding to larder-hoarding, supporting the larder defence hypotheses, not the catastrophic avoidance hypotheses. However, the relationship between hoarding patterns, and body size or sex, is rather complex and requires further investigation.

Cultivated walnut trees showed earlier but not final advantage over its wild relatives in competing for seed dispersers.

Little is known about seeding regeneration of cultivated trees compared to wild relatives in areas where seed dispersers are shared. Here, we investigated the differences in seed fates of cultivated walnut (Juglans regia) and wild Manchurian walnut (Juglans mandshurica) trees under rodent predation and dispersal. J. regia seeds have higher nutritional value (large size, mass and kernel mass) and lower mechanical defensiveness (thin endocarp) than J. mandshurica seeds. We tracked seeds of J. regia and J. mandshurica under both enclosure and field conditions to assess differences in competing for seed dispersers of the two co-occurring tree species of the same genus. We found that rodents preferred to harvest, eat and scatter-hoard seeds of J. regia as compared to those of J. mandshurica. Seeds of J. regia were removed and scatter-hoarded faster than those of J. mandshurica. Caches of J. regia were more likely to be rediscovered by rodents than those of J. mandshurica. These results suggest that J. regia showed earlier dispersal fitness but not the ultimate dispersal fitness over J. mandshurica in seeding regeneration under rodent mediation, implying that J. regia has little effect on seeding regeneration of J. mandshurica in the field. The effects of seed traits on seed dispersal fitness may vary at different dispersal stages under animal mediation.

Rodent-favored cache sites do not favor seedling establishment of shade-intolerant wild apricot (Prunus armeniaca Linn.) in northern China

Seed dispersal by scatter hoarders is widely assumed to involve directed dispersal, in which microhabitats selected for caching also benefit seedling establishment and growth. However, in many systems, this may not be true if animal-favored cache sites do not match the safe sites for plants, or if cache sites benefit the plant in one life stage and not another. Here, we investigated whether cache sites selected by rodents are favorable for seedling establishment and growth of shade-intolerant wild apricot (Prunus armeniaca Linn.) in northern China. We tracked tagged seeds and compared the germination and growth of seedlings from rodent-cached seeds with that of naturally established seedlings in a secondary forest and shrubland stand. Rodents preferred to cache seeds under shrubs with medium canopy cover (31–60xa0%) in litter substrate in the secondary forest, and under shrubs with high canopy cover (>60xa0%) in soil or litter substrate in the shrubland stand, neither of which conveyed an advantage for seedling establishment. Although fewer caches were made along shrub edges, or under low canopy cover (≤30xa0%) in the secondary forest, or along shrub edges, open areas of grass, or under low canopy cover in the shrubland stand, these cache sites consistently contributed to higher survival rates. The microhabitats of grass, soil, or low canopy cover significantly promoted the emergence, survival, and growth of naturally established seedlings. Our results are best explained by the conflicting demands of rodents for caching seeds in more secure sites and P. armeniaca’s high-light requirements for seedling recruitment. We argue that the relationship between favored cache sites for seed hoarders and safe sites for plants will often not match but may still allow a reasonable rate of establishment and regeneration.

Rapid sequestration and recaching by a scatter-hoarding rodent (Sciurotamias davidianus)

Abstract Many seed-hoarding species are faced with ephemeral pulses of seeds that result in competition at seed sources and the need to minimize hoarding time during the limited time seeds are available. Here we tested the hypothesis that a seed-hoarding species (Père Davids rock squirrel [Sciurotamias davidianus]) rapidly scatter hoards seeds near seed sources to maximize harvest rate, and then subsequently recaches seeds to further reduce cache losses. We tracked the caches of wild walnut (Juglans mandshurica) scatter hoarded by S. davidianus, the exclusive dispersal agent of this highly preferred nut species. We followed dispersed nuts in both the field and in a large enclosure in a manner that allowed us to follow patterns of recaching through the scatter-hoarding process. In the field, S. davidianus initially cached close to nut sources and then subsequently recached nuts on multiple occasions progressively farther from sources, always in the same direction, at lower densities, and at sites with more vegetative cover (e.g., under shrubs). In enclosures, each of 6 squirrels first cached nuts closer to the nut source on the 1st day of observation, and then subsequently recached nuts closer to the nest, sometimes at decreasing densities. We suggest that, in addition to pilferage risk, cache spacing by S. davidianus may be influenced by the potential for competition at the seed source and proximity to the burrow or the core of the home range, and that caches might be managed to accommodate all of these factors. Future studies should consider how such recaching behavior influences patterns of cache recovery, the ultimate distribution of dispersed nuts, and seed fates.

Effects of interspecific competition on food hoarding and pilferage in two sympatric rodents

Food hoarding and pilferage in rodents may be regulated by intense competition between sympatric species that have similar habitats, diets and activity, but studies exploring this remain rare. Here, we used semi-natural enclosures to investigate food-hoarding and cache pilferage interactions between sympatric Korean field mice (KFM) (Apodemus peninsulae) and Chinese white-bellied rats (CWR) (Niviventer confucianus). KFM and CWR have similar diets, habitat and nocturnal activity, but the smaller KFM larder and scatter hoards and larger CWR larder hoard only. We found that KFM harvest, larder-hoard and eat seeds at a greater intensity when CWR are present as an audience (present but cannot pilfer). KFM ate 11.5%, re-larder-hoarded 17.9% and re-scatter-hoarded 1.3% of their scatter-hoarded seeds, and ate 29.3% of their larder-hoarded seeds when CWR were present as pilferers. A total of 12.8% of the seeds scatter-hoarded and 50% of seeds directly put on the ground by KFM were pilfered by CWR. CWR did not alter hoarding intensity in the presence of KFM and their stores cannot be pilfered by KFM. These results indicate that large-sized rodent species (more dominant) significantly increase the hoarding intensity of small-sized species and show a unidirectional pilferage of seeds cached by small-sized species. The behavioural differences between these two species may reduce competition for resources and promote coexistence between sympatric rodents.

Seed trait-mediated selection by rodents affects mutualistic interactions and seedling recruitment of co-occurring tree species.

As mutualists, seed dispersers may significantly affect mutualistic interactions and seedling recruitment of sympatric plants that share similar seed dispersers, but studies are rare. Here, we compared seed dispersal fitness in two co-occurring plant species (Armeniaca sibirica and Amygdalus davidiana) that inhabit warm temperate deciduous forest in northern China. We tested the hypothesis that seed trait-mediated selection by rodents may influence mutualistic interactions with rodents and then seedling establishment of co-occurring plant species. A.xa0davidiana seeds are larger and harder (thick endocarps) than A.xa0sibirica seeds, but they have similar levels of nutrients (crude fat, crude protein), caloric value and tannin. More A.xa0sibirica seedlings are found in the field. Semi-natural enclosure tests indicated that the two seed species were both harvested by the same six rodent species, but that A.xa0sibirica had mutualistic interactions (scatter hoarding) with four rodent species (Apodemus peninsulae, A. agrarius, Sciurotamias davidianus, Tamias sibiricus), and A.xa0davidiana with only one (S. davidianus). Tagged seed dispersal experiments in the field indicated that more A.xa0sibirica seeds were scatter-hoarded by rodents, and more A.xa0sibirica seeds survived to the next spring and became seedlings. A.xa0sibirica seeds derive more benefit from seed dispersal by rodents than A.xa0davidiana seeds, particularly in years with limited seed dispersers, which well explained the higher seedling recruitment of A.xa0sibirica compared with that of A.xa0davidiana under natural conditions. Our results suggest that seed dispersers may play a significant role in seedling recruitment and indirect competition between co-occurring plant species.

Mutualistic and predatory interactions are driven by rodent body size and seed traits in a rodent–seed system in warm-temperate forest in northern China

Abstract Context. Mutualistic interactions between animals and plants shape the structure of plant–animal systems and, subsequently, affect plant-community structure and regeneration. Aims. To assess the effects of plant and rodent functional traits on the formation of mutualistic and predatory interactions regarding seed dispersal and predation in a warm-temperate forest. Methods. Seed scatter-hoarding and predation by six sympatric rodent species on seeds belonging to five sympatric tree species were tested under enclosure conditions. Key results. Functional traits (i.e. rodent body size and seed traits) are important to mutualism/predation in this seed–rodent system. The rodent–seed network is highly nested: large-sized rodents have mutualistic or predatory interactions with both large- and small-sized seed species, but small-sized rodents interacted with small-sized seed species only. Large seeds or seeds with hard coats enhanced mutualism and reduced predation. Conclusion. Body size of rodents and seed traits such as handling time and nutritional value are key factors in the formation of mutualistic and predatory interactions within seed–rodent systems. Implications. To promote seedling establishment in degenerated forests, introducing or protecting large-sized scatter hoarders and reducing the density of pure seed eaters are needed.

Hoarding without reward: Rodent responses to repeated episodes of complete cache loss

For food-hoarding strategies to be maintained in a population, the benefits of hoarding must outweigh the costs. If rewards are too low to offset the costs of hoarding, hoarders might be expected to abandon hoarding and/or shift to an alternative storing strategy (e.g., increase food consumption). However the ability to adjust to such circumstances requires that animals anticipate long-term rewards and adjust storing strategies to modify future outcomes. To test this, we subjected three sympatric food-hoarding species (the Korean field mouse, Apodemus peninsulae, both a scatter and larder hoarder; the Chinese white-bellied rat, Niviventer confucianus, only a larder hoarder; and Père Davids rock squirrel, Sciurotamias davidianus, predominantly a scatter hoarder) to repeated episodes of complete cache loss over nine sequential trials in semi-natural enclosures. Although these species increased harvest and consumption rates throughout the experiment, none of these three species ceased hoarding under these conditions. The variation in responses observed across species and gender suggest some degree of behavioural plasticity to compensate for such extreme losses, but a general inability to abandon hoarding or shift to an alternative strategy. Future studies should consider how such responses correspond to natural patterns of intensive pilferage in the field.