Zhishu Xiao

The effects of seed abundance on seed predation and dispersal by rodents in Castanopsis fargesii (Fagaceae)

Based on the animal dispersal hypothesis and the predator satiation hypothesis, we examined the effects of seed abundance at both population (i.e., mast seeding) and community levels on seed predation and dispersal of Castanopsis fargesii (Fagaceae), a rodent-dispersed mast species in Eastern Asia. In a subtropical evergreen broadleaved forest in the Dujiangyan region of Sichuan Province, China, individual seeds with coded tin tags were tracked in two contrasting stands (seed-poor and seed-rich) over two years (2000, a low-seed year; 2001, a high-seed year). Our results showed that: (1) small rodents did not harvest the tagged seeds of C. fargesii more rapid in the high-seed year than in the low-seed year in either stand. But, seed harvest was significantly faster in the seed-rich stand than in the seed-poor stand. (2) The removal proportion was significantly lower in the high-seed year than in the low-seed year for either stand, but the removal proportion was slightly higher in the seed-poor stand than in the seed-poor stand. This indicates that high seed abundance decreases seed removal (predator satiation hypothesis). (3) There were only small differences about seed caching, seed survival and seedling establishment of C. fargesii between years and stands. During the survey, no cached seeds survived to geminate in the spring for both stands and years. (4) Mean dispersal distances of the cached seeds are much shorter in the high-seed year (3.1 m) than in the low-seed year (8.1 m) in the seed-rich stand, though similar trend is not examined in the seed-poor stand. Our results indicate that seed predation and dispersal of C. fargesii are influenced by both mast seeding and community-level seed abundance, which is not completely consistent with either the animal dispersal hypothesis or the predator satiation hypothesis, but seems more related to the predator satiation hypothesis.

Testing the high-tannin hypothesis with scatter-hoarding rodents: experimental and field evidence

With a combination of both experimental (caged, hours/daily) and field (free-ranging, several months) studies, we tested the high-tannin hypothesis that hoarding animals prefer to eat more low-tannin food items immediately but hoard more high-tannin items for later consumption. We studied two common rat species (Edwards long-tailed rat, Leopoldamys edwardsi; and chestnut rat, Niviventer fulvescens) and two nut species (Henrys chestnut, Castanea henryi; and cork oak, Quercus variabilis) that show varying tannin levels (0.6% versus 11.7%) but are similar in other traits. Based on the high-tannin hypothesis, we predicted that (1) both rat species would eat more low-tannin C. henryi nuts instantly but fewer high-tannin Q. variabilis nuts and (2) after harvesting a given nut, they would prefer to hoard more Q. variabilis nuts and fewer C. henryi nuts. The first prediction was firmly supported in our study: both rat species ate more C. henryi nuts than Q. variabilis nuts under all conditions. However, the second prediction was supported only in the field study, which lasted over several months, in contrast to the experiments conducted in seminatural enclosures (only 1 day). We found that high-tannin Q. variabilis nuts, in contrast to low-tannin C. henryi nuts, had a significantly higher probability of being hoarded and surviving as seedlings in the field. We conclude that experimental conditions used here are less likely to result in natural feeding preferences of tested animals and the high-tannin hypothesis is supported especially in the field setting.

Hoarding decisions by Edward's long-tailed rats (Leopoldamys edwardsi) and South China field mice (Apodemus draco): The responses to seed size and germination schedule in acorns

Co-varying traits in acorns such as seed size and germination schedule are important to influence the behavioural decisions of hoarding rodents. Using acorn pairs from cork oak (Quercus variabilis) (large size and short germination schedules) serrate oak (Q. serrata) (small size and short germination schedule) and qinggang (Cyclobalanopsis glauca) (small size and long germination schedule) with contrasting seed size and germination schedule, we conducted a series of experiments to investigate hoarding preferences in response to seed size and germination schedule by Edwards long-tailed rats (Leopoldamys edwardsi) and South China field mice (Apodemus draco) in semi-natural enclosures. We found that the seed size hypothesis was consistently supported: both rodent species ate more small acorns but hoarded more large ones regardless of germination schedules. However, the germination schedule hypothesis was also supported when similar sized acorns were simultaneously provided, e.g. Q. serrata versus C. glauca or germinating versus non-germinating Q. variabilis. Our results, contrary to the studies from North America, indicate that seed size is more important than germination schedules in determining whether the tested animals eat or hoard a given seed.

Long‐term seed survival and dispersal dynamics in a rodent‐dispersed tree: testing the predator satiation hypothesis and the predator dispersal hypothesis

Summary 1. Mast seeding in animal-dispersed plants has previously been accounted for by two main hypotheses: the predator satiation hypothesis (that it increases seed survival and establishment before dispersal) and the predator dispersal hypothesis (that it increases seed dispersal or dispersal distance). However, neither hypothesis has been rigorously tested with simultaneous data on seed production, seed predation and seed dispersal by vertebrate seed predators. 2. We studied oil tea Camellia oleifera (Theaceae) seed production for eight years (2002–2009) in a subtropical forest in south-west China, and investigated how annual seed and rodent abundance determined per capita seed availability for rodent seed predators and seed dispersers and how seed and rodent abundance were related to seed dispersal and seed survival via scatter-hoarding. We predicted the patterns of seed dispersal and survival to test the two hypotheses about mast seeding. Edward’s long-tailed rat Leopoldamys edwardsi acted as the principal seed disperser of oil tea seeds because of scatter-hoarding, while other sympatric rodent species acted only as seed predators. 3. We first provided a reasonable method to estimate per capita seed availability based on annual seed abundance and annual metabolic rodent abundance (corrected for metabolic-scaling body mass of each rodent species). We found that annual seed abundance, annual metabolic rodent abundance and per capita seed availability all had some significant effects on different estimators of seed fates (including dispersal distances) across each stage from seedfall to seedling establishment. Both annual seed abundance and per capita seed availability were positively correlated with pre-dispersal seed survival, but negatively correlated with scatter-hoarding (and recaching), seed survival after dispersal and dispersal distances. However, annual metabolic rodent abundance had a positive effect on scatter-hoarding, but had a negative effect on the time to cache recovery. 4. Synthesis. Since greater seed production was associated with improvement in pre-dispersal survival of oil tea seeds but a reduction in dispersal (including secondary dispersal and dispersal distance), our long-term study indicates that, compared with the predator dispersal hypothesis, the predator satiation hypothesis provides a better mechanism predicting seed dispersal and seed survival in animal-dispersed plants by integrating seed abundance and animal abundance.

High regeneration capacity helps tropical seeds to counter rodent predation

Rapid germination of non-dormant seeds is one adaptation plants have evolved to counter seed predation by rodents. Some rodent species have evolved behaviors that prevent or slow the seed germination process through seed embryo removal or seed pruning; however, no plant species is known to have successfully escaped embryo removal or seed pruning by rodents. Here, we report that the non-dormant seeds of Pittosporopsis kerrii Craib in tropical rain forests in China have a high regeneration capacity to counter seed pruning by rodents. We found seed pruning, instead of embryo removal, was commonly used by rodents to increase food storage time by slowing down the seed germination process, but that P. kerrii seeds have a high regeneration capacity to escape seed predation by rodents: all pruned seeds, pruned roots and embryo-removed seeds by rodents or people retain the ability to develop into seedlings. Seeds of P. kerrii also have other capacities (i.e. rapid seed decomposition and indigestible dormant taproots) to escape predation by reducing the plant’s attractiveness to rodents. The association between seed pruning behavior in rodents and high regeneration capacity of pruned seeds or roots in P. kerrii seeds are likely novel adaptation strategies adopted by seeds and rodents, respectively.

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.

Trait-mediated seed predation, dispersal and survival among frugivore-dispersed plants in a fragmented subtropical forest, Southwest China

By tracking the fate of individual seeds from 6 frugivore-dispersed plants with contrasting seed traits in a fragmented subtropical forest in Southwest China, we explored how rodent seed predation and hoarding were influenced by seed traits such as seed size, seed coat hardness and seed profitability. Post-dispersal seed fates varied significantly among the 6 seed species and 3 patterns were witnessed: large-seeded species with a hard seed coat (i.e. Choerospoadias axillaries and Diospyros kaki var. silvestris) had more seeds removed, cached and then surviving at caches, and they also had fewer seeds predated but a higher proportion of seeds surviving at the source; medium-sized species with higher profitability and thinner seed coat (i.e. Phoebe zhennan and Padus braohypoda) were first harvested and had the lowest probability of seeds surviving either at the source or at caches due to higher predation before or after removal; and small-seeded species with lower profitability (i.e. Elaeocarpus japonicas and Cornus controversa) had the highest probability of seeds surviving at the source but the lowest probability of seeds surviving at caches due to lower predation at the source and lower hoarding at caches. Our study indicates that patterns of seed predation, dispersal and survival among frugivore-dispersed plants are highly determined by seed traits such as seed size, seed defense and seed profitability due to selective predation and hoarding by seed-eating rodents. Therefore, trait-mediated seed predation, dispersal and survival via seed-eating rodents can largely affect population and community dynamics of frugivore-dispersed plants in fragmented forests.

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.

Scatter-hoarding rodents as secondary seed dispersers of a frugivore-dispersed tree Scleropyrum wallichianum in a defaunated Xishuangbanna tropical forest, China

Local extinction or population decline of large frugivorous vertebrates as primary seed dispersers, caused by human disturbance and habitat change, might lead to dispersal limitation of many large-seeded fruit trees. However, it is not known whether or not scatter-hoarding rodents as secondary seed dispersers can help maintain natural regeneration (e.g. seed dispersal) of these frugivore-dispersed trees in the face of the functional reduction or loss of primary seed dispersers. In the present study, we investigated how scatter-hoarding rodents affect the fate of tagged seeds of a large-seeded fruit tree (Scleropyrum wallichianum Arnott, 1838, Santalaceae) from seed fall to seedling establishment in a heavily defaunated tropical forest in the Xishuangbanna region of Yunnan Province, in southwest China, in 2007 and 2008. Our results show that: (i) rodents removed nearly all S. wallichianum seeds in both years; (ii) a large proportion (2007, 75%; 2008, 67.5%) of the tagged seeds were cached individually in the surface soil or under leaf litters; (iii) dispersal distance of primary caches was further in 2007 (19.6 ± 14.6 m) than that in 2008 (14.1 ± 11.6 m), and distance increased as rodents recovered and moved seeds from primary caches into subsequent caching sites; and (iv) part of the cached seeds (2007, 3.2%; 2008, 2%) survived to the seedling stage each year. Our study suggests that by taking roles of both primary and secondary seed dispersers, scatter-hoarding rodents can play a significant role in maintaining seedling establishment of S. wallichianum, and are able to at least partly compensate for the loss of large frugivorous vertebrates in seed dispersal.

The combined effects of seed perishability and seed size on hoarding decisions by Pére David’s rock squirrels

The food perishability hypothesis reasons that the perishability of nondormant acorns through rapid germination is the primary determinant of hoarding decisions (e.g., embryo removal in nondormant acorns in particular) by scatter-hoarding squirrels. However, we do not know whether seed size and its interactions with seed germination schedule affect squirrel’s hoarding decisions. By presenting pairs of acorns with contrasting germination/dormancy conditions and seed size, we investigated the relative importance of each target trait in determining the hoarding decisions of free-ranging Pére David’s rock squirrel (Sciurotamias davidianus) in Central China. Consistent with the food perishability hypothesis, the squirrels were highly sensitive to subtle differences of acorn germination status either within nondormant acorns or between nondormant and dormant acorns. Though there were no significant differences in seed hoarding and dispersal distance, the embryo-removal probability of nondormant acorns (especially those germinated) was much higher than that of dormant acorns prior to hoarding. Our results also support the seed size hypothesis. Large acorns were often hoarded more and moved farther than small acorns, and large nondormant acorns also had a higher probability of having their embryos removed. Moreover, the interactions between seed size and seed germination schedule had a large effect on whether a given acorn was hoarded or hoarded with its embryo removed. Our study indicates that the combined effects from seed germination schedule and seed size have the potential to determine hoarding decisions of scatter-hoarding squirrels.