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.sempervirensflowers,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 thefirst 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.

Does scatter-hoarding of seeds benefit cache owners or pilferers?

The scatter-hoarding behavior of granivorous rodents plays an important role in seed dispersal and seedling re­generation of trees,as well as the evolution of several well-known mutualisms between trees and rodents in for­est ecosystems.Because it is difficult to identify seed hoarders and pilferers under field conditions by traditional methods,the full costs incurred and benefits accrued by scatter-hoarding have not been fully evaluated in most systems.By using infrared radiation camera tracking and seed tagging,we investigated the benefits and losses of scatter-hoarded seeds(Camellia oleifera)for 3 sympatric rodent species(Apodemus draco,Niviventer confu­cianus and Leopoldamys edwardsi)in a subtropical forest of Southwest China during 2013 to 2015.We estab­lished the relationships between the rodents and the seeds at the individual level.For each rodent species,we calculated the cache recovery rate of cache owners,as well as conspecific and interspecific pilferage rates.We found that all 3 sympatric rodent species had a cache recovery advantage with rates that far exceeded average pilferage rates over a 30-day tracking period.The smallest species(A.draco)showed the highest rate of scat­ter-hoarding and the highest recovery advantage compared with the other 2 larger species(N.confucianus and L.edwardsi).Our results suggest that scatter-hoarding benefits cache owners in food competition,supporting the pilferage avoidance hypothesis.Therefore,scatter-hoarding behavior should be favored by natural selection,and plays a significant role in species coexistence of rodent community and in the formation of mutualism between seeds and rodents in forest ecosystems.

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 hu-man 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 south-west 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.

Mechanisms underlying detection of seed dormancy by a scatter-hoarding rodent

The mechanism underlying detection of seed dormancy by scatter-hoarding rodents is unclear,although previous work suggests that the pericarp plays an important role in signaling dormancy status.Eastern gray squirrels(Sciurus carolinensis)consume early germinating seeds as they are more likely to perish immediately,whereas dormant seeds tend to be cached.To examine the mechanisms underlying dormancy detection,we characterized physical and chemical differences between germinating and dormant pericarps of northern red oak(Quercus rubra),American chestnut(Castanea dentata)and the BC3 hybrid of Chinese chestnut and American chestnut(Castanea mollissima×C.dentata)using scanning electron microscopy and gas chromatography-mass spectrometry.We found that,as seeds break dormancy,the wax layer on the pericarp degrades and is accompanied by the escape of lower molecular weight kernel compounds or lipid metabolism byproducts.Our field experiments showed that squirrels were 4-8 times more likely to consume seeds that were altered to remove pericarp wax coating or that were sprayed with seed chemicals.We argue that dormancy detection by scatter-hoarding rodents is a complex process involving physical cues such as loss of pericarp wax and chemical cues such as emission of olfactory cues.

Olfaction alters spatial memory strategy of scatter-hoarding animals

Although it has been suggested that olfaction is closely interconnected with hippocampal systems,whether olfaction regulates spatial memory strategy remains never known.Furthermore,no study has examined how olfaction mediates spatial memory established on the external objects,for example,caches made by scatter-hoarding animals.Here,we experimentally induced nondestructive and reversible olfaction loss of a scatter-hoarding animal Leopoldamys edwardsi,to test whether and how olfaction regulates spatial memory to mediate cache recovery and pilferage.Our results showed that the normal L.edwardsi preferred to pilfer caches of others rather than to recover their own using accurate spatial memory(35.7%vs.18.6%).Anosmic L.edwardsi preferred to recover the caches they made prior to olfaction loss rather than to pilfer from others relied on spatial memory(54.2%vs.36.0%).However,L.edwardsi with anosmia showed no preference either to the caches they established after olfaction loss or caches made by others(25.8%vs.29.1%).These collectively indicate that olfaction loss has a potential to affect new memory formation but not previously established spatial memory on caches.Our study first showed that olfaction modified spatial memory strategy in cache recovery and pilferage behaviors of scatter-hoarding animals.We suggest that future studies pay more attention to the evolution of olfaction and its relationship with spatial memory strategy.

Seed value influences cache pilfering rates by desert rodents

Some rodents gather and store seeds.How many seeds they gather and how they treat those seeds is largely determined by seed traits such as mass,nutrient content,hardness of the seed coat,presence of secondary compounds,and germination schedule.Through their consumption and dispersal of seeds,rodents act as agents of natural selection on seed traits,and those traits influence how rodents forage.Many seeds that are scatter-hoarded by rodents are pilfered,or stolen,by other rodents,and seed traits also likely influence pilfering rates and seed fates of pilfered seeds.To clarify coevolutionary relationships between rodents and the plants that they disperse,one needs to understand the role of seed traits in rodent foraging decisions.We compared how the seeds of 4 species of plants that are dispersed by scatter-hoarding animals and that differ in value(singleleaf piñon pine,Pinus monophylla;desert peach,Prunus andersonii;antelope bitterbrush,Purshia tridentata;Utah juniper,Juniperus osteosperma)were pilfered and recached by rodents.One hundred artificial caches of the 4 seed species(25 per species)were prepared,and removal by rodents was monitored.Rodents pilfered high-value seeds more rapidly than the other seeds.Desert peach seeds,which contain toxic secondary compounds,were more frequently recached.Relatively low value seeds like Utah juniper and antelope bitterbrush were pil-fered more slowly and were sometimes left at cache sites,and seeds of the latter species were transported shorter distances to new cache sites.The background density of seeds also appeared to influence the relative value of seeds.

Fluctuation in seed abundance has contrasting effects on the fate of seeds from two rapidly germinating tree species in an Asian tropical forest

The seed predator satiation hypothesis states that high seed abundance can satiate seed predators or seed dispersers,thus promoting seed survival.However,for rapidly germinating seeds in tropical forests,high seed abundance may limit dispersal as the seeds usually remain under parent trees for long periods,which may lead to high mortality due to rodent predation or fungal infestations.By tracking 2 species of rapidly germinating seeds(Pittosporopsis kerrii,family Icacinaceae;Camellia kissi,family Theaceae),which depend on dispersal by scatter-hoarding rodents,we investigated the effects of seed abundance at the community level on predation and seed dispersal in the tropical forest of Xishuangbanna Prefecture,Southwest China.We found that high seed abundance at the community level was associated with delayed and reduced seed removal,decreased dispersal distance and increased pre-dispersal seed survival for both plant species.High seed abundance was also associated with reduced seed caching of C.kissi,but it showed little effect on seed caching of P.kerrii.However,post-dispersal seed survival for the 2 plant species followed the reverse pattern.High seed abundance in the community was associated with higher post-dispersal survival of P.kerrii seeds,but with lower post-dispersal survival of C.kissi seeds.Our results suggest that different plant species derive benefit from fluctuations in seed production in different ways.

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.

Palatability and profitability of co-occurring seeds alter indirect interactions among rodent-dispersed trees

Beyond direct species interactions,seed dispersal is potentially affected by indirect seed–seed interactions among co-occurring nut-bearing trees which are mediated by scatter-hoarding animals as shared seed dispersers.A relevant question in such systems is to what extent different functional traits related to food palatability and profitability affect the kinds of indirect interactions that occur among co-occurring seeds,and the consequences for seed dispersal.We used field experiments to track seed dispersal with individually tagged seeds in both monospecific and mixed seed communities.We measured indirect effects based on 3 seed–seed species pairs from the family Fagaceae with contrasting seed size,tannin level,and dormancy in a subtropical forest in Southwest China.When all else was equal,the presence of adjacently placed seeds with contrasting seed traits created different indirect effects measured through a variety of dispersal-related indicators.Apparent mutualism was reciprocal due to increasing seed dispersal in mixed seed patches with mixed differences in seed tannins and dormancy.However,differences in either seed size or dormancy in co-occurring adjacently placed seeds caused apparent competition with reduced seed removal or seed dispersal(distance)in at least one species.Our study supports the hypothesis that different functional traits related to food palatability and profitability in co-occurring seeds modify foraging decisions of scatter-hoarding animals,and subsequently cause indirect effects on seed dispersal among rodent-dispersed trees.We conclude that such indirect effects mediated by shared seed dispersers may act as an important determinant of seed dispersal for co-fruiting animal-dispersed trees in many natural forests.