Chromosome-level genome of Osmia excavata (Hymenoptera: Megachilidae) provides insights into low-temperature tolerance of Osmia pollinator.

The solitary bee Osmia excavata (Hymenoptera: Megachilidae) is a key pollinator managed on a large scale. It has been widely used for commercial pollination of fruit trees, vegetables, and other crops with high efficiency in increasing the crop seeding rate, yield, and seed quality in Northern hemisphere. Here, a high-quality chromosome-level genome of O. excavata was generated using PacBio sequencing along with Hi-C technology. The genome size was 207.02 Mb, of which 90.25% of assembled sequences were anchored to 16 chromosomes with a contig N50 of 9,485 kb. Approximately 186.83 Mb, accounting for 27.93% of the genome, was identified as repeat sequences. The genome comprises 12,259 protein-coding genes, 96.24% of which were functionally annotated. Comparative genomics analysis suggested that the common ancestor of O. excavata and Osmia bicornis (Hymenoptera: Megachilidae) lived 8.54 million years ago. Furthermore, cytochrome P450 family might be involved in the responses of O. excavata to low-temperature stress. Taken together, the chromosome-level genome assembly of O. excavata provides in-depth knowledge and will be a helpful resource for the pollination biology research.

Temporal niche partitioning among sympatric wild and domestic ungulates between warm and cold seasons.

The coexistence of sympatric species with similar ecological niches has been a central issue in ecology. Clarifying the daily activity patterns of sympatric wild ungulates can help understand their temporal niche differentiation and the mechanisms of coexistence, providing information for their conservation. The Baotianman National Nature Reserve in northern China is rich in wild ungulates, but little is known about the daily activity patterns of wild ungulates in the area, making it difficult to develop effective conservation strategies. We studied five representative wild ungulates (i.e. forest musk deer, Chinese goral, Reeve's muntjac, Siberian roe deer, and wild boar) of the region using camera-trapping data, focusing on the seasonal daily activity patterns and effects of seasonal grazing of domestic sheep, to reveal their coexistence based on temporal ecological niche differentiation. Comparative analyses of the seasonal daily activity showed that forest musk deer exhibited a single-peak activity in the warm season. Other ungulates exhibited multipeak activity. All five ungulates differed significantly in daily activity patterns. Notably, wild boar and Reeve's muntjac showed high overlap coefficients between the cold and warm seasons. In both cold and warm seasons, the five wild ungulates and domestic sheep displayed low overlap in their daily activity rhythms potentially indicating temporal ecological niche differentiation. The results suggest that temporal isolation might be a strategy for wild ungulates to avoid domestic sheep and reduce interspecific competition, and that temporal ecological niche differentiation potentially promoted the coexistence among the studied sympatric ungulates. This understanding may provide new insights for the development of targeted conservation strategies.

Stability and Assembly Mechanisms of Butterfly Communities across Environmental Gradients of a Subtropical Mountain.

Mountain ecosystems harbor evolutionarily unique and exceptionally rich biodiversity, particularly in insects. In this study, we characterized the diversity, community stability, and assembly mechanisms of butterflies on a subtropical mountain in the Chebaling National Nature Reserve, Guangdong Province, China, using grid-based monitoring across the entire region for two years. The results showed that species richness, abundance, and Faith's phylogenetic diversity decreased with increasing elevation; taxonomic diversity played a considerable role in mediating the effects of environmental changes on stability. Moreover, our results showed that stochastic processes are dominant in governing the assembly of butterfly communities across all elevational gradients, with habitats at an elevation of 416-580 m subjected to the strongest stochastic processes, whereas heterogeneous selection processes displayed stronger effects on the assembly of butterfly communities at 744-908 m, 580-744 m, and 908-1072 m, with abiotic factors inferred as the main driving forces. In addition, significant differences were detected between the barcode tree and the placement tree for the calculated ß-NTI values at 416-580 m. Overall, this study provides new insights into the effects of environmental change on the stability and assembly of butterflies in Chebaling, which will be beneficial for biodiversity conservation and policy development.

Disentangling spatiotemporal dynamics in metacommunities through a species-patch network approach.

Colonization and extinction at local and regional scales, and gains and losses of patches are important processes in the spatiotemporal dynamics of metacommunities. However, analytical challenges remain in quantifying such spatiotemporal dynamics when species extinction-colonization and patch gain and loss processes act simultaneously. Recent advances in network analysis show great potential in disentangling the roles of colonization, extinction, and patch dynamics in metacommunities. Here, we developed a species-patch network approach to quantify metacommunity dynamics including (i) temporal changes in network structure, and (ii) temporal beta diversity of species-patch links and its components that reflect species extinction-colonization and patch gain and loss. Application of the methods to simulated datasets demonstrated that the approach was informative about metacommunity assembly processes. Based on three empirical datasets, our species-patch network approach provided additional information about metacommunity dynamics through distinguishing the effects of species colonization and extinction at different scales from patch gains and losses and how specific environmental factors related to species-patch network structure. In conclusion, our species-patch network framework provides effective methods for monitoring and revealing long-term metacommunity dynamics by quantifying gains and losses of both species and patches under local and global environmental change.

Fine-Scale Interactions between Leopard Cats and Their Potential Prey with Contrasting Diel Activities in a Livestock-Dominated Nature Reserve.

Habitat use and the temporal activities of wildlife can be largely modified by livestock encroachment. Therefore, identifying the potential impacts of livestock on the predator-prey interactions could provide essential information for wildlife conservation and management. From May to October 2017, we used camera trapping technology to investigate fine-scale spatiotemporal interactions in a predator-prey system with the leopard cat (Prionailurus bengalensis) as a common mesopredator, and its prey with contrasting activity patterns (i.e., nocturnal rats and diurnal squirrels) in a livestock-dominated nature reserve in Northern China. We found that the prey species showed different habitat preferences with the leopard cats. The nocturnal rats had strong positive effects on the site-use of the leopard cats, while the influence of livestock on the diurnal squirrels' site-use changed from strong positive effects to weak effects as the livestock disturbance increased. The temporal overlap between the leopard cats and the nocturnal rats was almost four times that of the leopard cats and the diurnal squirrels, regardless of the livestock disturbance. Our study demonstrated that the fine-scale spatiotemporal use patterns of the leopard cats were consistent and highly correlated with the nocturnal rats under livestock disturbance. We suggest that appropriate restrictions on livestock disturbance should be implemented by reserve managers to reduce the threat to wildlife and achieve multi-species coexistence.

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.

An intercontinental comparison of insect seed predation between introduced and native oaks.

Novel interactions between introduced oaks and their natural enemies across different continents provide an opportunity to test the enemy release hypothesis (ERH) at local and global scales. Based on the ERH, we assessed the impacts of native seed-feeding insects on introduced and native oaks within and among continents. We combined a common-garden experiment in China and biogeographic literature surveys to measure seed predation by insects and the proportion of acorn embryos surviving after insect infestation among 4 oak species with different geographical origins: Quercus mongolica origin from China, Q. robur and Q. petraea from Europe, and Q. rubra from North America. Mostly supporting the ERH, oaks in introduced continents escaped seed predation compared to those in native continents and compared to other native oaks in introduced continents. Common-garden comparisons showed that total acorn infestation rate of introduced Q. rubra (section Lobatae) was considerably lower than that of native oaks (section Quercus) in China and Europe, likely because of the differences in seed traits associated with different oak sections. Literature surveys showed that seed predation of introduced oaks was lower in the introduced continent than in the native continent. Embryo survival was higher in introduced Q. rubra than native oaks in China and Poland. However, insect seed predation of recently introduced Q. rubra in China was similar to that in Europe, which is not consistent with the ERH. Our results suggest that reduced acorn attack by native insects and higher embryo survival after acorn damage could increase the establishment success or invasion risk of introduced oaks in non-native continents.

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.

The functional roles of species in metacommunities, as revealed by metanetwork analyses of bird-plant frugivory networks.

Understanding how biodiversity and interaction networks change across environmental gradients is a major challenge in ecology. We integrated metacommunity and metanetwork perspectives to test species' functional roles in bird-plant frugivory interactions in a fragmented forest landscape in Southwest China, with consequences for seed dispersal. Availability of fruit resources both on and under trees created vertical feeding stratification for frugivorous birds. Bird-plant interactions involving birds feeding only on-the-tree or both on and under-the-tree (shared) had a higher centrality and contributed more to metanetwork organisation than interactions involving birds feeding only under-the-tree. Moreover, bird-plant interactions associated with large-seeded plants disproportionately contributed to metanetwork organisation and centrality. Consequently, on-the-tree and shared birds contributed more to metanetwork organisation whereas under-the-tree birds were more involved in local processes. We would expect that species' roles in the metanetwork will translate into different conservation values for maintaining functioning of seed-dispersal networks.

Endozoochory of frugivorous birds as potential dispersal of seed parasites from Pistacia chinesis: experimental evidence.

The plant-disperser-fruit pest triads involve 3 interacting animals or groups (plants, vertebrates and seed parasites), and the dispersal of both seeds and seed parasites, which can both benefit from endozoochory via defecation or regurgitation by frugivorous vertebrates. However, we have very limited knowledge about the ecological and evolutionary consequences of these plant-disperser-fruit pest triads. Across central Northern China, several seed wasps (mainly Eurytoma plotnikov attack Pistacia chinensis fruits, and seed wasp larvae can develop, diapause and finally emerge as adults inside a seed during the following 1-3 years. In this study, we experimentally investigated whether frugivorous birds discriminated P. chinesis fruits with or without seed parasites, and whether bird endozoochory (by defecation or regurgitation) affected larval survival of seed parasites. The infestation rate by seed parasites was 37% of the P. chinesis fruit crop but with up to 48% of aborted fruits. We found that all 5 bird species can discriminate and then reject all unhealthy fruits (including aborted and insect-infested). However, 4 of the 5 bird species, in particular bulbul species, consumed 15-41% of aborted and insect-infested fruits as complementary food only when these unhealthy fruits were provided. Moreover, all larva of seed parasites remained alive after bird defecation or regurgitation. In conclusion, our study demonstrates that endozoochory by frugivorous birds could lead to potential dispersal of seed parasites of P. chinensis but with a very low probability.

How seed defense and seed abundance predict dispersal and survival patterns in Camellia.

Little is known about how seed defense and seed abundance interact with behavioral responses of seed dispersers to predict dispersal and survival dynamics in animal-dispersed plants. By tracking the fate of individual seeds in Camellia stands with high and low seed abundance in Southwest China in 2007, we investigated the dispersal and survival of 2 high-saponin Camellia species (Camellia oleifera and Camellia sinensis and 1 non-saponin species (peanut Arachis hypogaea) as a control. Saponins in Camellia seeds are chemical compounds that act as seed defense. Our results were most consistent with the predictions based on the predator satiation hypothesis and the plant defense hypothesis. At the abundant Camellia stand (predators and dispersers were satiated), more Camellia seeds survived at the source but fewer were hoarded and survived at cache sites. At the sparse Camellia stand (predators and dispersers were not satiated), no Camellia seeds survived at the source, but more Camellia seeds were hoarded and survived at cache sites. Unlike Camellia seeds, no peanuts survived at the source at both stands, while more peanuts were hoarded and then survived at cache sites in the abundant Camellia stand compared to none at the sparse Camellia stand. In addition, the 2 Camellia species showed similar trends for seed fates across different dispersal stages. Our study indicates that the combined effects of seed abundance and seed defense, compared to their separate effects, provide a more accurate prediction for dispersal and survival patterns in animal-dispersed Camellia species.

Activity Rhythms of Coexisting Red Serow and Chinese Serow at Mt. Gaoligong as Identified by Camera Traps.

Surveying the activity rhythms of sympatric herbivorous mammals is essential for understanding their niche ecology, especially for how they partition resources and their mechanisms of coexistence. Over a five-year period, we conducted infrared camera-trapping to monitor the activity rhythms of coexisting red serow (Capricornis rubidus) and Chinese serow (C. milneedwardsii milneedwardsii) in the remote mountainous region of Pianma, Mt. Gaoligong, Yunnan, China. Cameras captured images of red serow and Chinese serow on 157 and 179 occasions, respectively. We used circular kernel density models to analyze daily activity rhythms and how temporal variations in activity ensure their co-existence. Although their overall activity levels and patterns were similar, temporal activity and behavior partitioning among the two species occurred during the wet season. Compared with Chinese serows, red serows exhibited less variable daily activity levels, patterns, as well as feeding and vigilance behaviors between seasons. When the two species occasionally ranged together, red serows tended to alter their activity pattern while Chinese serows significantly increased their activity level. Red serow and Chinese serow are exploitative competitors but coexist by altering their daily activity rhythms when in contact and changing activity patterns during the wet season, enabling their coexistence.

Gut region influences the diversity and interactions of bacterial communities in pikas (Ochotona curzoniae and Ochotona daurica).

The mammalian microbial communities in the gastrointestinal tract (GIT) play important roles in host nutrition and health. However, we still lack an understanding of how these communities are organized across GIT in natural environments. Here, using 16S rRNA gene sequencing, we analyzed the bacterial community diversity, network interactions and ecosystem stability across five gut regions (mouth, stomach, small intestine, cecum and colon) emanating from two common pika species in China, including Plateau pikas (Ochotona curzoniae) inhabiting high-altitude regions, as well as Daurian pikas (O. daurica) occupying low-altitude areas. The relative abundances of dominant Bacteroidetes and Firmicutes exhibited an increasing trend from mouth to colon. Cecum and colon harbored higher bacterial diversity compared with other anatomical regions. Gut region significantly influenced the structure of bacterial communities in the GIT. Network analysis indicated that topological features showed marked variations among gut regions. Interestingly, the ecosystem stability of bacterial communities increased gradually from mouth to colon. Our results suggest that gut region influences the diversity, structure and network interactions of bacterial communities in pikas. For hindgut-fermenting herbivorous mammals, relatively higher bacterial diversity and ecosystem stability in the cecum may provide a favorable condition for the fermentation of indigestible plant polysaccharides.

Seed-predator satiation and Janzen-Connell effects vary with spatial scales for seed-feeding insects.

BACKGROUND AND AIMS: The Janzen-Connell model predicts that common species suffer high seed predation from specialized natural enemies as a function of distance from parent trees, and consequently as a function of conspecific density, whereas the predator satiation hypothesis predicts that seed attack is reduced due to predator satiation at high seed densities. Pre-dispersal predation by insects was studied while seeds are still on parent trees, which represents a frequently overlooked stage in which seed predation occurs. METHODS: Reproductive tree density and seed production were investigated from ten Quercus serrata populations located in south-west China, quantifying density-dependent pre-dispersal seed predation over two years by three insect groups. KEY RESULTS: Acorn infestation was nearly twice as high in the low-seed year as that in the high-seed year, with considerable spatio-temporal variation in the direction and magnitude of density-dependent pre-dispersal seed predation evident. Across whole populations of trees, a high density of reproductive trees caused predator satiation and reduced insect attack in the high-seed year. Within individual trees, and consistent with the Janzen-Connell model, overall insect seed predation was positively correlated with seed production in the low-seed year. In addition, there was variation among insect taxa, with positive density-dependent seed predation by Curculio weevils in the high-seed year and moths in the low-seed year, but apparent density independence by Cyllorhynchites weevils in both years. CONCLUSIONS: The overall trend of negative density-dependent, pre-dispersal seed predation suggests that predator satiation limited the occurrence of Janzen-Connell effects across Q. serrata populations. Such effects may have large impacts on plant population dynamics and tree diversity, depending on the extent to which they are reduced by counteracting positive density-dependent predation for seeds on individual trees and other factors affecting successful recruitment.

Diet Diversity Is Associated with Beta but not Alpha Diversity of Pika Gut Microbiota.

Wild mammals often consume different food sources as they become geographical available. This change in diet composition is likely to influence the gut microbial community, yet it remains unclear what the relationship looks like-particularly in small herbivores-under natural conditions. We used DNA sequencing approaches to characterize the diet composition and gut microbial community of wild plateau pikas (Ochotona curzoniae) collected from three altitudes. We tested if diet and gut microbiota composition changes across altitudes, and the relationship between diet diversity and gut microbiota diversity. Our results showed that altitude significantly influences the composition of diet and gut microbial communities. Notably, the alpha diversity (Shannon diversity and observed OTUs) of individual diet was not significantly correlated with that of gut microbiota, whereas the beta diversity (Jaccard and Bray-Curtis dissimilarity) of diet was positively correlated with that of gut microbiota. Our study is the first time to highlight the relationship between diet and gut microbiota composition in wild pikas on the Qinghai-Tibet Plateau. It suggests that the species richness within individual gut microbiota does not linearly increase with diet diversity, whereas those individuals that are more similar in diet composition harbor more similar gut microbiota.

Evemphyron sinense, a new genus and species infesting legume seedpods in China (Coleoptera, Attelabidae, Rhynchitinae).

A new genus Evemphyron Alonso-Zarazaga, Lv & Wang, gen. n., belonging to Attelabidae Rhynchitinae, is described. Its single species, Evemphyron sinense Alonso-Zarazaga, Lv & Wang, sp. n., was reared from larvae found inside seed pods of the legume Callerya dielsiana (Fabaceae, Millettieae) in Sichuan Province (China). The species is figured and placed in the Deporaini because of the presence of minute labial palpi, the strongly crescentic apex of the postmentum, and the apodemes of male IX sternite and female VIII sternite curved sinistro-anterially near their cephalic end. It shows 3-segmented labial palpi and male sex patches on the procoxae, characters that suggest a basal position in the tribe.

Contrasting patterns of short-term indirect seed-seed interactions mediated by scatter-hoarding rodents.

It is well known that direct effects of seed predators or dispersers can have strong effects on seedling establishment. However, we have limited knowledge about the indirect species interactions between seeds of different species that are mediated by shared seed predators and/or dispersers and their consequences for plant demography and diversity. Because scatter-hoarding rodents as seed dispersers may leave some hoarded seeds uneaten, scatter hoarding may serve to increase seed survival and dispersal. Consequently, the presence of heterospecific seeds could alter whether the indirect interactions mediated by scatter-hoarding rodents have a net positive effect, creating apparent mutualism between seed species, or a net negative effect, creating apparent competition between seed species. We present a testable framework to measure short-term indirect effects between co-occurring plant species mediated by seed scatter-hoarding rodents. We tested this framework in a subtropical forest in south-west China using a replacement design and tracked the fate of individually tagged seeds in experimental patches. We manipulated the benefits to rodents by using low-tannin dormant chestnuts as palatable food and high-tannin non-dormant acorns as unpalatable food. We found that seed palatability changed the amount of scatter hoarding that occurred when seeds co-occurred either among or within patches. Consistent with our predictions, scatter-hoarding rodents created apparent mutualism through increasing seed removal and seed caching, and enhancing survival, of both plant species in mixed patches compared with monospecific patches. However, if we ignore scatter hoarding and treat all seed harvest as seed predation (and not dispersal), then apparent competition between palatable chestnuts and unpalatable acorns was also observed. This study is the first to demonstrate that foraging decisions by scatter-hoarding animals to scatter hoard seeds for later consumption (or loss) or consume them can influence indirect effects among co-occurring seeds, and rodent-mediated indirect effects vary depending on whether the harvested seeds are hoarded or eaten.

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.