Conflicting selection pressures on seed size and germination caused by carnivorous seed dispersers

Plants produce nutritious, fleshy fruits that attract various animals to facilitate seed dispersal and recruitment dynamic. Species-specific differential selection of seed size by multiple frugivorous disperser assemblages may affect the subsequent germination of the ingested seeds. However, there is little empirical evidence supporting this association. In the present study, we documented conflicting selection pressures exerted on seed size and germination by five frugivorous carnivores on a mammal-dispersed pioneer tree, the date-plum persimmon (Diospyros lotus), in a subtropical forest. Fecal analyses revealed that these carnivores acted as primary seed dispersers of D. lotus. We also observed that seed sizes were selected based on body mass and were species-specific, confirming the “gape limitation” hypothesis; three small carnivores (the masked palm civet Paguma larvata, yellow-throated marten Martes flavigula, and Chinese ferret-badger Melogale moschata) significantly preferred to disperse smaller seeds in comparison with control seeds obtained directly from wild plants whereas the largest Asiatic black bears (Ursus thibetanus) ingested larger seeds. Seeds dispersed by medium-sized hog badgers (Arctonyx albogularis) were not significantly different from control seeds. However, regarding the influence of gut passage on seed germination, three arboreal dispersal agents (martens, civets, and bears) enhanced germination success whereas terrestrial species (ferret-badgers and hog badgers) inhibited the germination process compared with undigested control seeds. These conflicting selection pressures on seed size and germination may enhance the heterogeneity of germination dynamics and thus increase species fitness through diversification of the regeneration niche. Our results advance our understanding of seed dispersal mechanisms and have important implications for forest recruitment and ecosystem dynamics.     

Detection of the Severe Acute Respiratory Syndrome‐Related Coronavirus and Alphacoronavirus in the Bat Population of Taiwan

Bats have been demonstrated to be natural reservoirs of severe acute respiratory syndrome coronavirus (SARS CoV) and Middle East respiratory syndrome (MERS) CoV. Faecal samples from 248 individuals of 20 bat species were tested for partial RNA‐dependent RNA polymerase gene of CoV and 57 faecal samples from eight bat species were tested positive. The highest detection rate of 44% for Scotophilus kuhlii, followed by 30% for Rhinolophus monoceros. Significantly higher detection rates of coronaviral RNA were found in female bats and Scotophilus kuhlii roosting in palm trees. Phylogenetic analysis classified the positive samples into SARS‐related (SARSr) CoV, Scotophilus bat CoV 512 close to those from China and Philippines, and Miniopterus bat CoV 1A‐related lineages. Coronaviral RNA was also detected in bat guano from Scotophilus kuhlii and Myotis formosus flavus on the ground and had potential risk for human exposure. Diverse bat CoV with zoonotic potential could be introduced by migratory bats and maintained in the endemic bat population in Taiwan.     

High rodent abundance increases seed removal but decreases scatter-hoarding and seedling recruitment along an elevational gradient

The distributions of small rodents in mountainous environments across different elevations can provide important information regarding the effects of climate change on the dispersal of plant species. However, few studies of oak forest ecosystems have compared the elevational patterns of sympatric rodent diversity, seed dispersal, seed bank, and seedling abundance. Thus, we tested the differences in the seed disperser composition and abundance, seed dispersal, seed bank abundance, and seedling recruitment for Quercus wutaishanica along 10 elevation levels in the Taihang Mountains, China. Our results provide strong evidence that complex asymmetric seed dispersal and seedling regeneration exist along an elevational gradient. The abundance of rodents had a significant negative correlation with the elevation and the seed removal rates peaked and then declined with increasing elevation. The seed removal rates were higher at middle and lower elevations than higher elevations but acorns were predated by 5 species of seed predators at middle and lower elevations, and thus, there was a lower likelihood of recruitment compared with those dropped beneath mother oaks at higher elevations. More importantly, the number of individual seeds in the seed bank and seedlings increased with the elevation, although dispersal services were reduced at sites lacking rodents. As conditional mutualists, the rodents could possibly act as antagonistic seed predators rather than mutualistic seed dispersers at low and middle elevations, thereby resulting in the asymmetric pattern of rodent and seedling abundance with increasing elevation to affect the community assembly and ecosystem functions on a large spatial scale.     

Detection and phylogenetic characterization of astroviruses in insectivorous bats from Central‐Southern Italy

In recent years, bats have been found to harbour many viruses, raising several questions about their role as reservoirs and potential disseminators of zoonotic viruses. We investigated the presence of six virus families in bats in three regions of Central‐Southern Italy. Astroviruses were identified in seven of 13 bat species. Sequence analysis revealed marked genetic heterogeneity among the astroviruses identified, with nucleotide identity ranging between 60.26% and 87.62%. Astrovirus diversity was not associated with the bat species, the geographic areas or the bat colony, suggesting the circulation of several astrovirus strains in Italian ecosystems. Genetic diversification and interspecies transmission appear common in bat astroviruses and could provide, potentially, the bases for transmission to humans and other mammals. Yet overemphasizing this risk might have detrimental consequences for bat conservation and preservation of the important ecosystem services bats provide.     

Predation of cassowary dispersed seeds: is the cassowary an effective disperser?

Post‐dispersal predation is a potentially significant modifier of the distribution of recruiting plants and an often unmeasured determinant of the effectiveness of a frugivore's dispersal service. In the wet tropical forests of Australia and New Guinea, the cassowary provides a large volume, long distance dispersal service incorporating beneficial gut processing; however, the resultant clumped deposition might expose seeds to elevated mortality. We examined the contribution of post‐dispersal seed predation to cassowary dispersal effectiveness by monitoring the fate of 11 species in southern cassowary (Casuarius casuarius johnsonii Linnaeus) droppings over a period of 1 year. Across all species, the rate of predation and removal was relatively slow. After 1 month, 70% of seeds remained intact and outwardly viable, while the number fell to 38% after 1 year. The proportion of seeds remaining intact in droppings varied considerably between species: soft‐seeded and large‐seeded species were more likely to escape removal and predation. Importantly, across all species, seeds in droppings were no more likely to be predated than those left undispersed under the parent tree. We speculate that seed predating and scatter‐hoarding rodents are responsible for the vast majority of predation and removal from droppings and that the few seeds which undergo secondary dispersal survive to germination. Our findings reinforce the conclusion that the cassowary is an important seed disperser; however, dispersal effectiveness for particular plant species can be reduced by massive post‐dispersal seed mortality.     

Book Review

Agricultural landscapes are typically associated with a decreased biodiversity, particularly when they extend across large spatial scales. Despite the fact that some African bat species seem to provide essential ecosystem services across landscapes, we only have a limited understanding of how intensive agricultural practices influence bat communities. This study investigated the effects of sugarcane monoculture on the composition of both bat species and functional groups across a conservation-agricultural matrix. Specifically, we wanted to understand changes in the bat communities within savannas and sugarcane plantations. We categorised bats into broad foraging (functional) groups based on their echolocation call structure: open-air; clutter-edge; and, clutter. To measure bat activity, we established twelve 25 ha grids randomly located in savanna and sugarcane vegetation. Within each grid we placed nine acoustic detectors, in 3 × 3 formation, 250 m apart; totalling 54 plots in each land use. We sampled each plot over four nights (two in the wet season and two in the dry season) during a one-year period. We did not observe a significant difference in species richness between savanna and sugarcane. However, there was a difference in functional group composition. Sugarcane negatively affected clutter foragers; this group was practically absent here despite occurring within neighbouring savannas. We observed distinct patterns of seasonality in bat activity, with activity of all functional groups being reduced in the dry season.     

Spatial and temporal effects on seed dispersal and seed predation of Musa acuminata in southern Yunnan, China

Wild bananas are abundant in tropical areas and many ecologists have observed that the succession process is quicker following increased disturbance. This study was conducted to analyze animal-seed interactions and their effects on the seed fate of a wild banana species (Musa acuminata) in tropical southern Yunnan (China) through experiments considering spatial (site and habitat) and temporal (seasons) variation. The largest proportion of fruits (81%) was removed by frugivorous seed dispersers, especially by bats at nighttime. Only 13% of the fruits were removed by climbing seed predators (different species of rats). In the exclosure treatment, rodents accounted for a significantly higher total artificially exposed seed removal number than ants, but with spatial and temporal differences. The highest seed predation rate by rodents (70%) was found in forest with wild banana stands, corresponding with the highest rodent diversity (species numbers and abundance) among the habitat types. In contrast, the seed removal number by ants (57%) was highest in the open land habitats, but there was no close correlation with ant diversity. Seed removal numbers by ants were significantly higher in the dry compared to the rainy season, but rodent activity showed no differences between seasons. The overall results suggest that the largest proportion of seeds produced by wild banana are primarily dispersed by bats. Primary seed dispersal by bats at nighttime is essential for wild banana seeds to escape seed predation.     

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.     

高寒草甸牦牛皮毛种子库大小与组成的模拟研究

动物体外传播(Epizoochorous dispersal)是植物种子实现远距离传播的一种重要方式,尤其在放牧生态系统中,这种现象更为普遍。为探究放牧季节(暖季和冷季)及种子性状(质量、形状和附属结构)对高寒草甸牦牛皮毛种子库的大小及组成特征的调控作用,分别在2019年暖季(8月下旬)和冷季(10月中旬),模拟收集了牦牛皮毛附着的种子,并对皮毛种子库大小和组成及种子形态学特征(质量和形状)进行了统计。结果表明:暖季皮毛种子库大小(585.27±23.56粒/m ²)显著高于冷季(218.18±22.67粒/m ²)(P<0.05),并且暖季皮毛种子库物种丰富度(16)和多样性指数(1.85±0.19)均高于冷季(4和0.66±0.11)。暖季皮毛种子库主要由多年生植物构成(87.50%),冷季时只包括多年生植物。皮毛种子库主要由中等质量(1~10mg)、形状不规则(形状指数>0.01)的种子构成,并且附着的种子中有75%存在附属结构(芒、冠毛、翅和距)。在高寒草甸放牧生态系统中,植物种子可以通过牦牛进行体外传播,这是草-畜互作的一种表现形式,也是动物-植物共同进化的结果。     

Widespread infection with hemotropic mycoplasmas in bats in Spain,including a hemoplasma closely related to “Candidatus Mycoplasma hemohominis”

Molecular analyses of blood samples revealed infection with hemoplasmas in 97% of 31 cave bats captured in three caves in North-Eastern Spain. The characterization of 1250 bp of the 16S rRNA gene in 29 of the positive bats identified two different groups of sequences. Twenty-two Schreibers’ bats (Miniopterus schreibersii) and one long-eared bat (Myotis capaccinii) shared one group, composed of seven closely related sequences. These sequences showed an identity of about 97% with “Candidatus Mycoplasma hemohominis” and the phylogenetic branch including bat and human sequences showed a 100% bootstrap value, supporting a close phylogenetic relationship between these hemoplasmas. The second group, representing a potentially novel species, was composed of a single sequence shared by six Schreibers’ bats that had 91% identity with the recently reported hemoplasma from little brown bats in North America. Large bat aggregations in roosting caves probably benefits intra and inter-species transmission explaining the high observed prevalence.     

绢蒿荒漠植物种子大小、形状变异及其生态适应特征

广布于北疆地区的绢蒿荒漠草地作为重要牧场蕴含着丰富的生物多样性。收集了绢蒿荒漠的88种植物种子,对种子大小、形状及物种生活型进行了测定和分析,利用系统比较的方法对不同种子的大小和形状两个主要性状进行了谱系信号分析,并对不同种子对荒漠、半荒漠环境条件的适应类型进行了归纳分类。结果表明,88种种子大小可划分为A型(0.01~0.10 mg)、B型(0.10~1.00 mg)、C型(1.00~10.00 mg)和D型(10.00~50.00 mg) 4种类型,其中B和C型种子在数量上占优势地位。所涉及物种可分为6种生活型,以一年生、多年生及短命植物为主。种子形状指数为0.00~0.20,细长或扁平种子有42种,球形或接近球形种子有46种。种子大小和形状在不同科间、科内种间以及同种植物异型种子间均具有极显著差异。种子大小无明显的谱系信号,存在一定的可塑性。种子形状具有明显的谱系信号,表现出较强的稳定性。绝大多数植物种子能够通过种子多型性、产生种子粘液、具有助力传播结构、特殊生活型以及动物消化道传播等适应对策对特殊环境产生很强的适应性。     

Does multiple seed loading in Blue Jays result in selective dispersal of smaller acorns?

Studies from both tropical and temperate systems show that scatter‐hoarding rodents selectively disperse larger seeds farther from their source than smaller seeds, potentially increasing seedling establishment in larger‐seeded plants. Size‐biased dispersal is evident in many oaks (Quercus) and is true both across and within species. Here, we predict that intraspecifc variation in seed size also influences acorn dispersal by the Blue Jay (Cyanocitta cristata Linnaeus), but in an opposite manner. Blue Jays are gape‐limited and selectively disperse smaller acorn species (e.g. pin oaks [Quercus palustris Münchh]), but often carry several acorns in their crop during a single dispersal event. We predict that jays foraging on smaller acorns will load more seeds per trip and disperse seeds to greater distances than when single acorns are carried in the bill. To test this, we presented free‐ranging Blue Jays with pin oak acorns of different sizes over a 2‐year period. In each of 16 experimental trials, we monitored the birds at a feeding station with remote cameras and determined the number of acorns removed and the distance acorns were dispersed when cached. Jays were significantly more likely to engage in multiple seed loading with smaller seeds in both years of the study. During the second year, these smaller acorns were dispersed farther than larger acorns, and during the first year, larger acorns were dispersed farther, revealing an inconsistent response to seed size during our study. We suggest that in some circumstances, multiple seed loading by Blue Jays may favor dispersal in some plant species.     

Trends in national surveillance for rabies among bats in the United States (1993-2000)

OBJECTIVE: To describe surveillance trends and epidemiologic features of rabies in bats in the United States, focusing on 3 bat species primarily associated with variants of the rabies virus that affect humans. DESIGN: Retrospective study. ANIMALS: 31,380 bats. PROCEDURE: Data on rabies for bats identified to species and reported by state laboratories from 1993 to 2000 were analyzed, focusing on silver-haired, eastern pipistrelle, and Brazilian free-tailed bats. Categoric variables were derived from other provided information. RESULTS: Data were reported from 37 states during the study interval; complete species-specific data were not reported by any state for the entire interval. Bats primarily associated with rabies virus variants affecting humans were more likely to yield positive test results for rabies (22.7%), compared with all other bats (5.5%) in most seasons and from most regions of the United States. However, certain other bat species had higher percentages of positive results. Risk of positive results was highest in the fall and highest among bats originating in the southwestern United States. CONCLUSIONS AND CLINICAL RELEVANCE: Increased risk of rabies among certain groups of bat species was consistently found across seasons and most geographic regions of the United States. Results were in general agreement with those of previous studies conducted within smaller geographic regions. There are ongoing efforts to improve surveillance of rabies in bats, although surveillance is incomplete in some regions.     

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.     

Dispersal of invasive Phytolacca americana seeds by birds in an urban garden in China

Although seed dispersal is a key process determining the regeneration and spread of invasive plant populations, few studies have explicitly addressed the link between dispersal vector behavior and seedling recruitment to gain insight into the invasion process within an urban garden context. We evaluated the role of bird vectors in the dispersal of pokeweed (Phytolacca americana), a North American herb that is invasive in urban gardens in China. Fruiting P. americana attracted both generalist and specialist bird species that fed on and dispersed its seeds. The generalist species Pycnonotus sinensis and Urocissa erythrorhyncha were the most frequent dispersers. Seedling numbers of P. americana were strongly associated with the perching behavior of frugivorous birds. If newly recruited bird species use seedling‐safe perching sites, the P. americana will regenerate faster, which would enhance its invasive potential. Based on our observations, we conclude that the 2 main bird vectors, P. sinensis and U. erythrorhyncha, provide potential effective dispersal agents for P. americana. Our results highlight the role of native birds in seed dispersal of invasive plants in urban gardens.     

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.     

Effects of fragmentation on the seed predation and dispersal by rodents differ among species with different seed size

Fragmentation influences the population dynamics and community composition of vertebrate animals. Fragmentation effects on rodent species in forests may, in turn, affect seed predation and dispersal of many plant species. Previous studies have usually addressed this question by monitoring a single species, and their results are contradictory. Very few studies have discussed the fragmentation effect on rodent–seed interaction among tree species with different seed sizes, which can significantly influence rodent foraging preference and seed fate. Given that fruiting periods for many coexisting plant species overlap, the changing foraging preference of rodents may substantially alter plant communities. In this study, we monitored the dispersal and predation by rodents of 9600 seeds, belonging to 4 Fagaceae species with great variation in seed size, in both the edge and interior areas of 12 tropical forest fragments ranging in area from 6.3 to 13872.9 ha in Southwest China. The results showed that forest fragmentation altered the seed fates of all the species, but the intensity and even the direction of fragmentation effect differed between species with large versus small seeds. For the seeds harvested, fragment size showed negative effects in forest interiors but positive effects at edges for the 2 large‐seeded species, but showed little effect for the 2 small‐seeded species. For the seeds removed, negative effects of fragment size only existed among the small‐seeded species. The different fragmentation effect on seed dispersal and predation among plant species may, in turn, translate into the composition differences of the regeneration of the whole fragmented forest.     

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.     

青藏高原东缘唇形科植物种子大小对萌发的影响研究

以青藏高原东缘地区24种唇形科(Lamiaceae)种子为材料,在室外自然光照条件下进行萌发试验,研究种子大小与萌发特性的关系,为当地的植被保护或恢复对策的制定提供一定的科学依据。结果表明:24种唇形科植物种子的百粒重为0.0061～0.5688 g,跨越2个数量级,平均大小0.1200 g,60%的物种种子百粒重小于0.1200 g,表明在青藏高原东缘唇形科植物种子中小种子占优势。种子大小与萌发率和萌发速率指数呈极显著负相关(P<0.01);种子大小与集中度呈极显著正相关(P<0.001);种子大小与萌发开始时间的相关性不显著。这些结果说明,这24种唇形科植物的大种子物种和小种子物种有2种相反的萌发对策:小种子萌发率高,萌发速率快,萌发历期短,萌发整齐性好;大种子与小种子相反,并共同与其扩散能力构成了一个由小种子物种(拓植能力)到大种子物种(竞争能力)的连续体,从种子萌发对策上解释了大、小种子物种在同一自然群落中如何共存的问题。