The messenger matters: Pollinator functional group influences mating system dynamics

The incredible diversity of plant mating systems has fuelled research in evolutionary biology for over a century. Currently, there is broad concern about the impact of rapidly changing pollinator communities on plant populations. Very few studies, however, examine patterns and mechanisms associated with multiple paternity from cross‐pollen loads. Often, foraging pollinators collect a mixed pollen load that may result in the deposition of pollen from different sires to receptive stigmas. Coincident deposition of self‐ and cross‐pollen leads to interesting mating system dynamics and has been investigated in numerous species. But, mixed pollen loads often consist of a diversity of cross‐pollen and result in multiple sires of seeds within a fruit. In this issue of Molecular Ecology, Rhodes, Fant, and Skogen ( 2017 ) examine how pollinator identity and spatial isolation influence multiple paternity within fruits of a self‐incompatible evening primrose. The authors demonstrate that pollen pool diversity varies between two pollinator types, hawkmoths and diurnal solitary bees. Further, progeny from more isolated plants were less likely to have multiple sires regardless of the pollinator type. Moving forward, studies of mating system dynamics should consider the implications of multiple paternity and move beyond the self‐ and cross‐pollination paradigm. Rhodes et al. ( 2017 ) demonstrate the importance of understanding the roles that functionally diverse pollinators play in mating system dynamics.     

Morphological specialization of heterantherous Rhynchanthera grandiflora (Melastomataceae) accommodates pollinator diversity

• The tropical Melastomataceae are characterized by poricidal anthers which constitute a floral filter selecting for buzz‐pollinating bees. Stamens are often dimorphic, sometimes with discernible feeding and pollinating functions. Rhynchanthera grandiflora produces nectarless flowers with four short stamens and one long stamen; all anthers feature a narrow elongation with an upwards facing pore.
• We tested pollen transfer by diverse foraging bees and viability of pollen from both stamen types. The impact of anther morphology on pollen release direction and scattering angle was studied to determine the plant's reproductive strategy.
• Medium‐sized to large bees sonicated flowers in a specific position, and the probability of pollen transfer correlated with bee size even among these legitimate visitors. Small bees acted as pollen thieves or robbers. Anther rostrum and pore morphology serve to direct and focus the pollen jet released by floral sonication towards the pollinator's body. Resulting from the ventral and dorsal positioning of the short and long stamens, respectively, the pollinator's body was widely covered with pollen. This improves the plant's chances of outcrossing, irrespective of which bee body part contacts the stigma. Consequently, R. grandiflora is also able to employ bee species of various sizes as pollen vectors.
• The strategy of spreading pollen all over the pollinator's body is rather cost‐intensive but counterbalanced by ensuring that most of the released pollen is in fact transferred to the bee. Thus, flowers of R. grandiflora illustrate how specialized morphology may serve to improve pollination by a functional group of pollinators.

     

The effectiveness of flower strips and hedgerows on pest control,pollination services and crop yield: a quantitative synthesis

Floral plantings are promoted to foster ecological intensification of agriculture through provisioning of ecosystem services. However, a comprehensive assessment of the effectiveness of different floral plantings, their characteristics and consequences for crop yield is lacking. Here we quantified the impacts of flower strips and hedgerows on pest control (18 studies) and pollination services (17 studies) in adjacent crops in North America, Europe and New Zealand. Flower strips, but not hedgerows, enhanced pest control services in adjacent fields by 16% on average. However, effects on crop pollination and yield were more variable. Our synthesis identifies several important drivers of variability in effectiveness of plantings: pollination services declined exponentially with distance from plantings, and perennial and older flower strips with higher flowering plant diversity enhanced pollination more effectively. These findings provide promising pathways to optimise floral plantings to more effectively contribute to ecosystem service delivery and ecological intensification of agriculture in the future.     

Deceptive pollination of Calanthe by skippers that commonly act as nectar thieves

Flowers have developed different strategies to attract pollinators through visual or olfactory signals. Most flowers offer pollinators a reward (e.g. nectar and pollen) for the pollination service. However, one‐third of Orchidaceae have been shown not to provide a reward. Calanthe are terrestrial orchids distributed throughout China, Nepal, Japan and tropical Asia. Despite its high diversity, the pollination biology of Calanthe remains largely unknown, even though it is an important aspect of plant conservation. In the study, through field surveying, there were three Hesperiidae butterflies pollinating two species of Calanthe and the pollination behavior differed between the two species of Calanthe, which might lead to different fruit setting rates. There was no nectar in the flowers of the two species, indicating deceptive pollination. Using a glass cylinder experiment, it was deduced that the two species of Calanthe were most likely to attract pollinators by generalized food deception. Interestingly, Hesperiidae butterflies were traditionally thought to be nectar thieves and generally do not transmit pollinia. However, our findings showed that, in this case, the thieves were deceived by the plants and pollinated them for free.     

Darwin's vexing contrivance: a new hypothesis for why some flowers have two kinds of anther

Heteranthery, the presence of two or more anther types in the same flower, is taxonomically widespread among bee-pollinated angiosperms, yet has puzzled botanists since Darwin. We test two competing hypotheses for its evolution: the long-standing ‘division of labour'' hypothesis, which posits that some anthers are specialized as food rewards for bees whereas others are specialized for surreptitious pollination, and our new hypothesis that heteranthery is a way to gradually release pollen that maximizes pollen delivery. We examine the evolution of heteranthery and associated traits across the genus Clarkia (Onagraceae) and study plant–pollinator interactions in two heterantherous Clarkia species. Across species, heteranthery is associated with bee pollination, delayed dehiscence and colour crypsis of one anther whorl, and movement of that anther whorl upon dehiscence. Our mechanistic studies in heterantherous species show that bees notice, forage on and export pollen from each anther whorl when it is dehiscing, and that heteranthery promotes pollen export. We find no support for division of labour, but multifarious evidence that heteranthery is a mechanism for gradual pollen presentation that probably evolved through indirect male–male competition for siring success.     

Flower biology of the cactus Coryphantha elephantidens in the tropical dry forest of Central Mexico

Floral traits and sexual systems in angiosperms are strategies that enhance outcrossing within hermaphrodite flowers and among individuals in a population. Sexual systems with unisexual flowers have also evolved among angiosperms, resulting in sex specialization. Furthermore, the interaction of floral traits and floral visitors determines successful plant reproduction. Globose cacti are bee pollinated, and variation in the diversity of their pollinator assemblages is strongly associated with floral phenotype. Our objective was to describe the floral biology of the cactus Coryphantha elephantidens and to determine its relationship with pollinators. Floral traits were studied by direct observations in live and fixed flowers. The breeding system was determined using two estimators based on floral morphology: pollen grains to ovules per flower (P/O) ratio and outcrossing index. Pollination treatments were conducted to determine the mating system. Floral visitors were recorded using direct observation. Flowers of C. elephantidens are variable in color, protandric, herkogamous and nectarless. Estimators of the breeding system indicated xenogamy, which is consistent with the obligate outcrossing revealed by the pollination experiment. Thirty-seven percent of the plants have female flowers that do not produce pollen, making this population functionally gynodioecious. Both fruit and seed set were high compared to other globose cacti. Pollinators included eight species of native bees, a more diverse pollinator assemblage than other globose cacti. Given the high pressure on pollen due to functional gynodioecy, nectarless flowers, an outcrossing mating system, and the necessity of pollinators to set seeds, we concluded that native bees are highly efficient pollinators that play a crucial role in the sexual reproduction of C. elephantidens.     

Spatial behaviour of sheep during the neonatal period: Preliminary study on the influence of shelter

Effective shelter has been demonstrated to reduce neonatal lamb mortality rates during periods of inclement weather. Periods of high wind speed and rainfall have been shown to influence shelter usage; however, it is not yet known how ewe factors such as breed, age and body condition score influence shelter-seeking behaviour. This study, conducted on a working upland farm in the UK, examined impact of artificial shelter on the biological and climatic factors that influence peri-parturient ewe behaviour. Pregnant ewes (n = 147) were randomly allocated between two adjacent fields which were selected for their similarity in size, topography, pasture management, orientation to the prevailing wind and available natural shelter. In one field, three additional artificial shelters were installed to increase the available shelter for ewes, this field was designated the Test field; no additional artificial shelter was provided in the second field which was used as the Control field. Individual ewes were observed every 2 h between 0800 and 1600 for 14 continuous days to monitor their location relative to shelter. Ewe breed (Aberfield and Highlander), age (2–8 years) and body condition score were considered as explanatory variables to explain flock and individual variance in shelter-seeking behaviour and the prevalence of issues which required the intervention of the shepherd, termed ‘shepherding problems’. Any ewe observed with dystocia, a dead or poor vigour lamb or who exhibited mismothering behaviour was recorded as a shepherding problem. The prevalence of these shepherding problems which necessitate human intervention represents arguably the most critical limiting factor for the successful management of commercial sheep flocks in outdoor lambing systems. Overall, ewes in the Test field with access to additional artificial shelter experienced fewer shepherding problems than those in the Control field (P < 0.05). A significant breed effect was also observed, with Highlander ewes more likely to seek shelter than Aberfield ewes (P < 0.001), and experiencing significantly fewer shepherding interventions (P < 0.05). These findings demonstrate the substantial and significant benefits to animal welfare and productivity that can be achieved through the provision of shelter in commercial, upland, outdoor lambing systems in the UK.     

传粉昆虫下降背景下的授粉生态弹性: 内涵、机制和展望

全球传粉昆虫多样性正在下降, 如何保障农林生态系统传粉功能是当前研究的热点。理论上说, 传粉功能不仅与生态系统的传粉昆虫多样性相关, 还与生态系统的调节能力有关。近年来, 学者们逐渐认识到授粉生态弹性对传粉功能的影响。本文在回顾已有研究的基础之上, 总结传粉昆虫授粉生态弹性的内涵, 厘清授粉生态弹性与工程弹性、稳定性和抗性的异同。目前, 学者对授粉生态弹性形成机制开展广泛探讨, 提出功能冗余假说、密度补偿假说、响应多样性假说、连接周转假说和跨尺度弹性假说, 但这5个假说间的关系仍不清楚, 存在一词多义、词意混淆等现象。我们依次阐述功能冗余假说、密度补偿假说、响应多样性假说、连接周转假说和跨尺度弹性假说, 介绍不同假说中授粉生态弹性形成过程、研究热点和发展动态。通过解析授粉生态弹性的形成机制可知, 5个假说在内涵上存在紧密联系, 它们从不同空间尺度和研究对象下解释传粉昆虫授粉生态弹性的形成机制。未来授粉生态弹性研究将整合传粉昆虫群落动态和传粉功能动态的量化方法, 通过实验验证5个假说的合理性, 并揭示不同假说间的联系, 由此阐明授粉生态弹性的发生条件、形成阈值和动态规律。随着研究的深入, 授粉生态弹性理论有望用于指导农林生态系统传粉功能的经营管理。     

The pollination of Habenaria rhodocheila (Orchidaceae) in South China: When butterflies take sides

Habenaria is one of the largest terrestrial genera in the family Orchidaceae. Most field studies on Habenaria species with greenish–white and nocturnal scented flowers are pollinated by nocturnal hawkmoths and settling moths. However, H. rhodocheila presents reddish flowers lacking a detectable scent and fails to fit the moth pollination syndrome. We investigated the pollinators, breeding system, and functional traits of H. rhodocheila in South China and found that two diurnal swallowtail butterflies Papilio helenus and Papilio nephelus (Papilionidae) were the effective pollinators. When butterflies foraged for nectar in the spur, the pollinia became attached between the palpi. A triangular projected median rostellar lobe was found at the entrance (sinus) of the spur of H. rhodocheila. This lobe divided the spur opening into two entrances forcing butterflies to enter their proboscides through the left or right side. When the projection of median rostellar lobe was removed, the site of pollinium attachment changed to the eyes of the butterflies, leading to a higher rate of pollinium removal but lower rate of pollinium deposition. Our quartz glass cylinder choice experiment suggested that visual rather than olfactory cues provided the major stimuli for butterflies to locate these flowers. Hand pollination experiments suggested this species was self‐compatible but pollinator‐dependent. However, the proportion of seeds with large embryos produced in self‐pollinated fruits was significantly lower than in cross‐pollinated fruits, indicating a significant inbreeding depression. Unlike many other orchid species, fruit set was higher than rates of pollinium removal, indicating a high level of pollination efficiency in a species with friable pollinia. Shifts from moth to butterfly pollination in the genus Habenaria parallel other orchid lineages providing insights into the potential for pollinator‐mediated floral trait selection.     

Nectar sugar composition of European Caryophylloideae (Caryophyllaceae) in relation to flower length,pollination biology and phylogeny

Floral nectar composition has been explained as an adaptation to factors that are either directly or indirectly related to pollinator attraction. However, it is often unclear whether the sugar composition is a direct adaptation to pollinator preferences. Firstly, the lower osmolality of sucrose solutions means that they evaporate more rapidly than hexose solutions, which might be one reason why sucrose‐rich nectar is typically found in flowers with long tubes (adapted to long‐tongued pollinators), where it is better protected from evaporation than in open or short‐tubed flowers. Secondly, it can be assumed that temperature‐dependent evaporation is generally lower during the night than during the day so that selection pressure to secrete nectar with high osmolality (i.e. hexose‐rich solutions) is relaxed for night‐active flowers pollinated at night. Thirdly, the breeding system may affect selection pressure on nectar traits; that is, for pollinator‐independent, self‐pollinated plants, a lower selective pressure on nectar traits can be assumed, leading to a higher variability of nectar sugar composition independent of pollinator preferences, nectar accessibility and nectar protection. To analyse the relations between flower tube length, day vs. night pollination and self‐pollination, the nectar sugar composition was investigated in 78 European Caryophylloideae (Caryophyllaceae) with different pollination modes (diurnal, nocturnal, self‐pollination) using high‐performance liquid chromatography (HPLC). All Caryophylleae species (Dianthus and relatives) were found to have nectar with more than 50% sucrose, whereas the sugar composition of Sileneae species (Silene and relatives) ranged from 0% to 98.2%. In the genus Silene, a clear dichotomous distribution of sucrose‐ and hexose‐dominant nectars is evident. We found a positive correlation between the flower tube length and sucrose content in Caryophylloideae, particularly in day‐flowering species, using both conventional analyses and phylogenetically independent contrasts.