Pollen nutrition structures bee and plant community interactions.

As bees' main source of protein and lipids, pollen is critical for their development, reproduction, and health. Plant species vary considerably in the macronutrient content of their pollen, and research in bee model systems has established that this variation both modulates performance and guides floral choice. Yet, how variation in pollen chemistry shapes interactions between plants and bees in natural communities is an open question, essential for both understanding the nutritional dynamics of plant-pollinator mutualisms and informing their conservation. To fill this gap, we asked how pollen nutrition (relative protein and lipid content) sampled from 109 co-flowering plant species structured visitation patterns observed among 75 subgenera of pollen-collecting bees in the Great Basin/Eastern Sierra region (USA). We found that the degree of similarity in co-flowering plant species' pollen nutrition predicted similarity among their visitor communities, even after accounting for floral morphology and phylogeny. Consideration of pollen nutrition also shed light on the structure of this interaction network: Bee subgenera and plant genera were arranged into distinct, interconnected groups, delineated by differences in pollen macronutrient values, revealing potential nutritional niches. Importantly, variation in pollen nutrition alone (high in protein, high in lipid, or balanced) did not predict the diversity of bee visitors, indicating that plant species offering complementary pollen nutrition may be equally valuable in supporting bee diversity. Nutritional diversity should thus be a key consideration when selecting plants for habitat restoration, and a nutritionally explicit perspective is needed when considering reward systems involved in the community ecology of pollination.

Honey bees switch mechanisms to drink deep nectar efficiently.

The feeding mechanisms of animals constrain the spectrum of resources that they can exploit profitably. For floral nectar eaters, both corolla depth and nectar properties have marked influence on foraging choices. We report the multiple strategies used by honey bees to efficiently extract nectar at the range of sugar concentrations and corolla depths they face in nature. Honey bees can collect nectar by dipping their hairy tongues or capillary loading when lapping it, or they can attach the tongue to the wall of long corollas and directly suck the nectar along the tongue sides. The honey bee feeding apparatus is unveiled as a multifunctional tool that can switch between lapping and sucking nectar according to the instantaneous ingesting efficiency, which is determined by the interplay of nectar-mouth distance and sugar concentration. These versatile feeding mechanisms allow honey bees to extract nectar efficiently from a wider range of floral resources than previously appreciated and endow them with remarkable adaptability to diverse foraging environments.

The all-day pollinator visits of sunflower inflorescences in Helianthus annuus plantations are independent of head orientation: Testing a widespread hypothesis.

Mature inflorescences of sunflowers (Helianthus annuus) orient constantly on average to the geographical east. According to one of the explanations of this phenomenon, the eastward orientation of sunflower inflorescences increases the number of attracted insect pollinators. We tested this hypothesis in three field experiments performed in flowering sunflower plantations. In experiments 1 and 2 we measured the number of insects trapped by the vertical walls of sticky sunflower models facing north, east, south, and west. In experiment 3 we counted the pollinators' landings on real sunflower inflorescences facing naturally east or turned artificially toward north, south, and west. We found that the all-day number of pollinators (predominantly bees) attracted to model and real sunflowers in H. annuus plantations is independent of the azimuth direction of sunflower heads, and after 10 h in the morning, the average number of pollinators counted every 20 min is practically constant in the rest of the day.

The Extraordinary Alkali Bee, Nomia melanderi (Halictidae), the World's Only Intensively Managed Ground-Nesting Bee.

Among the ground-nesting bees are several proven crop pollinators, but only the alkali bee (Nomia melanderi) has been successfully managed. In <80 years, it has become the world's most intensely studied ground-nesting solitary bee. In many ways, the bee seems paradoxical. It nests during the torrid, parched midsummer amid arid valleys and basins of the western United States, yet it wants damp nesting soil. In these basins, extensive monocultures of an irrigated Eurasian crop plant, alfalfa (lucerne), subsidize millions of alkali bees. Elsewhere, its polylectic habits and long foraging range allow it to stray into neighboring crops contaminated with insecticides. Primary wild floral hosts are either non-native or poorly known. Kleptoparasitic bees plague most ground nesters, but not alkali bees, which do, however, host other well-studied parasitoids. Building effective nesting beds requires understanding the hydraulic conductivity of silty nesting soils and its important interplay with specific soil mineral salts. Surprisingly, some isolated populations endure inhospitably cold climates by nesting amid hot springs. Despite the peculiarities and challenges associated with its management, the alkali bee remains the second most valuable managed solitary bee for US agriculture and perhaps the world.

Patterns and drivers of heat production in the plant genus Amorphophallus.

Thermogenesis - the ability to generate metabolic heat - is much more common in animals than in plants, but it has been documented in several plant families, most prominently the Araceae. Metabolic heat is produced in floral organs during the flowering time (anthesis), with the hypothesised primary functions being to increase scent volatilisation for pollinator attraction, and/or to provide a heat reward for invertebrate pollinators. Despite in-depth studies on the thermogenesis of single species, no attempts have yet been made to examine plant thermogenesis across an entire clade. Here, we apply time-series clustering algorithms to 119 measurements of the full thermogenic patterns in inflorescences of 80 Amorphophallus species. We infer a new time-calibrated phylogeny of this genus and use phylogenetic comparative methods to investigate the evolutionary determinants of thermogenesis. We find striking phenotypic variation across the phylogeny, with heat production in multiple clades reaching up to 15°C, and in one case 21.7°C above ambient temperature. Our results show that the thermogenic capacity is phylogenetically conserved and is also associated with inflorescence thickness. Our study paves the way for further investigations of the eco-evolutionary benefits of thermogenesis in plants.

Putative Signals of Generalist Plant Species Adaptation to Local Pollinator Communities and Abiotic Factors.

The reproductive success of flowering plants with generalized pollination systems is influenced by interactions with a diverse pollinator community and abiotic factors. However, knowledge about the adaptative potential of plants to complex ecological networks and the underlying genetic mechanisms is still limited. Based on a pool-sequencing approach of 21 natural populations of Brassica incana in Southern Italy, we combined a genome-environmental association analysis with a genome scan for signals of population genomic differentiation to discover genetic variants associated with the ecological variation. We identified genomic regions putatively involved in the adaptation of B. incana to the identity of local pollinator functional categories and pollinator community composition. Interestingly, we observed several shared candidate genes associated with long-tongue bees, soil texture, and temperature variation. We established a genomic map of potential generalist flowering plant local adaptation to complex biotic interactions, and the importance of considering multiple environmental factors to describe the adaptive landscape of plant populations.

Multitrophic Higher-Order Interactions Modulate Species Persistence.

AbstractEcologists increasingly recognize that interactions between two species can be affected by the density of a third species. How these higher-order interactions (HOIs) affect species persistence remains poorly understood. To explore the effect of HOIs stemming from multiple trophic layers on a plant community composition, we experimentally built a mesocosm with three plants and three pollinator species arranged in a fully nested and modified network structure. We estimated pairwise interactions among plants and between plants and pollinators, as well as HOIs initiated by a plant or a pollinator affecting plant species pairs. Using a structuralist approach, we evaluated the consequences of the statistically supported HOIs on the persistence probability of each of the three competing plant species and their combinations. HOIs substantially redistribute the strength and sign of pairwise interactions between plant species, promoting the opportunities for multispecies communities to persist compared with a non-HOI scenario. However, the physical elimination of a plant-pollinator link in the modified network structure promotes changes in per capita pairwise interactions and HOIs, resulting in a single-species community. Our study provides empirical evidence of the joint importance of HOIs and network structure in determining species persistence within diverse communities.

Embryo recovery(rescue) studies in different Vitis species.

BACKROUND: In recent years, with the increasing demand for seedless grape varieties that have lower production costs, are disease resistant/tolerant and require less chemical pesticides, the embryo recovery technique has begun to be used more in table grape breeding studies. However, the desired high success rate has not yet been achieved in these studies. Although there are different reasons for this, especially the grape varieties selected for cross-breeding and the timing of transferring the embryos to medium are among the most important reasons. In this study, focusing on these two important factors, the embryos obtained from different hybridization combinations were transferred to agar medium at different weeks for 4 years and the most successful combination and time were determined. In addition, seedless and large berry grape varieties and some seeded varieties that are resistant/tolerant to fungal diseases were selected as parents because they can provide resistance to disease infections in vitro and thus increase the success rate. RESULTS: The results obtained from the study showed that the selected variety and combination significantly affected the success rate in embryo rescue. Especially in combinations with the 'Yalova Seedless' variety as the female parent, more successful results were obtained compared to combinations of other varieties. When 'Yalova Seedless' variety was pollinated with pollen of 'Red Globe', 'Muscat Bailey A' and 'Exalta' varieties, more seedlings were obtained with the help of embryo rescue. The results obtained over four years showed that the best sampling time after pollination was the eighth week and then the seventh week. CONCLUSIONS: According to the results obtained, it has been shown that the selected varieties and the sampling time significantly affect the success rate in embryo rescue studies. Therefore, higher success rates can be achieved in comprehensive breeding studies in which they will be included as pollinators, especially in different seeded varieties that are resistant to diseases and have larger berry size.

Genotypic variation in blueberry flower morphology and nectar reward content affects pollinator attraction in a diverse breeding population.

BACKGROUND: Pollination is crucial to obtaining optimal blueberry yield and fruit quality. Despite substantial investments in seasonal beekeeping services, blueberry producers consistently report suboptimal pollinator visitation and fruit set in some cultivars. Flower morphology and floral rewards are among the key factors that have shown to contribute to pollinator attraction, however little is known about their relative importance for improving yield in the context of plant breeding. Clarifying the relationships between flower morphology, nectar reward content, pollinator recruitment, and pollination outcomes, as well as their genetic components, can inform breeding priorities for enhancing blueberry production. In the present study, we measured ten flower and nectar traits and indices of successful pollination, including fruit set, seed count, and fruit weight in 38 southern highbush blueberry genotypes. Additionally, we assessed pollinator visitation frequency and foraging behavior over two growing seasons. Several statistical models were tested to optimize the prediction of pollinator visitation and pollination success, including partial least squares, BayesB, ridge-regression, and random forest. RESULTS: Random forest models obtained high predictive abilities for pollinator visitation frequency, with values of 0.54, 0.52, and 0.66 for honey bee, bumble bee, and total pollinator visits, respectively. The BayesB model provided the most consistent prediction of fruit set, fruit weight, and seed set, with predictive abilities of 0.07, -0.08, and 0.42, respectively. Variable importance analysis revealed that genotypic differences in nectar volume had the greatest impact on honey bee and bumble bee visitation, although preferences for flower morphological traits varied depending on the foraging task. Flower density was a major driving factor attracting nectar-foraging honey bees and bumble bees, while pollen-foraging bumble bees were most influenced by flower accessibility, specifically corolla length and the length-to-width ratio. CONCLUSIONS: Honey bees comprised the majority of pollinator visits, and were primarily influenced by nectar volume and flower density. Corolla length and the length-to-width ratio were also identified as the main predictors of fruit set, fruit weight, seed count, as well as pollen-foraging bumble bee visits, suggesting that these bees and their foraging preferences may play a pivotal role in fruit production. Moderate to high narrow-sense heritability values (ranging from 0.30 to 0.77) were obtained for all floral traits, indicating that selective breeding efforts may enhance cultivar attractiveness to pollinators.

Gardens reduce seasonal hunger gaps for farmland pollinators.

Gardens can benefit pollinators living in surrounding farmland landscapes, but the reason for their value is not clear. Gardens are no different from many semi-natural farmland habitats in terms of the quantity of floral resources (pollen and nectar) they produce, but the timing of their resource supply is very different, which may explain their value. We show that gardens provide 15% of overall annual nectar in farmland landscapes in Southwest UK, but between 50% and 95% during early spring and late summer when farmland supplies are low. Gardens can therefore reduce seasonal nectar gaps experienced by farmland bumblebees. Consistent with this pattern, bumblebee activity increased in gardens relative to farmland during early spring and late summer. An agent-based model reinforces this point, showing that timing, not quantity, of garden nectar supply enhances bumblebee colony growth and survival in farmland. We show that over 90% of farmland in Great Britain is within 1 km of a garden and therefore positive actions by gardeners could have widespread spillover benefits for pollinators across the country. Given the widespread distribution of gardens around the world, we highlight their important interplay with surrounding landscapes for pollinator ecology and conservation.

The potential for evolutionary rescue in an Arctic seashore plant threatened by climate change.

The impacts of climate change may be particularly severe for geographically isolated populations, which must adjust through plastic responses or evolve. Here, we study an endangered Arctic plant, Primula nutans ssp. finmarchica, confined to Fennoscandian seashores and showing indications of maladaptation to warming climate. We evaluate the potential of these populations to evolve to facilitate survival in the rapidly warming Arctic (i.e. evolutionary rescue) by utilizing manual crossing experiments in a nested half-sibling breeding design. We estimate G-matrices, evolvability and genetic constraints in traits with potentially conflicting selection pressures. To explicitly evaluate the potential for climate change adaptation, we infer the expected time to evolve from a northern to a southern phenotype under different selection scenarios, using demographic and climatic data to relate expected evolutionary rates to projected rates of climate change. Our results indicate that, given the nearly 10-fold greater evolvability of vegetative than of floral traits, adaptation in these traits may take place nearly in concert with changing climate, given effective climate mitigation. However, the comparatively slow expected evolutionary modification of floral traits may hamper the evolution of floral traits to track climate-induced changes in pollination environment, compromising sexual reproduction and thus reducing the likelihood of evolutionary rescue.

Body-size-dependent effects of landscape-level resource energetics on pollinator abundance in woodland remnants.

Land use change alters floral resource availability, thereby contributing to declines in important pollinators. However, the severity of land use impact varies by species, influenced by factors such as dispersal ability and resource specialization, both of which can correlate with body size. Here. we test whether floral resource availability in the surrounding landscape (the 'matrix') influences bee species' abundance in isolated remnant woodlands, and whether this effect varies with body size. We sampled quantitative flower-visitation networks within woodland remnants and quantified floral energy resources (nectar and pollen calories) available to each bee species both within the woodland and the matrix. Bee abundance in woodland increased with floral energy resources in the surrounding matrix, with strongest effects on larger-bodied species. Our findings suggest important but size-dependent effects of declining matrix floral resources on the persistence of bees in remnant woodlands, highlighting the need to incorporate landscape-level floral resources in conservation planning for pollinators in threatened natural habitats.

A century of wild bee sampling: historical data and neural network analysis reveal ecological traits associated with species loss.

We analysed the wild bee community sampled from 1921 to 2018 at a nature preserve in southern Michigan, USA, to study long-term community shifts in a protected area. During an intensive survey in 1972 and 1973, Francis C. Evans detected 135 bee species. In the most recent intensive surveys conducted in 2017 and 2018, we recorded 90 species. Only 58 species were recorded in both sampling periods, indicating a significant shift in the bee community. We found that the bee community diversity, species richness and evenness were all lower in recent samples. Additionally, 64% of the more common species exhibited a more than 30% decline in relative abundance. Neural network analysis of species traits revealed that extirpation from the reserve was most likely for oligolectic ground-nesting bees and kleptoparasitic bees, whereas polylectic cavity-nesting bees were more likely to persist. Having longer phenological ranges also increased the chance of persistence in polylectic species. Further analysis suggests a climate response as bees in the contemporary sampling period had a more southerly overall distribution compared to the historic community. Results exhibit the utility of both long-term data and machine learning in disentangling complex indicators of bee population trajectories.

Flower-bee versus pollen-bee metanetworks in fragmented landscapes.

Understanding the organization of mutualistic networks at multiple spatial scales is key to ensure biological conservation and functionality in human-modified ecosystems. Yet, how changing habitat and landscape features affect pollen-bee interaction networks is still poorly understood. Here, we analysed how bee-flower visitation and bee-pollen-transport interactions respond to habitat fragmentation at the local network and regional metanetwork scales, combining data from 29 fragments of calcareous grasslands, an endangered biodiversity hotspot in central Europe. We found that only 37% of the total unique pairwise species interactions occurred in both pollen-transport and flower visitation networks, whereas 28% and 35% were exclusive to pollen-transport and flower visitation networks, respectively. At local level, network specialization was higher in pollen-transport networks, and was negatively related to the diversity of land cover types in both network types. At metanetwork level, pollen transport data revealed that the proportion of single-fragment interactions increased with landscape diversity. Our results show that the specialization of calcareous grasslands' plant-pollinator networks decreases with landscape diversity, but network specialization is underestimated when only based on flower visitation information. Pollen transport data, more than flower visitation, and multi-scale analyses of metanetworks are fundamental for understanding plant-pollinator interactions in human-dominated landscapes.

Floral scent changes in response to pollen removal are rare in buzz-pollinated Solanum.

MAIN CONCLUSION: One of seven Solanum taxa studied displayed associations between pollen presence and floral scent composition and volume, suggesting buzz-pollinated plants rarely use scent as an honest cue for foraging pollinators. Floral scent influences the recruitment, learning, and behaviour of floral visitors. Variation in floral scent can provide information on the amount of reward available or whether a flower has been visited recently and may be particularly important in species with visually concealed rewards. In many buzz-pollinated flowers, tubular anthers opening via small apical pores (poricidal anthers) visually conceal pollen and appear similar regardless of pollen quantity within the anther. We investigated whether pollen removal changes floral scent composition and emission rate in seven taxa of buzz-pollinated Solanum (Solanaceae). We found that pollen removal reduced both the overall emission of floral scent and the emission of specific compounds (linalool and farnesol) in S. lumholtzianum. Our findings suggest that in six out of seven buzz-pollinated taxa studied here, floral scent could not be used as a signal by visitors as it does not contain information on pollen availability.

The absence of bumblebees on an oceanic island blurs the species boundary of two closely related orchids.

Oceanic islands offer valuable natural laboratories for studying evolution. The Izu Islands, with their recent geological origin, provide an exceptional opportunity to explore the initial evolution on oceanic islands. Another noteworthy aspect is the absence of bumblebee species on most Izu Islands. We used ecological, morphological, and molecular data to investigate the impact of bumblebee absence on the evolution of two closely related orchid species, Goodyera henryi and Goodyera similis, focusing on Kozu Island, the Izu Islands. Our investigation revealed that while G. henryi exclusively relies on a bumblebee species for pollination on the mainland, G. similis is pollinated by scoliid wasps on both the mainland and the island. Intriguingly, all specimens initially categorized as G. henryi on Kozu Island are hybrids of G. henryi and G. similis, leading to the absence of pure G. henryi distribution on the island. These hybrids are pollinated by the scoliid wasp species that also pollinates G. similis on the island. The absence of bumblebees might result in sporadic and inefficient pollination of G. henryi by scoliid wasps, consequently promoting hybrid proliferation on the island. Our findings suggest that the absence of bumblebees can blur plant species boundaries.

Sexually concordant selection on floral traits despite greater opportunity for selection through male fitness.

Pollinators are important drivers of floral trait evolution, yet plant populations are not always perfectly adapted to their pollinators. Such apparent maladaptation may result from conflicting selection through male and female sexual functions in hermaphrodites. We studied sex-specific mating patterns and phenotypic selection on floral traits in Aconitum gymnandrum. After genotyping 1786 offspring, we partitioned individual fitness into sex-specific selfed and outcrossed components and estimated phenotypic selection acting through each. Relative fitness increased with increasing mate number, and more so for male function. This led to greater opportunity for selection through outcrossed male fitness, though patterns of phenotypic selection on floral traits tended to be similar, and with better support for selection through female rather than male fitness components. We detected directional selection through one or more fitness component for larger flower number, larger flowers, and more negative nectar gradients within inflorescences. Our results are consistent with Bateman's principles for sex-specific mating patterns and illustrate that, despite the expected difference in opportunity for selection, patterns of variation in selection across traits can be rather similar for the male and female sexual functions. These results shed new light on the effect of sexual selection on the evolution of floral traits.

A multifunctional role for riboflavin in the yellow nectar of Capsicum baccatum and Capsicum pubescens.

A few Capsicum (pepper) species produce yellow-colored floral nectar, but the chemical identity and biological function of the yellow pigment are unknown. A combination of analytical biochemistry techniques was used to identify the pigment that gives Capsicum baccatum and Capsicum pubescens nectars their yellow color. Microbial growth assays, visual modeling, and honey bee preference tests for artificial nectars containing riboflavin were used to assess potential biological roles for the nectar pigment. High concentrations of riboflavin (vitamin B2) give the nectars their intense yellow color. Nectars containing riboflavin generate reactive oxygen species when exposed to light and reduce microbial growth. Visual modeling also indicates that the yellow color is highly conspicuous to bees within the context of the flower. Lastly, field experiments demonstrate that honey bees prefer artificial nectars containing riboflavin. Some Capsicum nectars contain a yellow-colored vitamin that appears to play roles in (1) limiting microbial growth, (2) the visual attraction of bees, and (3) as a reward to nectar-feeding flower visitors (potential pollinators), which is especially interesting since riboflavin is an essential nutrient for brood rearing in insects. These results cumulatively suggest that the riboflavin found in some Capsicum nectars has several functions.

Quantifying the production of plant pollen at the farm scale.

Plant pollen is rich in protein, sterols and lipids, providing crucial nutrition for many pollinators. However, we know very little about the quantity, quality and timing of pollen availability in real landscapes, limiting our ability to improve food supply for pollinators. We quantify the floral longevity and pollen production of a whole plant community for the first time, enabling us to calculate daily pollen availability. We combine these data with floral abundance and nectar measures from UK farmland to quantify pollen and nectar production at the landscape scale throughout the year. Pollen and nectar production were significantly correlated at the floral unit, and landscape level. The species providing the highest quantity of pollen on farmland were Salix spp. (38%), Filipendula ulmaria (14%), Rubus fruticosus (10%) and Taraxacum officinale (9%). Hedgerows were the most pollen-rich habitats, but permanent pasture provided the majority of pollen at the landscape scale, because of its large area. Pollen and nectar were closely associated in their phenology, with both peaking in late April, before declining steeply in June and remaining low throughout the year. Our data provide a starting point for including pollen in floral resource assessments and ensuring the nutritional requirements of pollinators are met in farmland landscapes.

Manipulation of soil mycorrhizal fungi influences floral traits.

Most plants form root hyphal relationships with mycorrhizal fungi, especially arbuscular mycorrhizal fungi (AMF). These associations are known to positively impact plant biomass and competitive ability. However, less is known about how mycorrhizas impact other ecological interactions, such as those mediated by pollinators. We performed a meta-regression of studies that manipulated AMF and measured traits related to pollination, including floral display size, rewards, visitation, and reproduction, extracting 63 studies with 423 effects. On average, the presence of mycorrhizas was associated with positive effects on floral traits. Specifically, we found impacts of AMF on floral display size, pollinator visitation and reproduction, and a positive but nonsignificant impact on rewards. Studies manipulating mycorrhizas with fungicide tended to report contrasting results, possibly because fungicide destroys both beneficial and pathogenic microbes. Our study highlights the potential for relationships with mycorrhizal fungi to play an important, yet underrecognized role in plant-pollinator interactions. With heightened awareness of the need for a more sustainable agricultural industry, mycorrhizal fungi may offer the opportunity to reduce reliance on inorganic fertilizers. At the same time, fungicides are now ubiquitous in agricultural systems. Our study demonstrates indirect ways in which plant-belowground fungal partnerships could manifest in plant-pollinator interactions.