A functional view reveals substantial predictability of pollinator-mediated selection

A predictive understanding of adaptation to changing environments hinges on a mechanistic understanding of the extent and causes of variation in natural selection. Estimating variation in selection is difficult due to the complex relationships between phenotypic traits and fitness, and the uncertainty associated with individual selection estimates. Plant-pollinator interactions provide ideal systems for understanding variation in selection and its predictability, because both the selective agents (pollinators) and the process linking phenotypes to fitness (pollination) are generally known. Through examples from the pollination literature, I discuss how explicit consideration of the functional mechanisms underlying trait-performance relationships can clarify the relationship between traits and fitness, and how variation in the ecological context that generates selection can help disentangle biologically important variation in selection from sampling variation. I then evaluate the predictability of variation in pollinator-mediated selection through a survey, reanalysis, and synthesis of results from the literature. The synthesis demonstrates that pollinator-mediated selection often varies substantially among trait functional groups, as well as in time and space. Covariance between patterns of selection and ecological variables provides additional support for the biological importance of observed selection, but the detection of such covariance depends on careful choice of relevant predictor variables as well as consideration of quantitative measurements and their meaning, an aspect often neglected in selection studies.

Sending private messages: Floral ultraviolet signals are correlated with pollination syndromes in Erica

The presence of ultraviolet (UV, wavelengths between 300-400 nm) reflectance in insect-pollinated flowers has been linked to pollination efficiency and pollination shifts, but little is known about its prevalence and function in other pollination systems and African species. We chose the genus Erica for studying the prevalence of UV because of its extreme radiation (c. 680 species) in the Cape, South Africa, with a diversity of pollination syndromes. This study quantified the prevalence and brightness of UV reflectance for five Erica pollination syndromes and tested pollinator preferences for UV reflectance in the two groups with the highest prevalence: sunbirds and long-proboscid flies. Our results show that UV colouration is absent or rare in Erica species pollinated by unclassified insects, rodents or wind. About 17 % of bird-pollinated species reflected UV but choice experiments revealed that free-ranging sunbirds showed no preference for UV signals. All sampled long-proboscid fly-pollinated species reflected UV and its experimental removal decreased seed set drastically, suggesting that long-proboscid flies in the Cape strongly prefer or depend on UV and thereby contributed to selecting for the evolution of this signal.

Catching the thief: Nectar robbing behaviour by bumblebees on naturalised Fuchsia magellanica in Ireland

Fuchsia magellanica (Ongaraceae) is a plant with a traditionally ornithopholous pollination system, pollinated primarily by hummingbirds in its native range. As a naturalised alien plant in Ireland, F. magellanica is visited largely by bumblebees, with evidence for nectar robbing behaviour of the long-tubed flowers. We aimed to investigate nectar robbing behaviour of bumblebees on F. magellanica, and in particular whether floral and pollinator traits (size) determined likelihood of nectar robbing. While F. magellanica was visited by a number of bumblebee species, only two with shorter tongue lengths were observed to rob nectar from flowers. Although there was no observed relationship between intra-specific bee body size and nectar robbing behaviour, nectar robbing was observed most frequently in the site with the highest number of bees. Proportions of robbed flowers were low overall and varied between populations, but there was a significant relationship between flower size and whether it was nectar robbed with larger flowers robbed more often. Our work suggests that floral size determines whether a flower-visitor will choose to nectar rob or not in this system. Nectar robbing may also be related to bee density which could suggest this behaviour is driven by competition for resources, or that it is learnt by observing other bees.

The importance of wild bee communities as urban pollinators and the influence of honeybee hive density

While urban beekeeping is on the rise, data on the role of wild bee communities as crop pollinators in cities is still scarce. We analysed wild bee visitation rates on apple, plum, cherry, pear, blackberry, raspberry, and strawberry in a Bavarian city with a very high honeybee density of c. 19 hives/km2. During 137.5 hours of observation time, we observed 52 wild bee species on the studied crop plants. During more than 50 h of observation time on fruit trees in flower, we found that wild bees provided 41% of the total bee visits, honeybees the remaining 59%. Honeybee hive density had a significantly negative effect on wild bee abundance. Bumblebees appeared more tolerant to poor weather conditions than all other bee groups. Wild bee species richness on apple flowers was not significantly impacted by flower diversity in the surroundings of the trees. Together, our results suggest that species-rich wild bee communities in urban areas are important for pollination success in common fruit crops, especially under unstable spring weather conditions. Bee-friendly management of urban spaces should be prioritised to support wild bee communities as well as the increasing number of honeybees in cities.

Consequences of the high abundance of Bombus terrestris on the pollination of Vicia faba

One of the main visitors to Fabia bean crops (Vicia faba) in South America is the invasive bumblebee species Bombus terrestris. This is particularly true in Chile, where B. terrestris was first introduced in 1997 and is now common over much of the country. In this study, we evaluated the activity of the principal pollinators of V. faba over two cropping seasons by assessing their visitation rates while distinguishing between legitimate visits, likely to lead to pollination, and nectar robbery. We then determined the net contribution of insect visitation on pod and seed set. We recorded seven species of floral visitors. Most visits (legitimate visits and robbery) were from the honeybee (Apis mellifera), with B. terrestris being the next most common visitor. In the case of B. terrestris, 87.19% of visits were nectar robbery. On average, the same flower perforation was visited 23 times by B. terrestris during the flower's lifespan. In general, the frequency of legitimate visits varied with pollinator identity and year. For B. terrestris, each flower received an average of 0.95 legitimate visits during its entire lifespan. The time spent by B. terrestris visiting flowers for both nectar robbery or pollen collection decreased after the first day of flowering suggesting resource depletion. The number of pods, total seed number, and seed weight were lower where self rather than open pollination. This suggests that open pollination increased reproductive success. We conclude that B. terrestris was likely to contribute relatively little to pollination while at the same time depleting floral resources throughout the flowers’ lifespan.

Testing for apomixis in an obligate pollination mutualism

Plants with a small number of specific pollinators may be vulnerable to fluctuations in the availability of those pollinators, which could limit plant reproductive success and even result in extinction. Plants can develop mechanisms to mitigate this risk, such as apomixis. Reproductive assurance mechanisms have been largely ignored in obligate pollination mutualisms (OPMs), that are some of the most specialised of plant-pollinator interactions. Furthermore, although OPMs are often referred to as obligate, this is rarely tested. We performed a flower-bagging experiment to test if the unisexual flowers of Breynia oblongifolia could set fruit in the absence of its highly specialised seed-eating moth pollinators. Surprisingly, many bagged female flowers developed fruits, suggesting apomixis. We therefore conducted a second series of experiments in which we 1) added or excluded pollinators from caged plants; and 2) surveyed a wild population for apomictic reproduction using mother-offspring genotyping. In the absence of pollinators, no fruits developed. In addition, we detected no genetic evidence for apomixis when comparing between mothers and their offspring or between adults in a wild population. We explain the production of fruits in bagged branches by our discovery that B. oblongifolia can retain pollinated female flowers over the winter period. These flowers develop to fruits in the spring in the absence of male flowers or pollinators. Our study thus shows that B. oblongifolia is unable to produce fruit in the absence of its specialist moth pollinators. Thus, the highly specific interaction between plant and pollinators appears to be truly obligate.

An updated insect exclosure design for pollination ecology

Exclosures are a common method for quantifying the effects of animal pollinators on flowering plant species. However, a lack of standardized designs or clear descriptions of previously implemented exclosure designs decreases replicability in pollination studies and reduces scientific rigor. We summarized previous descriptions of pollination exclosure designs, and developed/tested a novel exclosure design in alpine environments on the Beartooth Plateau in northern Wyoming, USA. This exclosure design consists of a cylindrical internal wire frame, integrated ground stakes, and various mesh materials attached to the exterior. Exclosures on the plateau showed high efficacy in inhibiting insects from pollinating flowering plants, and nearly all of these exclosures remained functional throughout the time they were in place. Our updated exclosure design is effective, inexpensive, easy to produce, and widely applicable across differing ecosystems and experimental design types.

Open-top warming chambers reduce animal pollination of two subalpine herbs

Open top chambers (OTCs) are a popular method for studying the biological effects of climate change through passive heating, but their effects on biotic interactions are poorly understood, especially for pollination. Here we use the subalpine plants Delphinium nuttallianum and Potentilla pulcherrima to examine the possibility that the effects of OTCs on plant reproduction are not the result of warming but rather OTCs acting as barriers to pollinator movement. Pollinator observations were conducted and stigmas collected from plants inside and outside of OTCs in a meadow in the Rocky Mountains of Colorado, USA. Very few visitors were observed inside of OTCs, which led to severe reductions in visitation rates, by 92% in Delphinium and 85% in Potentilla. The number of conspecific pollen grains on stigmas was 73% lower in OTCs for Delphinium but not Potentilla, likely because it is capable of autogamous self-pollination. This study clearly shows that OTCs can reduce animal pollination, which is also likely to reduce plant reproductive output of outcrossing plants via decreases in the quantity or quality of pollen. OTCs may therefore confound effects of warming on plant reproduction with pollination effects. Although the unintended effects of OTCs on abiotic conditions are well-studied, this study highlights that their effects on biotic interactions require further investigation.

Plant phylogeny as a major predictor of flower visitation by nitidulid beetles, a lineage of ancestral angiosperm pollinators

Plant phylogeny sometimes predicts interspecific variation in pollinator composition better than floral features, and its predictive value seems to differ among major groups of insect pollinators. Earlier findings suggesting that pollination by Plant phylogeny sometimes predicts interspecific variation in pollinator composition better than gross floral features, and its predictive value seems to differ among major groups of insect pollinators. Pollination by beetles exhibits the strongest phylogenetic signal and the strongest phylogenetic conservatism, which is particularly intriguing given that beetles were probably the pollinators of early angiosperms. We examine in this paper the relationship between plant phylogeny and flower visitation by nitidulid beetles (Coleoptera: Nitidulidae), an old monophyletic group of flower specialists and pollinators of gymnosperms and angiosperms. Using quantitative data on pollinator composition for 251 plant species (belonging to 167 genera in 46 families) from well-preserved Mediterranean montane habitats from southeastern Spain, the following questions were addressed: Is pollination by nitidulids correlated with plant phylogeny in the large species sample studied, and if it does, which are the relative importances of plant phylogeny, floral characteristics, and environmental features as predictors of nitidulid pollination in the plant assemblage studied ? Nitidulids were recorded in flowers of 25% of the plant species considered. Their distribution was significantly related to plant phylogeny, being clustered on certain lineages (Ranunculales, Malvales, Rosales, Asterales) and remarkably absent from others (e.g., Fabales, Lamiales). None of the environmental (habitat type, elevation) or macroscopic floral features considered (perianth type and color, flower mass) predicted nitidulid visitation after statistically accounting for the effect of plant phylogeny. We theorize that nitidulid beetles use characters of plants that track plant phylogeny at least as deep as the early radiation of the eudicots, imaginably characters such as the chemical signatures of pollen.

Pollination and nectar larceny by birds and bees in novel forests of the Hawaiian Islands

The extinction of native species and introduction of non-native species may lead to the disruption of biotic interactions. Pollination is a critical ecosystem process that often requires mutualisms between animals and plants. Non-native animals may interact with native flowering plants, with the potential to pollinate or steal nectar (larceny) from flowers without pollination. In the Hawaiian Islands, many native plants have lost their original pollinators. Birds and insects are known to visit native plant flowers, but it is unclear whether they pollinate or steal nectar, whether native and non-native species differ in their interactions with flowers, and what influences visitation to flowers. On Oʻahu, we deployed camera traps and conducted in-person observations on four at-risk species of Hawaiian lobelioids (Campanulaceae). We observed birds, mammals, and insects visiting flowers, with a native bird and native bee visiting most frequently. Regardless of native versus non-native status, bees made contact with reproductive structures during most visits (90.5% of visits), while birds stole nectar during most visits (99.3% of visits). Bee and bird visitation increased with the number of flowers on focal plants. Bird visitation also increased with canopy cover and the number of nearby conspecific flowers and decreased with the number of nearby heterospecific flowers. Our results indicate that bees may pollinate plants that were historically bird-pollinated, while native and non-native birds have neutral or negative impacts on these plants. Broadly, we contribute to an understanding of how native plant pollination can be altered in changing ecosystems.