Predation risk and floral rewards: How pollinators balance these conflicts and the consequences on plant fitness.

Foraging behavior of pollinators is shaped by, among other factors, the conflict between maximizing resource intake and minimizing predation risk; yet, empirical studies quantifying variation in both forces are rare, compared to those investigating each separately. Here, we discuss the importance of simultaneously assessing bottom-up and top-down forces in the study of plant-pollinator interactions, and propose a conceptual and testable graphical hypothesis for pollinator foraging behavior and plant fitness outcomes as a function of varying floral rewards and predation risk. In low predation risk scenarios, no noticeable changes in pollinator foraging behavior are expected, with reward levels affecting only the activity threshold. However, as predation risk increases we propose that there is a decrease in foraging behavior, with a steeper decline as plants are more rewarding and profitable. Lastly, in high predation risk scenarios, we expect foraging to approach zero, regardless of floral rewards. Thus, we propose that pollinator foraging behavior follows an inverse S-shape curve, with more pronounced changes in foraging activity at intermediate levels of predation risk, especially in high reward systems. We present empirical evidence that is consistent with this hypothesis. In terms of the consequences for plant fitness, we propose that specialized plant-pollinator systems should be more vulnerable to increased predation risk, with a steeper and faster decline in plant fitness, compared with generalist systems, in which pollinator redundancy can delay or buffer the effect of predators. Moreover, whereas we expect that specialist systems follows a similar inverse S-shape curve, in generalist systems we propose three different scenarios as a function not only of reward level but also compatibility, mating-system, and the interplay between growth form and floral display. The incorporation of trade-offs in pollinator behavior balancing the conflicting demands between feeding and predation risk has a promising future as a key feature enabling the development of more complex foraging models.

Floral trait variation across individual plants within a population enhances defense capability to nectar robbing.

Floral trait variation may help pollinators and nectar robbers identify their target plants and, thus, lead to differential selection pressure for defense capability against floral antagonists. However, the effect of floral trait variation among individuals within a population on multi-dimensional plant-animal interactions has been little explored. We investigated floral trait variation, pollination, and nectar robbing among individual plants in a population of the bumble bee-pollinated plant, Caryopteris divaricata, from which flowers are also robbed by bumble bees with varying intensity across individuals. We measured the variation in corolla tube length, nectar volume and sugar concentration among individual plants, and evaluated whether the variation were recognized by pollinators and robbers. We investigated the influence of nectar robbing on legitimate visitation and seed production per fruit. We found that the primary nectar robber (Bombus nobilis) preferred to forage on plants with long-tubed flowers, which produced less nectar and had lower sugar concentration compared to those with shorter corolla tubes. Individuals with shorter corolla tubes had comparatively lower nectar robbing intensity but higher visitation by legitimate visitors (mainly B. picipes) and higher seed production. Nectar robbing significantly reduced seed production because it decreased pollinator visits. However, neither pollination nor seed production differed between plants with long and short corolla tubes when nectar robbers were excluded. This finding suggests that floral trait variation might not be driven by pollinators. Such variation among individual plants thus allows legitimate visitors and nectar robbers to segregate niches and enhances population defense against nectar robbing in unpredictable conditions.

The effects of urbanization on pollinators and pollination: A meta-analysis.

Urbanization is increasing worldwide, with major impacts on biodiversity, species interactions and ecosystem functioning. Pollination is an ecosystem function vital for terrestrial ecosystems and food security; however, the processes underlying the patterns of pollinator diversity and the ecosystem services they provide in cities have seldom been quantified. Here, we perform a comprehensive meta-analysis of 133 studies examining the effects of urbanization on pollinators and pollination. Our results confirm the widespread negative impacts of urbanization on pollinator richness and abundance, with Lepidoptera being the most affected group. Furthermore, pollinator responses were found to be trait-specific, with below-ground nesting and solitary Hymenoptera, and spring flyers more severely affected by urbanization. Meanwhile, cities promote non-native pollinators, which may exacerbate conservation risks to native species. Surprisingly, despite the negative effects of urbanization on pollinator diversity, pollination service measured as seed set is enhanced in non-tropical cities likely due to abundant generalists and managed pollinators therein. We emphasize that the richness of local flowering plants could mitigate the negative impacts of urbanization on pollinator diversity. Overall, the results demonstrate the varying magnitudes of multiple moderators on urban pollinators and pollination services and could help guide conservation actions for biodiversity and ecosystem function for a sustainable future.

A global meta-analysis reveals contrasting impacts of air, light, and noise pollution on pollination.

In the face of biodiversity decline, understanding the impact of anthropogenic disturbances on ecosystem functions is critical for mitigation. Elevated levels of pollution are a major threat to biodiversity, yet there is no synthesis of their impact on many of the major ecosystem functions, including pollination. This ecosystem function is both particularly vulnerable as it depends on the fine-tuned interaction between plants and pollinators and hugely important as it underpins the flora of most habitats as well as food production. Here, we untangle the impact of air, light, and noise pollution on the pollination system by systematically evaluating and synthesizing the published evidence via a meta-analysis. We identified 58 peer-reviewed articles from three databases. Mixed-effects meta-regression models indicated that air pollution negatively impacts pollination. However, there was no effect of light pollution, despite previous studies that concentrated solely on pollinators suggesting a negative impact. Evidence for noise pollution was extremely limited. Unless action is taken to tackle air pollution, the capacity to support well-functioning diverse pollination systems will be compromised, with negative consequences for habitat conservation and food security.

Effects of ambient climate and three warming treatments on fruit production in an alpine, subarctic meadow community.

PREMISE: Climate change is having major impacts on alpine and arctic regions, and inter-annual variations in temperature are likely to increase. How increased climate variability will impact plant reproduction is unclear. METHODS: In a 4-year study on fruit production by an alpine plant community in northern Sweden, we applied three warming regimes: (1) a static level of warming with open-top chambers (OTC), (2) press warming, a yearly stepwise increase in warming, and (3) pulse warming, a single-year pulse event of higher warming. We analyzed the relationship between fruit production and monthly temperatures during the budding period, fruiting period, and whole fruit production period and the effect of winter and summer precipitation on fruit production. RESULTS: Year and treatment had a significant effect on total fruit production by evergreen shrubs, Cassiope tetragona, and Dryas octopetala, with large variations between treatments and years. Year, but not treatment, had a significant effect on deciduous shrubs and graminoids, both of which increased fruit production over the 4 years, while forbs were negatively affected by the press warming, but not by year. Fruit production was influenced by ambient temperature during the previous-year budding period, current-year fruiting period, and whole fruit production period. Minimum and average temperatures were more important than maximum temperature. In general, fruit production was negatively correlated with increased precipitation. CONCLUSIONS: These results indicate that predicted increased climate variability and increased precipitation due to climate change may affect plant reproductive output and long-term community dynamics in alpine meadow communities.

Broader phenology of pollinator activity and higher plant reproductive success in an urban habitat compared to a rural one.

Urban habitat characteristics create environmental filtering of pollinator communities. They also impact pollinating insect phenology through the presence of an urban heat island and the year-round availability of floral resources provided by ornamental plants.Here, we monitored the phenology and composition of pollinating insect communities visiting replicates of an experimental plant assemblage comprising two species, with contrasting floral traits: Sinapis alba and Lotus corniculatus, whose flowering periods were artificially extended. Plant assemblage replicates were set up over two consecutive years in two different habitats: rural and densely urbanized, within the same biogeographical region (Ile-de-France region, France).The phenology of pollination activity, recorded from the beginning (early March) to the end (early November) of the season, differed between these two habitats. Several pollinator morphogroups (small wild bees, bumblebees, honeybees) were significantly more active on our plant sets in the urban habitat compared to the rural one, especially in early spring and autumn. This resulted in different overall reproductive success of the plant assemblage between the two habitats. Over the course of the season, reproductive success of S. alba was always significantly higher in the urban habitat, while reproductive success of L. corniculatus was significantly higher in the urban habitat only during early flowering.These findings suggest different phenological adaptations to the urban habitat for different groups of pollinators. Overall, results indicate that the broadened activity period of pollinating insects recorded in the urban environment could enhance the pollination function and the reproductive success of plant communities in cities.

Floral asymmetry and predation risk modify pollinator behavior, but only predation risk decreases plant fitness.

Although predators and floral herbivores can potentially decrease plant fitness by changing pollinator behaviors, studies comparing the strength of these factors as well as their additive and interactive effects on pollinator visitation and plant fitness have not been conducted. In this study, we manipulated the floral symmetry and predator presence (artificial crab spiders) on the flowers of the shrub Rubus rosifolius (Rosaceae) in a 2 × 2 factorial randomized block design. We found that asymmetry and predators decreased pollinator visitation (mainly hymenopterans), and overall these factors did not interact (additive effects). The effect of predation risk on pollinator avoidance behavior was 62 % higher than that of floral asymmetry. Furthermore, path analyses revealed that only predation risk cascaded down to plant fitness, and it significantly decreased fruit biomass by 33 % and seed number by 28 %. We also demonstrated that R. rosifolius fitness is indirectly affected by visiting and avoidance behaviors of pollinators. The strong avoidance behavioral response triggered by predation risk may be related to predator pressure upon flowers. Although floral asymmetry caused by herbivory can alter the quality of resources, it should not exert the same evolutionary pressure as that of predator-prey interactions. Our study highlights the importance of considering simultaneous forces, such as predation risk and floral asymmetry, as well as pollinator behavior when evaluating ecological processes involving mutualistic plant-pollinator systems.

Novel interactions of non-pollinating ants with pollinators and fruit consumers in a tropical forest.

The tropical ants Ectatomma ruidum and E. tuberculatum (Formicidae) regularly patrol leaves, flowers, and fruits of the understory shrub, Psychotria limonensis (Rubiaceae), on Barro Colorado Island, Panama. Ant and pollinator exclusion experiments elucidated both positive and negative effects of ant attendance on plant reproductive success, including pollination, fruit set, fruit loss, and fruit removal. Ants did not pollinate flowers but did contribute to higher pollination success, probably by increasing the relocation frequency of winged pollinators and thus the rate of flower visitation. Ants also prevented fruit loss to herbivorous insects which were common during the early stages of fruit development. Thus, ant attendance strongly improved both pollination and fruit set whereby plants with ants set more fruit per flower and also lost fewer fruits during fruit maturation. In contrast, ants had a negative effect on the removal of ripe fruits by avian frugivores. Thus, ant attendance has a non-trivial influence on plant reproduction, this interaction being beneficial at some stages of the plant reproductive cycle and carrying costs at another stage. A tight ecological or co-evolved relationship between these Ectatomma spp. and P. limonensis is unlikely given that ant attendance of plants is detrimental to fruit removal.