Honeybees disrupt the structure and functionality of plant-pollinator networks.

The honeybee is the primary managed species worldwide for both crop pollination and honey production. Owing to beekeeping activity, its high relative abundance potentially affects the structure and functioning of pollination networks in natural ecosystems. Given that evidences about beekeeping impacts are restricted to observational studies of specific species and theoretical simulations, we still lack experimental data to test for their larger-scale impacts on biodiversity. Here we used a three-year field experiment in a natural ecosystem to compare the effects of pre- and post-establishment stages of beehives on the pollination network structure and plant reproductive success. Our results show that beekeeping reduces the diversity of wild pollinators and interaction links in the pollination networks. It disrupts their hierarchical structural organization causing the loss of interactions by generalist species, and also impairs pollination services by wild pollinators through reducing the reproductive success of those plant species highly visited by honeybees. High-density beekeeping in natural areas appears to have lasting, more serious negative impacts on biodiversity than was previously assumed.

Functional consequences of plant-animal interactions along the mutualism-antagonism gradient.

Plant-animal interactions are pivotal for ecosystem functioning, and usually form complex networks involving multiple species of mutualists as well as antagonists. The costs and benefits of these interactions show a strong context-dependency directly related to individual variation in partner identity and differential strength. Yet understanding the context-dependency and functional consequences of mutualistic and antagonistic interactions on individuals remains a lasting challenge. We use a network approach to characterize the individual, plant-based pollination interaction networks of the Canarian Isoplexis canariensis (Plantaginaceae) with a mixed assemblage of vertebrate mutualists (birds and lizards) and invertebrate antagonists (florivores, nectar larcenists, and predispersal seed predators). We identify and quantify interaction typologies based on the sign (mutualistic vs. antagonistic) and strength (weak vs. strong) of animal-mediated pollination and test the relationship with individual female reproductive success (FRS). In addition, we document pollinator movement patterns among individual plants to infer events of pollen transfer/receipt that define the plant mating networks and test the relationship with FRS. We identify six interaction typologies along a mutualism-antagonism gradient, with two typologies being over-represented involving both mutualists and antagonists and influencing FRS. Plants showing strong mutualistic interactions, but also (weak or strong) interactions with antagonists are relatively better connected in the mating network (i.e., with higher potential to transfer or receive pollen). Thus, mixed flower visitor assemblages with mutualists and antagonists give plants increased their importance in the mating networks, promote outcrossing and increasing both female and male fitness. Our approach helps characterize plant-animal interaction typologies, the context-specificity of diversified mutualisms, and a better forecasting of their functional consequences.

Hotspots of damage by antagonists shape the spatial structure of plant-pollinator interactions.

The balance between mutualistic and antagonistic plant-animal interactions and their spatial variation results in a highly dynamic mosaic of reproductive success within plant populations. Yet, the ecological drivers of this small-scale heterogeneity of interaction patterns and their outcomes remain virtually unexplored. We analyzed spatial structure in the frequency and intensity of interactions that vertebrate pollinators (birds and lizards) and invertebrate antagonists (florivores, nectar larcenists, and seed predators) had when interacting with the insular plant Isoplexis canariensis, and their effect on plant fitness. Spatially autocorrelated variation in plant reproductive success (fruit and viable seed set) emerged from the combined action of mutualists and antagonists, rather than reflecting the spatial pattern of any specific animal group. However, the influence of antagonists on plant fitness was stronger primarily due to the florivores' action on earlier reproductive stages, consuming and damaging floral structures before the arrival of pollinators. Our results indicate that the early action of antagonists creates hotspots of increased plant damage, where the effects of later acting mutualists are not translated into increased reproductive benefits. We foresee the potential for antagonists to shape the intra-population mosaics of plant fitness in situations where antagonists outnumber mutualists, when their interactions occur before those of mutualists, and when mutualists can detect and avoid damaged plants while foraging. Severely damaged plants in antagonistic hotspots might be excluded from the mating network and render a limited production of viable seeds, reducing both the growth rate of the plant population and the effective population size.

Quantity and quality components of effectiveness in insular pollinator assemblages.

Ecologically isolated habitats (e.g., oceanic islands) favor the appearance of small assemblages of pollinators, generally characterized by highly contrasted life modes (e.g., birds, lizards), and opportunistic nectar-feeding behavior. Different life modes should promote a low functional equivalence among pollinators, while opportunistic nectar feeding would lead to reduced and unpredictable pollination effectiveness (PE) compared to more specialized nectarivores. Dissecting the quantity (QNC) and quality (QLC) components of PE, we studied the opportunistic bird-lizard pollinator assemblage of Isoplexis canariensis from the Canary Islands to experimentally evaluate these potential characteristics. Birds and lizards showed different positions in the PE landscape, highlighting their low functional equivalence. Birds were more efficient than lizards due to higher visitation frequency (QNC). Adult lizards differed from juveniles in effecting a higher production of viable seeds (QLC). The disparate life modes of birds and lizards resulted in ample intra- and inter-specific PE variance. The main sources of PE variance were visitation frequency (both lizards and birds), number of flowers probed (lizards) and proportion of viable seeds resulting from a single visit (birds). The non-coincident locations of birds and lizards on the PE landscape indicate potential constraints for effectiveness. Variations in pollinator abundance can result in major effectiveness shifts only if QLC is relatively high, while changes in QLC would increase PE substantially only at high QNC. The low functional equivalence of impoverished, highly contrasted pollinator assemblages may be an early diagnostic signal for pollinator extinction potentially driving the collapse of mutualistic services.

Consequences of plant-pollinator and floral-herbivore interactions on the reproductive success of the Canary Islands endemic Canarina canariensis (Campanulaceae).

PREMISE OF THE STUDY: Pollination is a critical phase for plant reproduction, but ecological and evolutionary outcomes by pollinators may be counteracted by floral herbivores. These interacting assemblages may also be altered (directly or indirectly) by introduced species, especially on oceanic islands. In this study, we analyzed the effects of opportunistic nectar-feeding passerine birds and native (semi-slugs) and introduced (rats) floral herbivores on the reproductive success of Canarina canariensis. • METHODS: Manual pollination experiments were conducted to determine plant breeding system and pollen limitation. We also identified floral visitors and their visitation frequencies by censuses. Bird pollination effectiveness was evaluated by selective exclosures. The intensity of floral herbivory by native vs. introduced herbivores and its effect on plant fitness was estimated in different areas within the Canary island of Tenerife. • KEY RESULTS: Canarina canariensis had a very low spontaneous selfing ability and high pollen limitation, despite being self-compatible. Birds increased fruit set and the percentage of viable seeds per fruit, while florivores, the principal floral visitors, reduced them. Semi-slugs mainly consumed male reproductive organs, while rats preferred female. There was a strong within-island spatial variation in the herbivory intensity. • CONCLUSIONS: Opportunistic nectar-feeding birds increase the production of viable seeds in C. canariensis, but their beneficial effects are counteracted by the high incidence of floral herbivory. Because native semi-slugs damaged anthers more frequently than did introduced rats, these florivores may differ in their effects on male and female plant reproductive success.

Opportunistic nectar-feeding birds are effective pollinators of bird-flowers from Canary Islands: experimental evidence from Isoplexis canariensis (Scrophulariaceae).

Insular floras, characterized by simple pollination networks, sometimes include novel mutualistic agents such as nonspecialist nectarivores. In this study we confirmed the effective pollination of Isoplexis canariensis by opportunistic nectar-feeding birds in Tenerife, Canary Islands, Spain. This plant is among the ornithophilous species of the Canarian flora that lack past and present specialist nectarivorous birds. Experimental hand pollinations revealed self-compatibility, but cross-pollinated flowers produced a greater percentage of viable seeds than self-pollinated ones. Flowers were visited by five species of birds (Phylloscopus canariensis, Parus caeruleus, Sylvia melanocephala, Serinus canarius, and Fringilla coelebs) and by the endemic lizard (Gallotia galloti, Lacertidae). Insect pollination was absent, and the few insect visitors acted as nectar thieves or secondary nectar robbers. Birds represented 93.1% of total visits, with the Canarian Chiffchaff, Ph. canariensis, being the most frequent visitor. Flowers visited by birds set more, larger, and heavier fruit than flowers from which birds were excluded. Bird visitation also enhanced seed viability. These results demonstrate the active role of these opportunistic birds as effective pollinators of this Canarian bird-flower species. Further, the results reveal the need to consider the effect of these birds on the evolution of ornithophilous floral traits in absence of specialist nectarivores.