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.
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.
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.
Abstract. 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.
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.
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