Life on oceanic islands deviate in many ways from that on the mainland. Their biodiversity is relatively poor and some groups are well-represented, others not, especially not insects. A scarcity of insects forces birds to explore alternative food, such as nectar and fruit. In this way, island birds may pollinate and disperse seed to an extent unseen on any mainland; they may even first consume floral resources of a plant species and then later harvest the fruit of the same species. Through this biotic reuse, they may act as double mutualists. The latter have never been studied at the level of the network, because they are traditionally considered rare. We sampled pollination and seed-dispersal interactions on Galápagos and constructed a plant-bird mutualism network of 108 plant (12% being double mutualists) and 21 bird species (48% being double mutualists), and their 479 interactions, being either single (95%) or double mutualisms (5%). Double mutualists constitute the core in the pollination-dispersal network, coupling the two link types together. They may also initiate positive feedbacks (more pollination leading to more dispersal), which theoretically are known to be unstable. Thus, double mutualisms may be a necessary, but risky prerequisite to the survival of island biodiversity.
A double mutualism (DM) occurs when two interacting species benefit each other in two different functions, e.g. when an animal species acts both as pollinator and seed disperser of the same plant. Besides the double benefit, a DM also imposes a larger risk to both functions if the performance of one partner declines. We conducted the first global review of DMs involving pollinators and seed dispersers, aiming to: 1) assess their prevalence across ecosystems and biogeographical regions; 2) identify the main plant and animal taxa, and their traits, implicated in DMs; and 3) evaluate the conservation status of double mutualist species. We compiled published and unpublished DM records using specific search terms, noting the species involved, their conservation status and geographic location, as well as the type of study (species vs communitylevel) in which the DM was detected. We identified 302 DM cases involving 207 plant and 92 animal species from 16 mainland and 17 island areas. Most records come from tropical regions and islands. Animals included birds (62%), mammals (22%), and reptiles (16%), mostly opportunist species; only 18% were nectarivores. Plants were mainly fleshy-fruited shrub or tree species (59%) with actinomorphic flowers that were visited by several or many pollinator species (87%). Most (56%) DMs were detected in community-level studies. DMs are mostly prevalent in ecosystems with limited food resources and mutualist partners, and with high generalization levels. Nearly 30% of the species involved in DMs are threatened according to IUCN criteria, 68% of which are found on islands. The high prevalence of DM on islands paired with the threat status of island species suggest that the loss of a double mutualists and its cascading consequences may have a severe impact on community composition and functioning of fragile island ecosystems.
An increasing number of double mutualisms (i.e. two interacting species benefiting each other in two different functions, e.g. pollination and seed dispersal) have been reported, mainly from island ecosystems, although we still lack much information on how effective such species are in both processes. Here, we assessed the pollination effectiveness of a double mutualism between an ancient Mediterranean gymnosperm, Ephedra fragilis, and a lizard, Podarcis lilfordi. On the one hand, we assessed the lizard contribution to different fitness measures (seed set and germination success), relative to that of insects and the wind effect; on the other, we determined the lizards’ seed removal rate (i.e. the quantity component of seed dispersal effectiveness). In both processes, we further tested for differences in their contributions among male, female and juvenile lizards. Ephedra fragilis showed to be mostly anemophilous, lizards and insects playing only a minor role on seed set. However, lizards qualitatively contributed to pollination success, as seeds coming from lizard-pollinated cones germinated at higher rates than those pollinated by wind or insects, although this was detected only for small seeds (<8 mg). The plant produced a low seed set (c. 23 %), which was compensated by a high seed germinability (c. 70 %). Adult male lizards were those most implicated in pollination, quantitatively more important than insects, and in seed dispersal. This work, thus, reports the importance of a lizard species in one of the few double mutualisms found in the World involving a gymnosperm, and it represents the first documentation of a double mutualism in the Mediterranean region. Our findings further contribute to highlight the role of both inter- and intraspecific differences in the effectiveness of mutualistic interactions.
Seed sowing may be a cheap and efficient reforestation method that can yield high-quality seedlings for many woody species, but this option is usually discarded against seedling planting due to the high seed losses to mammal predators. The search for methods to reduce seed predation is therefore a key issue to broaden reforestation options and restoration success. In this study we tested (1) the effectiveness of a new device to prevent small mammals from consuming large seeds such as acorns and (2) its effect on initial seedling performance. The device consists of a capsule made of two truncated pyramids joined at the bases, with two small openings at the top and the bottom where the stem and root can exit but rodents cannot enter. We conducted a field seed-predation experiment using fenced plots (only rodents present) and unfenced plots (rodents ? wild boar present) and a nursery experiment to check seedling emergence and growth. Acorn predation by rodents was almost nil when protected by the device (1.1 vs. 53.4 % without seed shelter), whereas predation by wild boar in the unfenced plots was not reduced by the device (12.4 %). In the nursery experiment there was no effect of the device on seedling emergence or growth. These results suggest that physical protectors like the one used in this study could represent a cheap method to foster the restoration of tree cover via seed sowing, especially if used in combination with fences or habitat features to reduce predation by large animals.
Habitat fragmentation threatens plant and pollinator communities, as well as their interactions. However, the effects of landscape fragmentation on the pollination of wild plant species are not well understood yet, partly because there are many correlated features in fragmented landscapes (e.g., decreased patch size, increased isolation, and patch complexity) whose influences are difficult to disentangle. Using a structural equation modeling approach, we assessed the direct and indirect effects of landscape fragmentation (patch size, isolation and complexity, percentage of surrounding land in forest) on the abundance, functional‐group richness, and evenness of pollinators of 24 habitat fragments within an agricultural landscape in Southern Norway. In addition, we studied how these variables affected visitation rates (visits per flower) and seed production (seed set, seed mass) in the four most abundant plant species in the area. Flower abundance was higher in larger and complex patches and decreased with the percentage of forest in the surroundings, while flower richness increased with patch complexity. We found a direct negative relationship between patch complexity and the overall number of pollinator visits that the habitat fragments received. Apart from this direct landscape effect, pollinator visits were mostly affected by the floral communities, with overall flower abundance and richness increasing both total number of pollinator visits and pollinator‐group richness, and flower richness having an additional negative influence on pollinator‐group evenness. Interestingly, we did not find any direct link between visitation rates and reproductive success for any of the study plant species. Instead, several landscape variables directly affected species seed production, although the effects of landscape on seed production were highly species specific. Patch complexity had a negative effect on seed production in two of the four focal species, while other components of the landscape had species‐specific effects. Increasing fragmentation of agricultural landscapes affects pollination interactions at the community level and the reproduction of wild plants. However, understanding the effects of fragmentation on seed production requires going beyond estimating visitation rates, since landscape effects on plant reproduction are not always related to overall interaction frequencies.
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