In legume-Rhizobium symbioses, specialised soil bacteria fix atmospheric nitrogen in return for carbon. However, ineffective strains can arise, making discrimination essential. Discrimination can occur via partner choice, where legumes prevent ineffective strains from entering, or via sanctioning, where plants provide fewer resources. Several studies have inferred that legumes exercise partner choice, but the rhizobia compared were not otherwise isogenic. To test when and how plants discriminate ineffective strains we developed sets of fixing and non-fixing strains that differed only in the expression of nifH – essential for nitrogen fixation – and could be visualised using marker genes. We show that the plant is unable to select against the non-fixing strain at the point of entry, but that non-fixing nodules are sanctioned. We also used the technique to characterise mixed nodules (containing both a fixing and a non-fixing strain), whose frequency could be predicted using a simple diffusion model. We discuss that sanctioning is likely to evolve in preference to partner choice in any symbiosis where partner quality cannot be adequately assessed until goods or services are actively exchanged.
Mutualistic interactions form the basis for many ecological processes and are often analyzed within the framework of ecological networks. These interactions can be sampled with a range of methods and first analyses of pollination networks sampled with different methods showed differences in common network metrics. However, it is yet unknown if metrics of seed dispersal networks are similarly affected by the sampling method and if different methods detect a complementary set of frugivores. This is necessary to better understand the (dis‐)advantages of each method and to identify the role of each frugivore for the seed dispersal process. Here, we compare seed removal networks based on the observation of 2189 frugivore visits on ten focal plant species with seed deposition networks constructed by DNA barcoding of plant seeds in 3094 frugivore scats. We were interested in whether both methods identify the same disperser species and if species‐level network metrics of plant species were correlated between network types. Both methods identified the same avian super‐generalist frugivores, which accounted for the highest number of dispersed seeds. However, only with DNA barcoding, we detected elusive but frequent mammalian seed dispersers. The overall networks created by both methods were congruent but the plant species' degree, their interaction frequency and their specialization index (d′) differed. Our study suggests that DNA barcoding of defecated and regurgitated seeds can be used to construct quantitative seed deposition networks similar to those constructed by focal observations. To improve the overall completeness of seed dispersal networks it might be useful to combine both methods to detect interactions by both birds and mammals. Most importantly, the DNA barcoding method provides information on the post‐dispersal stage and thus on the qualitative contribution of each frugivore for the plant community thereby linking species interactions to regeneration dynamics of fleshy‐fruited plant species.
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The inability of small-gaped animals to consume very large fruits may limit seed dispersal of the respective plants. This has often been shown for large-fruited plant species that remain poorly dispersed when large-gaped animal species are lost due to anthropogenic pressure. Little is known about whether gape-size limitations similarly influence seed dispersal of small-fruited plant species that can show a large variation in fruit size within species. In this study, fruit sizes of 15 plant species were compared with the gape sizes of their 41 animal dispersers in the temperate, old-growth Białowieża Forest, Poland. The effect of gape-size limitations on fruit consumption was assessed at the plant species level, and for a subset of nine plant species, also at the individual level, and subindividual level (i.e., fruits of the same plant individual). In addition, for the species subset, fruit-seed trait relationships were investigated to determine whether a restricted access of small-gaped animals to large fruits results in the dispersal of fewer or smaller seeds per fruit. Fruit sizes widely varied among plant species (74.2%), considerably at the subindividual level (17.1%), and to the smallest extent among plant individuals (8.7%). Key disperser species should be able to consume fruits of all plant species and all individuals (except those of the largest-fruited plant species), even if they are able to consume only 28-55% of available fruits. Fruit and seed traits were positively correlated in eight out of nine plant species, indicating that gape size limitations will result in 49% fewer (in one) or 16–21% smaller seeds (in three plant species) dispersed per fruit by small-gaped than by large-gaped main dispersers, respectively. Our results show that a large subindividual variation in fruit size is characteristic for small-fruited plant species, and increases their connectedness with frugivores at the level of plants species and individuals. Simultaneously, however, the large variation in fruit size leads to gape-size limitations that may induce selective pressures on fruit size if large-gaped dispersers become extinct. This study emphasizes the mechanisms by which gape-size limitation at the species, individual and subindividual level shape plant-frugivore interactions and the co-evolution of small-fruited plants.
Forest degradation changes the structural heterogeneity of forests and species communities, with potential consequences for ecosystem functions including seed dispersal by frugivorous animals. While the quantity of seed dispersal may be robust towards forest degradation, changes in the effectiveness of seed dispersal through qualitative changes are poorly understood. Here, we carried out extensive field sampling on the structure of forest microhabitats, seed deposition sites and plant recruitment along three characteristics of forest microhabitats (canopy cover, ground vegetation and deadwood) in Europe's last lowland primeval forest (Białowieża, Poland). We then applied niche modelling to study forest degradation effects on multi-dimensional seed deposition by frugivores and recruitment of fleshy-fruited plants. Forest degradation was shown to (i) reduce the niche volume of forest microhabitat characteristics by half, (ii) homogenize the spatial seed deposition within and among frugivore species, and (iii) limit the regeneration of plants via changes in seed deposition and recruitment. Our study shows that the loss of frugivores in degraded forests is accompanied by a reduction in the complementarity and quality of seed dispersal by remaining frugivores. By contrast, structure-rich habitats, such as old-growth forests, safeguard the diversity of species interactions, forming the basis for high-quality ecosystem functions.
It is often assumed that the negative effects of inbreeding on fitness (inbreeding depression, ID) are particularly strong under stressful conditions. However, ID may be relatively mild under types of stress that plant populations have experienced for a long time, because environment‐specific deleterious alleles may already have been purged. We examined the performance of open‐ and self‐pollinated progeny of the short‐lived calcareous grassland plant Anthyllis vulneraria under three intensities of each of five types of stress. Drought, nutrient deficiency, and defoliation were chosen as stresses typical for the habitat of origin, while shade and waterlogging were expected to be novel, unfamiliar stresses for A. vulneraria. The stresses reduced plant biomass by up to 91%, and the responses of the plants were mostly in line with the functional equilibrium hypothesis. There was significant ID in biomass (δ = 0.17), leaf chlorophyll content, and the number of root nodules of the legume, but the magnitude of ID was independent of the stress treatments. In particular, there was no significant interaction between inbreeding and the intensity of any stress type, and ID was not higher under novel than under familiar stresses. In addition, phenotypic plasticity in biomass allocation, leaf functional traits and in root nodulation of the legume to the various stress treatments was not influenced by inbreeding. Our findings do not support the common hypothesis of stronger ID under stressful environments, not even if the stresses are novel to the plants.
Mutualistic interactions are by definition beneficial for each contributing partner. However, it is insufficiently understood how mutualistic interactions influence partners throughout their lives. Here, we used animal species-explicit, microhabitat-structured integral projection models to quantify the effect of seed dispersal by 20 animal species on the full life cycle of the tree Frangula alnus in Białowieża Forest, Eastern Poland. Our analysis showed that animal seed dispersal increased population growth by 2.5%. The effectiveness of animals as seed dispersers was strongly related to the interaction frequency but not the quality of seed dispersal. Consequently, the projected population decline due to simulated species extinction was driven by the loss of common rather than rare mutualist species. Our results support the notion that frequently interacting mutualists contribute most to the persistence of the populations of their partners, underscoring the role of common species for ecosystem functioning and nature conservation.
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