Bridging the gap between individual specialization and species persistence in mutualistic communities

The balance of pollination competition and facilitation among co-flowering plants and abiotic resource availability can modify plant species and individual reproduction. Floral resource succession and spatial heterogeneity modulate plant-pollinator interactions across ecological scales (individual plant, local assemblage, and interaction network of agroecological infrastructure across the farm). Intraspecific variation in flowering phenology can modulate the precise level of spatio-temporal heterogeneity in floral resources, pollen donor density, and pollinator interactions that a plant individual is exposed to, thereby affecting reproduction. We tested how abiotic resources and multi-scale plant-pollinator interactions affected individual plant seed set modulated by intraspecific variation in flowering phenology and spatio-temporal floral heterogeneity arising from agroecological infrastructure. We transplanted two focal insect-pollinated plant species (Cyanus segetum and Centaurea jacea, n=288) into agroecological infrastructure (10 sown wildflower and six legume-grass strips) across a farm-scale experiment (125 ha). We applied an individual-based phenologically explicit approach to match precisely the flowering period of plant individuals to the concomitant level of spatio-temporal heterogeneity in plant-pollinator interactions, potential pollen donors, floral resources, and abiotic conditions (temperature, water, and nitrogen). Individual plant attractiveness, assemblage floral density, and conspecific pollen donor density (C. jacea) improved seed set. Network linkage density increased focal species seed set and modified the effect of local assemblage richness and abundance on C. segetum. Mutual dependence on pollinators in networks increased C. segetum seed set, while C. jacea seed set was greatest where both specialization on pollinators and mutual dependence was high. Abiotic conditions were of little or no importance to seed set. Intra- and interspecific plant-pollinator interactions respond to spatio-temporal heterogeneity arising from agroecological management affecting wild plant species reproduction. The interplay of pollinator interactions within and between ecological scales affecting seed set implies a co-occurrence of pollinator-mediated facilitative and competitive interactions among plant species and individuals.

The Movement Ecology of Mutualism (<scp>CSEE</scp>/<scp>ESA</scp> 2022, <scp>OOS17</scp>)

BackgroundBelow-ground microbes mediate key ecosystem processes and play a vital role in plant nutrition and health. Understanding the composition of the belowground microbiome is therefore important for maintaining ecosystem stability. The structure of the belowground microbiome is largely determined by individual plants, but it is not clear how far their influence extends and, conversely, what the influence of other plants growing nearby is.ResultsTo determine the extent to which a focal host plant influences its soil and root microbiome when growing in a diverse community, we sampled the belowground bacterial and fungal communities of three plant species across a primary successional grassland sequence. The magnitude of the host effect on its belowground microbiome varied among microbial groups, soil and root habitats, and successional stages characterized by different levels of diversity of plant neighbours. Soil microbial communities were most strongly structured by sampling site and showed significant spatial patterns that were partially driven by soil chemistry. The influence of focal plant on soil microbiome was low but tended to increase with succession and increasing plant diversity. In contrast, root communities, particularly bacterial, were strongly structured by the focal plant species. Importantly, we also detected a significant effect of neighbouring plant community composition on bacteria and fungi associating with roots of the focal plants. The host influence on root microbiome varied across the successional grassland sequence and was highest in the most diverse site.ConclusionsOur results show that in a species rich natural grassland, focal plant influence on the belowground microbiome depends on environmental context and is modulated by surrounding plant community. The influence of plant neighbours is particularly pronounced in root communities which may have multiple consequences for plant community productivity and stability, stressing the importance of plant diversity for ecosystem functioning.

Despite increasing evidence of the importance of intraspecific trait variation in plant communities, its role in community trait responses to environmental variation, particularly along broad-scale climatic gradients, is poorly understood. We analyzed functional trait variation among early-successional herbaceous plant communities (old fields) across a 1200-km latitudinal extent in eastern North America, focusing on four traits: vegetative height, leaf area, specific leaf area (SLA), and leaf dry matter content (LDMC). We determined the contributions of species turnover and intraspecific variation to between-site functional dissimilarity at multiple spatial scales and community trait responses to edaphic and climatic factors. Among-site variation in community mean trait values and community trait responses to the environment were generated by a combination of species turnover and intraspecific variation, with species turnover making a greater contribution for all traits. The relative importance of intraspecific variation decreased with increasing geographic and environmental distance between sites for SLA and leaf area. Intraspecific variation was most important for responses of vegetative height and responses to edaphic compared to climatic factors. Individual species displayed strong trait responses to environmental factors in many cases, but these responses were highly variable among species and did not usually scale up to the community level. These findings provide new insights into the role of intraspecific trait variation in plant communities and the factors controlling its relative importance. The contribution of intraspecific variation to community trait responses was greatest at fine spatial scales and along edaphic gradients, while species turnover dominated at broad spatial scales and along climatic gradients.

Clarifying the functional consequences of intraspecific trait variability in response to interacting trophic levels would provide a significant improvement in our understanding of above‐ground–below‐ground linkages. In particular, the effects of grazing on plant traits may translate into altered litter quality, with potentially important consequences for litter‐feeding decomposers. Plant and litter variability in response to grazing is expected to depend on soil fertility levels, with tolerance and defensive strategies more commonly expressed on fertile and poorer soils, respectively. However, how grazing and fertility interactively alter litter quality and palatability to detritivores has not been explored yet. We conducted a cafeteria experiment with three common millipede (Diplopoda) species feeding on leaf litter from two plant species, the grass Bromopsis erecta and the forb Potentilla verna. Each millipede was offered a binary choice between litter types produced by the same plant species, but sampled in plots with distinct herbivory and fertilization status: litter originating from grazed areas or from 1‐year sheep exclosures, both in native areas and in adjacent paddocks that received chemical N and P fertilization, as well as litter from a 25‐year sheep exclosures in the native area. We found that fertilization and herbivore exclusion interactively affected Bromopsis litter quality and palatability, whereas Potentilla was much less affected. Bromopsis litter palatability was not affected by grazing when litter was collected in native plots, except for the long‐term exclosure which led to low palatability. In contrast, and in line with our expectations, herbivory was associated with much higher palatability in fertilized plots. The changes in palatability were associated with important alterations of litter quality. Overall, our study demonstrates that intraspecific variation in litter can have profound consequences for soil functioning. It emphasizes the role of grazing as a key, but plant species‐specific factor controlling litter intraspecific variability, and its complex interaction with soil fertility level. Moreover, our results advocate for a better understanding of the response of the different organisms involved in the decomposition process, in particular litter‐feeding macro‐detritivores. We encourage future studies aiming at disentangling the various and complex relationships between above‐ground processes such as herbivory and soil functioning.

Foliar Herbivory Affects Floral Characters and Plant Attractiveness to Pollinators: Implications for Male and Female Plant Fitness

QuestionsBoth species turnover and intraspecific trait variation can affect plant assemblage dynamics along environmental gradients. Here, we asked how community assemblage patterns in relation to species turnover and intraspecific variation differ between endemic and non‐endemic species. We hypothesized that endemic species show lower intraspecific variation than non‐endemic species because they tend to have high rates of in situ speciation, whereas non‐endemic species are expected to have a larger gene pool and higher phenotypic plasticity.LocationLa Palma, Canary Islands.MethodsWe established 44 sampling sites along a directional gradient of precipitation, heat load, soil nitrogen, phosphorus and pH. Along this gradient, we estimated species abundances and measured three traits (plant height, leaf area and leaf thickness) on perennial endemic and non‐endemic plant species. In total, we recorded traits for 1,223 plant individuals of 43 species. Subsequently, we calculated community‐weighted mean traits to measure the relative contribution of species turnover, intraspecific variation and their covariation along the analysed gradient.ResultsThe contribution of intraspecific variation to total variation was similar in endemic and non‐endemic assemblages. For plant height, intraspecific variation explained roughly as much variation as species turnover. For leaf area and leaf thickness, intraspecific variation explained almost no variation. Species turnover effects mainly drove trait responses along the environmental gradient, but intraspecific variation was important for responses in leaf area to precipitation.ConclusionsDespite their distinct evolutionary history, endemic and non‐endemic plant assemblages show similar patterns in species turnover and intraspecific variation. Our results indicate that species turnover is the main component of trait variation in the underlying study system. However, intraspecific variation can increase individual species’ fitness in response to precipitation. Overall, our study challenges the theory that intraspecific trait variation is more important for the establishment of non‐endemic species compared with endemic species.

Mycorrhizal response is the most common metric for characterizing how much benefit a plant derives from mycorrhizal symbiosis. Traditionally, ecologists have used these metrics to generalize benefit from mycorrhizal symbiosis in plant species, ignoring the potential for plant intraspecific trait variation to alter the outcome of the mutualism. In order for mean trait values to be useful as a functional trait to describe a species, as has been attempted for mycorrhizal response traits, interspecific variation must be much larger than intraspecific variation. While the variation among species has been extensively studied with respect to mycorrhizal response traits, variation within species has rarely been examined. We conducted a systematic review and analyzed how much variation for mycorrhizal growth and nutrient response typically exists within a plant species. We assessed 28 publications that included 60 individual studies testing mycorrhizal response in at least five genotypes of a plant species, and we found that intraspecific trait variation for mycorrhizal response was generally very large and highly variable depending on study design. The difference between the highest and lowest growth response in a study ranged from 10% to 350% across studies, and 36 of the studies included species for which both positive and negative growth responses to mycorrhizae were observed across different genotypes. The intraspecific variation for mycorrhizal growth response in some of these studies was larger than the variation documented among species across the plant kingdom. Phosphorus concentration and content was measured in 17 studies and variation in phosphorus response was similar to variation in growth responses. We also found that plant genotype was just as important for predicting mycorrhizal response as the effects of fungal inoculant identity. Our analysis highlights not only the potential importance of intraspecific trait variation for mycorrhizal response, but also the lack of research that has been done on the scale of this variation in plant species. Including intraspecific variation into research on the interactions between plants and their symbionts can increase our understanding of plant coexistence and ecological stability.

Much effort has been spent on the conservation of rare, threatened, and endangered plants in the biodiversity hotspot of the California Floristic Province, however little is known about the identity of their pollinators. In this study we provide the first formal study on the identity of the invertebrate pollinators of five rare endemic island plant species from San Clemente Island, the southernmost of the California Channel Islands: Delphinium variegatum ssp kinkiense, Lithophragma maximum, Malacothamnus clementinus, Malva assurgentiflora ssp glabra, and Sibara filifolia. We surveyed plant-pollinator interactions at populations of each focal plant species using timed sweep-netting. We used pollinator capture data to compile bipartite interaction networks for each plant population, and calculated centrality indices (degree, betweenness centrality, and closeness centrality) of pollinators to identify species important to network stability. We found a significant effect of pollinator taxonomic group (fly, bee, wasp, or Lepidopteran) on some indices of pollinator centrality in interaction networks, and variation in pollinator centrality between different locations. Hoverflies, moths, and butterflies were important generalists with higher network centrality across all plant populations, while bees tended to be more specialists within their networks, except for the Malva assurgentiflora ssp glabra network, where bees were on average of higher centrality than flies. We recommend targeted restoration practices for future study that could support pollination both directly and indirectly to focal rare plant species of conservation interest across plant populations. These practices could augment general pollinator conservation best practices such as reducing pesticide use and planting native plant species to provide increased pollination to endangered plants.

Plant–pollinator interactions within the urban environment

Global plant trait datasets commonly identify trait relationships that are interpreted to reflect fundamental trade-offs associated with plant strategies, but often these trait relationships are not identified when evaluating them at smaller taxonomic and spatial scales. In this study we evaluate trait relationships measured on individual plants for five widespread Protea species in South Africa to determine whether broad-scale patterns of structural trait (e.g. leaf area) and physiological trait (e.g. photosynthetic rates) relationships can be detected within natural populations, and if these traits are themselves related to plant fitness. We evaluated the variance structure (i.e. the proportional intraspecific trait variation relative to among-species variation) for nine structural traits and six physiological traits measured in wild populations. We used a multivariate path model to evaluate the relationships between structural traits and physiological traits, and the relationship between these traits and plant size and reproductive effort. While intraspecific trait variation is relatively low for structural traits, it accounts for between 50 and 100 % of the variation in physiological traits. Furthermore, we identified few trait associations between any one structural trait and physiological trait, but multivariate regressions revealed clear associations between combinations of structural traits and physiological performance (R2 = 0.37-0.64), and almost all traits had detectable associations with plant fitness. Intraspecific variation in structural traits leads to predictable differences in individual-level physiological performance in a multivariate framework, even though the relationship of any particular structural trait to physiological performance may be weak or undetectable. Furthermore, intraspecific variation in both structural and physiological traits leads to differences in plant size and fitness. These results demonstrate the importance of considering measurements of multivariate phenotypes on individual plants when evaluating trait relationships and how trait variation influences predictions of ecological and evolutionary outcomes.

Individual generalist predators often have more specialized diets than their populations do. Individual specialization (IS) is influenced by ecological opportunity, intraspecific competition, and interspecific competition, although the effects of these parameters are inconsistent across studies. We investigated IS in five species of frogs and toads, Anaxyrus americanus, A. fowleri, Lithobates catesbeianus, L. clamitans, and L. sphenocephalus. We used the natural history and ecology of each species to predict which parameters would influence IS. Our predictions were supported for some species but not others. We predicted IS would be positively influenced by resource diversity in all species, but this prediction held for only three species, with the relationship significant in A. fowleri and L. catesbeianus and marginally significant in A. americanus. We also predicted that interspecific competition would have a negative relationship with IS in L. clamitans because L. catesbeianus is competitively superior to L. clamitans and likely to suppress its foraging options. This prediction was upheld. Finally, we predicted that IS in A. americanus, A. fowleri, and L. clamitans would be influenced by intraspecific competition. However, IS was not influenced by intraspecific competition in any species, a surprising result given that intraspecific competition has traditionally been assumed to be the ecological parameter with the strongest effects on IS. Many previous studies did not simultaneously consider all three ecological parameters, which may have increased the apparent importance of intraspecific competition for IS. Our results revealed that the ecological parameters affected IS differently even across closely related and ecologically similar species, and demonstrated that these differences are sometimes predictable based on natural history. This study also suggests that sympatric ecological speciation based on IS may be rare because the ecological parameters driving IS are inconsistent across species, and the strength of their effects on intraspecific diet variation varies in space.

Climate change is driving species' range shifts, which are in turn disrupting species interactions due to species-specific differences in their abilities to migrate in response to climate. We evaluated the consequences of asynchronous range shifts in an alpine plant-pollinator community by transplanting replicated alpine meadow turfs downslope along an elevational gradient thereby introducing them to warmer climates and novel plant and pollinator communities. We asked how these novel plant-pollinator interactions affect plant reproduction. We found that pollinator communities differed substantially across the elevation/temperature gradient, suggesting that these plants will likely interact with different pollinator communities with warming climate. Contrary to the expectation that floral visitation would increase monotonically with warmer temperatures at lower elevations, visitation rate to the transplanted communities peaked under intermediate warming at midelevation sites. In contrast, visitation rate generally increased with temperature for the local, lower elevation plant communities surrounding the experimental alpine turfs. For two of three focal plant species in the transplanted high-elevation community, reproduction declined at warmer sites. For these species, reproduction appears to be dependent on pollinator identity such that reduced reproduction may be attributable to decreased visitation from key pollinator species, such as bumble bees, at warmer sites. Reproduction in the third focal species appears to be primarily driven by overall pollinator visitation rate, regardless of pollinator identity. Taken together, the results suggest climate warming can indirectly affect plant reproduction via changes in plant-pollinator interactions. More broadly, the experiment provides a case study for predicting the outcome of novel species interactions formed under changing climates.

Summary Co‐occurring and simultaneously fruiting plant species may either compete for dispersal by shared frugivores or enhance each other's dispersal through joint attraction of frugivores. While competitive plant–plant interactions are expected to cause the evolutionary divergence of fruit phenologies, facilitative interactions are assumed to promote their convergence. To which extent competitive and facilitative interactions among plant species with similar phenological niches are controlled by spatial variation in their local abundance and co‐occurrence is poorly understood. Here, we test the hypotheses that when a plant species fruits in high densities, large phenological overlap with other plant species causes competition for seed dispersers owing to frugivore satiation. Conversely, we expect large phenological overlap to enhance the dispersal of a plant species fruiting in low densities through attraction of frugivores by other species in its local neighbourhood. We test these predictions on plant–frugivore networks based on seed removal from 15 woody, fleshy‐fruited plant species by 30 avian and 4 mammalian frugivore species across 13 study sites in Białowieża Forest, Poland. A null model indicated that fruit phenologies of the regional plant assemblage were more differentiated than expected by chance. In the local networks, the tendency of plants to share frugivores increased with phenological overlap. High phenological overlap reduced the seed removal rates, interaction strength (proportion of interactions) and the number of partners of plant species fruiting in high densities. Conversely, plant species fruiting in low densities mainly profited from high phenological overlap with other species. Importantly, the sharing of mutualistic partners among co‐fruiting plant species was also reflected in their co‐occurrence. Synthesis. Our study highlights that, in spite of the overall signal of competition, frugivore‐mediated interactions among cofruiting plant species may consistently promote the establishment and persistence of rare species through facilitation. In addition, our results suggest that, among other factors, indirect coupling of species through shared mutualistic partners might be an important determinant of plant community assembly. The coupling through shared mutualists may cause the formation of associations among co‐dispersed plant species and might contribute to the coexistence of species in plant–animal mutualistic communities.

BackgroundPlants grow in multi-species communities rather than monocultures. Yet most studies on the emission of volatile organic compounds (VOCs) from plants in response to insect herbivore feeding focus on one plant species. Whether the presence and identity of neighboring plants or plant community attributes, such as plant species richness and plant species composition, affect the herbivore-induced VOC emission of a focal plant is poorly understood.MethodsWe established experimental plant communities in pots in the greenhouse where the focal plant species, red clover (Trifolium pratense), was grown in monoculture, in a two species mixture together with Geranium pratense or Dactylis glomerata, or in a mixture of all three species. We measured VOC emission of the focal plant and the entire plant community, with and without herbivory of Spodoptera littoralis caterpillars caged on one red clover individual within the communities.ResultsHerbivory increased VOC emission from red clover, and increasing plant species richness changed emissions of red clover and also from the entire plant community. Neighbor identity strongly affected red clover emission, with highest emission rates for plants growing together with D. glomerata.ConclusionThe results from this study indicate that the blend of VOCs perceived by host searching insects can be affected by plant-plant interactions.