Frugivore-mediated seed dispersal in fragmented landscapes: Compositional and functional turnover from forest to matrix.

Seed dispersal by frugivores is a fundamental function for plant community dynamics in fragmented landscapes, where forest remnants are typically embedded in a matrix of anthropogenic habitats. Frugivores can mediate both connectivity among forest remnants and plant colonization of the matrix. However, it remains poorly understood how frugivore communities change from forest to matrix due to the loss or replacement of species with traits that are less advantageous in open habitats and whether such changes ultimately influence the composition and traits of dispersed plants via species interactions. Here, we close this gap by using a unique dataset of seed-dispersal networks that were sampled in forest patches and adjacent matrix habitats of seven fragmented landscapes across Europe. We found a similar diversity of frugivores, plants, and interactions contributing to seed dispersal in forest and matrix, but a high turnover (replacement) in all these components. The turnover of dispersed seeds was smaller than that of frugivore communities because different frugivore species provided complementary seed dispersal in forest and matrix. Importantly, the turnover involved functional changes toward larger and more mobile frugivores in the matrix, which dispersed taller, larger-seeded plants with later fruiting periods. Our study provides a trait-based understanding of frugivore-mediated seed dispersal through fragmented landscapes, uncovering nonrandom shifts that can have cascading consequences for the composition of regenerating plant communities. Our findings also highlight the importance of forest remnants and frugivore faunas for ecosystem resilience, demonstrating a high potential for passive forest restoration of unmanaged lands in the matrix.

The attitudinal space framework: Embracing the multidimensionality of attitudinal diversity.

Attitude polarization describes an increasing attitude difference between groups and is increasingly recognized as a multidimensional phenomenon. However, a unified framework to study polarization across multiple dimensions is lacking. We introduce the attitudinal space framework (ASF) to fully quantify attitudinal diversity. We highlight two key measures-attitudinal extremization and attitudinal dispersion-to quantify across- and within-group attitudinal patterns. First, we show that affective polarization in the US electorate is weaker than previously thought based on mean differences alone: in both Democrat and Republican partisans, attitudinal dispersion increased between 1988 and 2008. Second, we examined attitudes toward wolves in Germany. Despite attitude differences between regions with and without wolves, we did not find differences in attitudinal extremization or dispersion, suggesting only weak attitude polarization. These results illustrate how the ASF is applicable to a wide range of social systems and offers an important avenue to understanding societal transformations.

Fossil leaves reveal drivers of herbivore functional diversity during the Cenozoic.

Herbivorous arthropods are the most diverse group of multicellular organisms on Earth. The most discussed drivers of their inordinate taxonomic and functional diversity are high niche availability associated with the diversity of host plants and dense niche packing due to host partitioning among herbivores. However, the relative contributions of these two factors to dynamics in the diversity of herbivores throughout Earth's history remain unresolved. Using fossil data on herbivore-induced leaf damage from across the Cenozoic, we infer quantitative bipartite interaction networks between plants and functional feeding types of herbivores. We fit a general model of diversity to these interaction networks and discover that host partitioning among functional groups of herbivores contributed twice as much to herbivore functional diversity as host diversity. These findings indicate that niche packing primarily shaped the dynamics in the functional diversity of herbivores during the past 66 my. Our study highlights how the fossil record can be used to test fundamental theories of biodiversity and represents a benchmark for assessing the drivers of herbivore functional diversity in modern ecosystems.

Common seed dispersers contribute most to the persistence of a fleshy-fruited tree.

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 Bialowieza 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.

Species richness is more important for ecosystem functioning than species turnover along an elevational gradient.

Many experiments have shown that biodiversity enhances ecosystem functioning. However, we have little understanding of how environmental heterogeneity shapes the effect of diversity on ecosystem functioning and to what extent this diversity effect is mediated by variation in species richness or species turnover. This knowledge is crucial to scaling up the results of experiments from local to regional scales. Here we quantify the diversity effect and its components-that is, the contributions of variation in species richness and species turnover-for 22 ecosystem functions of microorganisms, plants and animals across 13 major ecosystem types on Mt Kilimanjaro, Tanzania. Environmental heterogeneity across ecosystem types on average increased the diversity effect from explaining 49% to 72% of the variation in ecosystem functions. In contrast to our expectation, the diversity effect was more strongly mediated by variation in species richness than by species turnover. Our findings reveal that environmental heterogeneity strengthens the relationship between biodiversity and ecosystem functioning and that species richness is a stronger driver of ecosystem functioning than species turnover. Based on a broad range of taxa and ecosystem functions in a non-experimental system, these results are in line with predictions from biodiversity experiments and emphasize that conserving biodiversity is essential for maintaining ecosystem functioning.

Limited potential for bird migration to disperse plants to cooler latitudes.

Climate change is forcing the redistribution of life on Earth at an unprecedented velocity1,2. Migratory birds are thought to help plants to track climate change through long-distance seed dispersal3,4. However, seeds may be consistently dispersed towards cooler or warmer latitudes depending on whether the fruiting period of a plant species coincides with northward or southward migrations. Here we assess the potential of plant communities to keep pace with climate change through long-distance seed dispersal by migratory birds. To do so, we combine phenological and migration information with data on 949 seed-dispersal interactions between 46 bird and 81 plant species from 13 woodland communities across Europe. Most of the plant species (86%) in these communities are dispersed by birds migrating south, whereas only 35% are dispersed by birds migrating north; the latter subset is phylogenetically clustered in lineages that have fruiting periods that overlap with the spring migration. Moreover, the majority of this critical dispersal service northwards is provided by only a few Palaearctic migrant species. The potential of migratory birds to assist a small, non-random sample of plants to track climate change latitudinally is expected to strongly influence the formation of novel plant communities, and thus affect their ecosystem functions and community assembly at higher trophic levels.

Scale-dependent effects of niche specialisation: The disconnect between individual and species ranges.

One of the most general expectations of species range dynamics is that widespread species tend to have broader niches. However, it remains unclear how this relationship is expressed at different levels of biological organisation, which involve potentially distinctive processes operating at different spatial and temporal scales. Here, we show that range sizes of terrestrial non-volant mammals at the individual and species level show contrasting relationships with two ecological niche dimensions: diet and habitat breadth. While average individual home range size appears to be mainly shaped by the interplay of diet niche breadth and body mass, species geographical range size is primarily related to habitat niche breadth but not to diet niche breadth. Our findings suggest that individual home range size is shaped by the trade-off between energetic requirements, movement capacity and trophic specialisation, whereas species geographical range size is related to the ability to persist under various environmental conditions.

The role of the brown bear Ursus arctos as a legitimate megafaunal seed disperser.

Megafaunal frugivores can consume large amounts of fruits whose seeds may be dispersed over long distances, thus, affecting plant regeneration processes and ecosystem functioning. We investigated the role of brown bears (Ursus arctos) as legitimate megafaunal seed dispersers. We assessed the quantity component of seed dispersal by brown bears across its entire distribution based on information about both the relative frequency of occurrence and species composition of fleshy fruits in the diet of brown bears extracted from the literature. We assessed the quality component of seed dispersal based on germination experiments for 11 fleshy-fruited plant species common in temperate and boreal regions and frequently eaten by brown bears. Across its distribution, fleshy fruits, on average, represented 24% of the bear food items and 26% of the total volume consumed. Brown bears consumed seeds from at least 101 fleshy-fruited plant species belonging to 24 families and 42 genera, of which Rubus (Rosaceae) and Vaccinium (Ericaceae) were most commonly eaten. Brown bears inhabiting Mediterranean forests relied the most on fleshy fruits and consumed the largest number of species per study area. Seeds ingested by bears germinated at higher percentages than those from whole fruits, and at similar percentages than manually depulped seeds. We conclude that brown bears are legitimate seed dispersers as they consume large quantities of seeds that remain viable after gut passage. The decline of these megafaunal frugivores may compromise seed dispersal services and plant regeneration processes.

Environmental context determines the limiting demographic processes for plant recruitment across a species' elevational range.

Plant recruitment is a multi-stage process determining population dynamics and species distributions. Still, we have limited understanding of how the successive demographic processes depend on the environmental context across species' distributional ranges. We conducted a large-scale transplant experiment to study recruitment of Pinus cembra over six years. We quantified the effects of environmental conditions on four demographic processes and identified the most limiting across and beyond the pines' elevational range over several years. Realized transition probabilities of the demographic processes varied substantially across the species' distributional range. Seed deposition decreased from the lower to the upper elevational range margin by 90%, but this reduction was offset by increased seed germination and seedling survival. Dispersal limitation at the upper range margin potentially stems from unsuitable seed caching conditions for the animal seed disperser, whereas increased seed germination might result from enemy escape from fungal pathogens and favourable abiotic conditions at the upper range margin. Our multi-year experiment demonstrates that environmental context is decisive for the local relevance of particular demographic processes. We conclude that experimental studies identifying the limiting demographic processes controlling species distributions are key for projecting future range dynamics of plants.

Trait-Based Assessments of Climate-Change Impacts on Interacting Species.

Plant-animal interactions are fundamentally important in ecosystems, but have often been ignored by studies of climate-change impacts on biodiversity. Here, we present a trait-based framework for predicting the responses of interacting plants and animals to climate change. We distinguish three pathways along which climate change can impact interacting species in ecological communities: (i) spatial and temporal mismatches in the occurrence and abundance of species, (ii) the formation of novel interactions and secondary extinctions, and (iii) alterations of the dispersal ability of plants. These pathways are mediated by three kinds of functional traits: response traits, matching traits, and dispersal traits. We propose that incorporating these traits into predictive models will improve assessments of the responses of interacting species to climate change.

Direct and plant-mediated effects of climate on bird diversity in tropical mountains.

AIM: Although patterns of biodiversity across the globe are well studied, there is still a controversial debate about the underlying mechanisms and their generality across biogeographic scales. In particular, it is unclear to what extent diversity patterns along environmental gradients are directly driven by abiotic factors, such as climate, or indirectly mediated through biotic factors, such as resource effects on consumers. LOCATION: Andes, Southern Ecuador; Mt. Kilimanjaro, Tanzania. METHODS: We studied the diversity of fleshy-fruited plants and avian frugivores at the taxonomic level, that is, species richness and abundance, as well as at the level of functional traits, that is, functional richness and functional dispersion. We compared two important biodiversity hotspots in mountain systems of the Neotropics and Afrotropics. We used field data of plant and bird communities, including trait measurements of 367 plant and bird species. Using structural equation modeling, we disentangled direct and indirect effects of climate and the diversity of plant communities on the diversity of bird communities. RESULTS: We found significant bottom-up effects of fruit diversity on frugivore diversity at the taxonomic level. In contrast, climate was more important for patterns of functional diversity, with plant communities being mostly related to precipitation, and bird communities being most strongly related to temperature. MAIN CONCLUSIONS: Our results illustrate the general importance of bottom-up mechanisms for the taxonomic diversity of consumers, suggesting the importance of active resource tracking. Our results also suggest that it might be difficult to identify signals of ecological fitting between functional plant and animal traits across biogeographic regions, since different species groups may respond to different climatic drivers. This decoupling between resource and consumer communities could increase under future climate change if plant and animal communities are consistently related to distinct climatic drivers.

Reward regulation in plant-frugivore networks requires only weak cues.

Theory assumes that fair trade among mutualists requires highly reliable communication. In plant-animal mutualisms the reliability of cues that indicate reward quality is often low. Therefore, it is controversial whether communication allows animal mutualists to regulate their reward intake. Here we show that even loose relationships between fruit brightness and nutritional rewards (r2 = 0.11-0.35) allow birds to regulate their nutrient intake across distinct European plant-frugivore networks. Resident, over-wintering generalist frugivores that interact with diverse plant species select bright, lipid-rich fruits, whereas migratory birds select dark, sugar- and antioxidant-rich fruits. Both nutritional strategies are consistent with previous physiological experiments suggesting that over-wintering generalists aim to maximize their energy intake, whereas migrants aim to enhance the build-up of body fat, their immune response and oxidative status during migration. Our results suggest that animal mutualists require only weak cues to regulate their reward intake according to specific nutritional strategies.

Plant and animal functional diversity drive mutualistic network assembly across an elevational gradient.

Species' functional traits set the blueprint for pair-wise interactions in ecological networks. Yet, it is unknown to what extent the functional diversity of plant and animal communities controls network assembly along environmental gradients in real-world ecosystems. Here we address this question with a unique dataset of mutualistic bird-fruit, bird-flower and insect-flower interaction networks and associated functional traits of 200 plant and 282 animal species sampled along broad climate and land-use gradients on Mt. Kilimanjaro. We show that plant functional diversity is mainly limited by precipitation, while animal functional diversity is primarily limited by temperature. Furthermore, shifts in plant and animal functional diversity along the elevational gradient control the niche breadth and partitioning of the respective other trophic level. These findings reveal that climatic constraints on the functional diversity of either plants or animals determine the relative importance of bottom-up and top-down control in plant-animal interaction networks.

Moving from frugivory to seed dispersal: Incorporating the functional outcomes of interactions in plant-frugivore networks.

There is growing interest in understanding the functional outcomes of species interactions in ecological networks. For many mutualistic networks, including pollination and seed dispersal networks, interactions are generally sampled by recording animal foraging visits to plants. However, these visits may not reflect actual pollination or seed dispersal events, despite these typically being the ecological processes of interest. Frugivorous animals can act as seed dispersers, by swallowing entire fruits and dispersing their seeds, or as pulp peckers or seed predators, by pecking fruits to consume pieces of pulp or seeds. These processes have opposing consequences for plant reproductive success. Therefore, equating visitation with seed dispersal could lead to biased inferences about the ecology, evolution and conservation of seed dispersal mutualisms. Here, we use natural history information on the functional outcomes of pairwise bird-plant interactions to examine changes in the structure of seven European plant-frugivore visitation networks after non-mutualistic interactions (pulp pecking and seed predation) have been removed. Following existing knowledge of the contrasting structures of mutualistic and antagonistic networks, we hypothesized a number of changes following interaction removal, such as increased nestedness and lower specialization. Non-mutualistic interactions with pulp peckers and seed predators occurred in all seven networks, accounting for 21%-48% of all interactions and 6%-24% of total interaction frequency. When non-mutualistic interactions were removed, there were significant increases in network-level metrics such as connectance and nestedness, while robustness decreased. These changes were generally small, homogenous and driven by decreases in network size. Conversely, changes in species-level metrics were more variable and sometimes large, with significant decreases in plant degree, interaction frequency, specialization and resilience to animal extinctions and significant increases in frugivore species strength. Visitation data can overestimate the actual frequency of seed dispersal services in plant-frugivore networks. We show here that incorporating natural history information on the functions of species interactions can bring us closer to understanding the processes and functions operating in ecological communities. Our categorical approach lays the foundation for future work quantifying functional interaction outcomes along a mutualism-antagonism continuum, as documented in other frugivore faunas.

Humans and climate change drove the Holocene decline of the brown bear.

The current debate about megafaunal extinctions during the Quaternary focuses on the extent to which they were driven by humans, climate change, or both. These two factors may have interacted in a complex and unexpected manner, leaving the exact pathways to prehistoric extinctions unresolved. Here we quantify, with unprecedented detail, the contribution of humans and climate change to the Holocene decline of the largest living terrestrial carnivore, the brown bear (Ursus arctos), on a continental scale. We inform a spatially explicit metapopulation model for the species by combining life-history data and an extensive archaeofaunal record from excavations across Europe with reconstructed climate and land-use data reaching back 12,000 years. The model reveals that, despite the broad climatic niche of the brown bear, increasing winter temperatures contributed substantially to its Holocene decline - both directly by reducing the species' reproductive rate and indirectly by facilitating human land use. The first local extinctions occurred during the Mid-Holocene warming period, but the rise of the Roman Empire 2,000 years ago marked the onset of large-scale extinctions, followed by increasingly rapid range loss and fragmentation. These findings strongly support the hypothesis that complex interactions between climate and humans may have accelerated megafaunal extinctions.

Ecological networks are more sensitive to plant than to animal extinction under climate change.

Impacts of climate change on individual species are increasingly well documented, but we lack understanding of how these effects propagate through ecological communities. Here we combine species distribution models with ecological network analyses to test potential impacts of climate change on >700 plant and animal species in pollination and seed-dispersal networks from central Europe. We discover that animal species that interact with a low diversity of plant species have narrow climatic niches and are most vulnerable to climate change. In contrast, biotic specialization of plants is not related to climatic niche breadth and vulnerability. A simulation model incorporating different scenarios of species coextinction and capacities for partner switches shows that projected plant extinctions under climate change are more likely to trigger animal coextinctions than vice versa. This result demonstrates that impacts of climate change on biodiversity can be amplified via extinction cascades from plants to animals in ecological networks.

Correlated loss of ecosystem services in coupled mutualistic networks.

Networks of species interactions promote biodiversity and provide important ecosystem services. These networks have traditionally been studied in isolation, but species are commonly involved in multiple, diverse types of interaction. Therefore, whether different types of species interaction networks coupled through shared species show idiosyncratic or correlated responses to habitat degradation is unresolved. Here we study the collective response of coupled mutualistic networks of plants and their pollinators and seed dispersers to the degradation of Europe's last relict of old-growth lowland forest (Bialowieza, Poland). We show that logging of old-growth forests has correlated effects on the number of partners and interactions of plants in both mutualisms, and that these effects are mediated by shifts in plant densities on logged sites. These results suggest bottom-up-controlled effects of habitat degradation on plant-animal mutualistic networks, and predict that the conversion of primary old-growth forests to secondary habitats may cause a parallel loss of multiple animal-mediated ecosystem services.