Metatranscriptomics reveals contrasting effects of elevation on the activity of bacteria and bacterial viruses in soil.

Soil microbial diversity affects ecosystem functioning and global biogeochemical cycles. Soil bacterial communities catalyse a diversity of biogeochemical reactions and have thus sparked considerable scientific interest. One driver of bacterial community dynamics in natural ecosystems has so far been largely neglected: the predator-prey interactions between bacterial viruses (bacteriophages) and bacteria. To generate ground level knowledge on environmental drivers of these particular predator-prey dynamics, we propose an activity-based ecological framework to simultaneous capture community dynamics of bacteria and bacteriophages in soils. An ecological framework and specifically the analyses of community dynamics across latitudinal and elevational gradients have been widely used in ecology to understand community-wide responses of innumerable taxa to environmental change, in particular to climate. Here, we tested the hypothesis that the activity of bacteria and bacteriophages codeclines across an elevational gradient. We used metatranscriptomics to investigate bacterial and bacteriophage activity patterns at five sites across 400 elevational metres in the Swiss Alps in 2015 and 2017. We found that metabolic activity (transcription levels) of bacteria declined significantly with increasing elevation, but activity of bacteriophages did not. We showed that bacteriophages are consistently active in soil along the entire gradient, making bacteriophage activity patterns divergent from that of their putative bacterial prey. Future efforts will be necessary to link the environment-activity relationship to predator-prey dynamics, and to understand the magnitude of viral contributions to carbon, nitrogen and phosphorus cycling when infection causes bacterial cell death, a process that may represent an overlooked component of soil biogeochemical cycles.

Global and regional ecological boundaries explain abrupt spatial discontinuities in avian frugivory interactions.

Species interactions can propagate disturbances across space via direct and indirect effects, potentially connecting species at a global scale. However, ecological and biogeographic boundaries may mitigate this spread by demarcating the limits of ecological networks. We tested whether large-scale ecological boundaries (ecoregions and biomes) and human disturbance gradients increase dissimilarity among plant-frugivore networks, while accounting for background spatial and elevational gradients and differences in network sampling. We assessed network dissimilarity patterns over a broad spatial scale, using 196 quantitative avian frugivory networks (encompassing 1496 plant and 1004 bird species) distributed across 67 ecoregions, 11 biomes, and 6 continents. We show that dissimilarities in species and interaction composition, but not network structure, are greater across ecoregion and biome boundaries and along different levels of human disturbance. Our findings indicate that biogeographic boundaries delineate the world's biodiversity of interactions and likely contribute to mitigating the propagation of disturbances at large spatial scales.

Scatter-hoarding birds disperse seeds to sites unfavorable for plant regeneration.

Scatter-hoarding birds provide effective long-distance seed dispersal for plants. Transporting seeds far promotes population spread, colonization of new areas, and connectivity between populations. However, whether seeds transported over long distances are deposited in habitats favorable to plant regeneration has rarely been investigated, mainly due to methodological constraints. To investigate dispersal patterns and distances of Swiss stone pine (Pinus cembra) seeds we utilized advances in tracking technology to track the movements of their sole disperser, the spotted nutcracker (Nucifraga caryocatactes). We found routine individual movements between single seed harvesting and seed caching site. Harvesting sites of individual birds overlapped, whereas seed caching sites were separated and located on average 5.3 km away from the harvesting site. Interestingly, most distant caching sites were located at low elevations and in spruce forest, where Swiss stone pine does not naturally occur. This suggests that nutcrackers disperse seeds over long distances but that a large portion of these seeds are cached outside the known pine habitat. Therefore, we conclude that the implications of such long-distance seed dispersal movements for plant populations should be carefully considered in combination with the effects of habitat quality on plant recruitment.

Speciation and population divergence in a mutualistic seed dispersing bird.

Bird-mediated seed dispersal is crucial for the regeneration and viability of ecosystems, often resulting in complex mutualistic species networks. Yet, how this mutualism drives the evolution of seed dispersing birds is still poorly understood. In the present study we combine whole genome re-sequencing analyses and morphometric data to assess the evolutionary processes that shaped the diversification of the Eurasian nutcracker (Nucifraga), a seed disperser known for its mutualism with pines (Pinus). Our results show that the divergence and phylogeographic patterns of nutcrackers resemble those of other non-mutualistic passerine birds and suggest that their early diversification was shaped by similar biogeographic and climatic processes. The limited variation in foraging traits indicates that local adaptation to pines likely played a minor role. Our study shows that close mutualistic relationships between bird and plant species might not necessarily act as a primary driver of evolution and diversification in resource-specialized birds.

Biodiversity and ecosystem functions depend on environmental conditions and resources rather than the geodiversity of a tropical biodiversity hotspot.

Biodiversity and ecosystem functions are highly threatened by global change. It has been proposed that geodiversity can be used as an easy-to-measure surrogate of biodiversity to guide conservation management. However, so far, there is mixed evidence to what extent geodiversity can predict biodiversity and ecosystem functions at the regional scale relevant for conservation planning. Here, we analyse how geodiversity computed as a compound index is suited to predict the diversity of four taxa and associated ecosystem functions in a tropical mountain hotspot of biodiversity and compare the results with the predictive power of environmental conditions and resources (climate, habitat, soil). We show that combinations of these environmental variables better explain species diversity and ecosystem functions than a geodiversity index and identified climate variables as more important predictors than habitat and soil variables, although the best predictors differ between taxa and functions. We conclude that a compound geodiversity index cannot be used as a single surrogate predictor for species diversity and ecosystem functions in tropical mountain rain forest ecosystems and is thus little suited to facilitate conservation management at the regional scale. Instead, both the selection and the combination of environmental variables are essential to guide conservation efforts to safeguard biodiversity and ecosystem functions.

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.

Downsizing of animal communities triggers stronger functional than structural decay in seed-dispersal networks.

Downsizing of animal communities due to defaunation is prevalent in many ecosystems. Yet, we know little about its consequences for ecosystem functions such as seed dispersal. Here, we use eight seed-dispersal networks sampled across the Andes and simulate how downsizing of avian frugivores impacts structural network robustness and seed dispersal. We use a trait-based modeling framework to quantify the consequences of downsizing-relative to random extinctions-for the number of interactions and secondary plant extinctions (as measures of structural robustness) and for long-distance seed dispersal (as a measure of ecosystem function). We find that downsizing leads to stronger functional than structural losses. For instance, 10% size-structured loss of bird species results in almost 40% decline of long-distance seed dispersal, but in less than 10% of structural loss. Our simulations reveal that measures of the structural robustness of ecological networks underestimate the consequences of animal extinction and downsizing for ecosystem functioning.

Similar composition of functional roles in Andean seed-dispersal networks, despite high species and interaction turnover.

The species composition of local communities varies in space, and its similarity generally decreases with increasing geographic distance between communities, a phenomenon known as distance decay of similarity. It is, however, not known how changes in local species composition affect ecological processes, that is, whether they lead to differences in the local composition of species' functional roles. We studied eight seed-dispersal networks along the South American Andes and compared them with regard to their species composition and their composition of functional roles. We tested (1) if changes in bird species composition lead to changes in the composition of bird functional roles, and (2) if the similarity in species composition and functional-role composition decreased with increasing geographic distance between the networks. We also used cluster analysis to (3) identify bird species with similar roles across all networks based on the similarity in the plants they consume, (i) considering only the species identity of the plants and (ii) considering the functional traits of the plants. Despite strong changes in species composition, the networks along the Andes showed similar composition of functional roles. (1) Changes in species composition generally did not lead to changes in the composition of functional roles. (2) Similarity in species composition, but not functional-role composition, decreased with increasing geographic distance between the networks. (3) The cluster analysis considering the functional traits of plants identified bird species with similar functional roles across all networks. The similarity in functional roles despite the high species turnover suggests that the ecological process of seed dispersal is organized similarly along the Andes, with similar functional roles fulfilled locally by different sets of species. The high species turnover, relative to functional turnover, also indicates that a large number of bird species are needed to maintain the seed-dispersal process along the Andes.

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.

Different responses of taxonomic and functional bird diversity to forest fragmentation across an elevational gradient.

Many studies have investigated how habitat fragmentation affects the taxonomic and functional diversity of species assemblages. However, the joint effects of habitat fragmentation and environmental conditions on taxonomic and functional diversity, for instance across elevational gradients, have largely been neglected so far. In this study, we compare whether taxonomic and functional indicators show similar or distinct responses to forest fragmentation across an elevational gradient. We based our analysis on a comprehensive data set of species-rich bird assemblages from tropical montane forest in the Southern Andes of Ecuador. We monitored birds over 2 years in two habitat types (continuous and fragmented forest) at three elevations (i.e., 1000, 2000, and 3000 m a.s.l) and measured nine morphological traits for each bird species on museum specimens. Bird species richness and abundance were significantly higher in fragmented compared to continuous forests and decreased towards high elevations. In contrast, functional diversity was significantly reduced in fragmented compared to continuous forests at low elevations, but fragmentation effects on functional diversity tended to be reversed at high elevations. Our results demonstrate that taxonomic and functional indicators can show decoupled responses to forest fragmentation and that these effects are highly variable across elevations. Our findings reveal that functional homogenization in bird communities in response to fragmentation can be masked by apparent increases in taxonomic diversity, particularly in diverse communities at low elevations.

Direct and indirect effects of plant and frugivore diversity on structural and functional components of fruit removal by birds.

Seed dispersal is an important ecosystem function, but it is contentious how structural and functional diversity of plant and bird communities are associated with seed-dispersal functions. We used structural equation models to test how structural (i.e., abundance, species richness) and functional diversity (i.e., functional dispersion and community-weighted means of functional traits) of fruiting plants and frugivorous birds directly and indirectly influence the respective components of fruit removal. We recorded plant and bird diversity in point counts and observed plant-frugivore interactions in a tropical mountain forest in Ecuador. We also recorded plant and bird morphological traits to calculate measures of functional diversity. We found that fruit abundance had a positive direct effect on bird abundance, which directly and indirectly mediated the abundance of removed fruits. Plant and bird species richness were only directly related to the richness of the removed fruits. Functional dispersion of the plant community was positively associated to that of the bird community and to that of the removed fruits. Consistently, we found positive associations between community-weighted means of plant and bird traits and between community-weighted means of plant traits and that of plants with removed fruits. In contrast, community-weighted means of the bird community were unrelated to that of the removed fruits. Overall, our results suggest that plant abundance directly and indirectly influences fruit removal, likely because of avian fruit tracking. However, we did not find strong links between the functional diversity of the frugivore community and removed fruits, suggesting that other factors in addition to plant-animal trait matching might be important for the functional diversity of removed fruits. Our findings highlight the importance of frugivore abundance for maintaining seed dispersal by animals in tropical forests.

Spatio-temporal variation in bird assemblages is associated with fluctuations in temperature and precipitation along a tropical elevational gradient.

Understanding the spatial and temporal dynamics of species assemblages is a main challenge in ecology. The mechanisms that shape species assemblages and their temporal fluctuations along tropical elevational gradients are particularly poorly understood. Here, we examined the spatio-temporal dynamics of bird assemblages along an elevational gradient in Ecuador. We conducted bird point counts at three elevations (1000, 2000 and 3000 m) on 18 1-ha plots and repeated the sampling eight times over two years (216 hours in total). For each plot, we obtained data of monthly temperatures and precipitation and recorded the overall resource availability (i.e., the sum of flower, fruit, and invertebrate resources). As expected, bird richness decreased from low to high elevations. Moreover, we found a significant decrease in bird abundance and richness and an increase in evenness between the most and least humid season at each of the three elevations. Climatic factors were more closely related to these temporal fluctuations than local resource availability. While temperature had significant positive effects on the abundance of birds at mid and high elevations, precipitation negatively affected bird abundance at low and mid elevations. Our study highlights that bird assemblages along tropical elevational gradients can show pronounced seasonal fluctuations. In particular, low temperatures and high precipitation seem to impose important constraints on birds. We conclude that potential changes in climate, due to global warming, are likely to affect the spatio-temporal dynamics of bird assemblages along tropical elevational gradients.

Pollination and seed dispersal are the most threatened processes of plant regeneration.

Plant regeneration is essential for maintaining forest biodiversity and ecosystem functioning, which are globally threatened by human disturbance. Here we present the first integrative meta-analysis on how forest disturbance affects multiple ecological processes of plant regeneration including pollination, seed dispersal, seed predation, recruitment and herbivory. We analysed 408 pairwise comparisons of these processes between near-natural and disturbed forests. Human impacts overall reduced plant regeneration. Importantly, only processes early in the regeneration cycle that often depend on plant-animal interactions, i.e. pollination and seed dispersal, were negatively affected. Later processes, i.e. seed predation, recruitment and herbivory, showed overall no significant response to human disturbance. Conserving pollination and seed dispersal, including the animals that provide these services to plants, should become a priority in forest conservation efforts globally.

Contrasting taxonomic and phylogenetic diversity responses to forest modifications: comparisons of taxa and successive plant life stages in South African scarp forest.

The degradation of natural forests to modified forests threatens subtropical and tropical biodiversity worldwide. Yet, species responses to forest modification vary considerably. Furthermore, effects of forest modification can differ, whether with respect to diversity components (taxonomic or phylogenetic) or to local (α-diversity) and regional (ß-diversity) spatial scales. This real-world complexity has so far hampered our understanding of subtropical and tropical biodiversity patterns in human-modified forest landscapes. In a subtropical South African forest landscape, we studied the responses of three successive plant life stages (adult trees, saplings, seedlings) and of birds to five different types of forest modification distinguished by the degree of within-forest disturbance and forest loss. Responses of the two taxa differed markedly. Thus, the taxonomic α-diversity of birds was negatively correlated with the diversity of all plant life stages and, contrary to plant diversity, increased with forest disturbance. Conversely, forest disturbance reduced the phylogenetic α-diversity of all plant life stages but not that of birds. Forest loss neither affected taxonomic nor phylogenetic diversity of any taxon. On the regional scale, taxonomic but not phylogenetic ß-diversity of both taxa was well predicted by variation in forest disturbance and forest loss. In contrast to adult trees, the phylogenetic diversity of saplings and seedlings showed signs of contemporary environmental filtering. In conclusion, forest modification in this subtropical landscape strongly shaped both local and regional biodiversity but with contrasting outcomes. Phylogenetic diversity of plants may be more threatened than that of mobile species such as birds. The reduced phylogenetic diversity of saplings and seedlings suggests losses in biodiversity that are not visible in adult trees, potentially indicating time-lags and contemporary shifts in forest regeneration. The different responses of taxonomic and phylogenetic diversity to forest modifications imply that biodiversity conservation in this subtropical landscape requires the preservation of natural and modified forests.

Seed perishability determines the caching behaviour of a food-hoarding bird.

Many animals hoard seeds for later consumption and establish seed caches that are often located at sites with specific environmental characteristics. One explanation for the selection of non-random caching locations is the avoidance of pilferage by other animals. Another possible hypothesis is that animals choose locations that hamper the perishability of stored food, allowing the consumption of unspoiled food items over long time periods. We examined seed perishability and pilferage avoidance as potential drivers for caching behaviour of spotted nutcrackers (Nucifraga caryocatactes) in the Swiss Alps where the birds are specialized on caching seeds of Swiss stone pine (Pinus cembra). We used seedling establishment as an inverse measure of seed perishability, as established seedlings cannot longer be consumed by nutcrackers. We recorded the environmental conditions (i.e. canopy openness and soil moisture) of seed caching, seedling establishment and pilferage sites. Our results show that sites of seed caching and seedling establishment had opposed microenvironmental conditions. Canopy openness and soil moisture were negatively related to seed caching but positively related to seedling establishment, i.e. nutcrackers cached seeds preferentially at sites where seed perishability was low. We found no effects of environmental factors on cache pilferage, i.e. neither canopy openness nor soil moisture had significant effects on pilferage rates. We thus could not relate caching behaviour to pilferage avoidance. Our study highlights the importance of seed perishability as a mechanism for seed-caching behaviour, which should be considered in future studies. Our findings could have important implications for the regeneration of plants whose seeds are dispersed by seed-caching animals, as the potential of seedlings to establish may strongly decrease if animals cache seeds at sites that favour seed perishability rather than seedling establishment.

Constant properties of plant-frugivore networks despite fluctuations in fruit and bird communities in space and time.

Human-induced changes in anthropogenic landscapes are a predominant threat to biodiversity and have been documented to affect mutualistic interactions between plants and animals, such as avian seed dispersal. Interactions between fleshy-fruited plants and frugivorous birds are highly seasonal in temperate ecosystems. Nevertheless, combined effects of landscape modification and seasonal variation on plant-frugivore interactions have never been assessed from a network perspective. Here, we present the first study that simultaneously investigates effects of landscape modification and seasonal variation on plant-frugivore interactions and on functional and interaction diversity of plant-frugivore networks. We recorded visitation rates of 39 frugivorous bird species to 28 fruiting-plant species in Central Germany from early summer to late autumn in hedgerows within three landscape types arranged along a gradient of decreasing anthropogenic modification and increasing structural diversity (i.e., farmland, orchard, forest edge). We analyzed how species richness, abundance, and community composition, as well as functional and interaction diversity of fruiting plants and frugivorous birds changed with landscape type, fruit availability, and season. We found that visitation rates of frugivorous birds were lower in farmland, but only in summer. In autumn, visitation rates were similar in all landscape types and strongly increased with increasing local fruit availability. The functional diversity of fruits and frugivorous birds and their interaction diversity remained surprisingly constant in all landscape types. Due to seasonal changes in communities of fruiting plants and frugivorous birds, functional dispersion of fruiting plants was lower in autumn than in summer, whereas functional richness and dispersion of frugivorous birds was higher in autumn than in summer. Our results indicate that seasonal changes in fruit availability influence the abundance of frugivorous birds along gradients of structural diversity at the landscape scale. Although seasonal fluctuations influenced the functional diversity of avian frugivore communities, we found constant interaction diversity of plant-frugivore networks in space and time, probably due to the functional redundancy of frugivorous birds. These findings indicate a high robustness of avian frugivory to moderate levels of human-induced landscape modification in temperate ecosystems and call for studies testing the generality of these findings for ultimate avian seed dispersal functions.