Airborne DNA reveals predictable spatial and seasonal dynamics of fungi.

Fungi are among the most diverse and ecologically important kingdoms in life. However, the distributional ranges of fungi remain largely unknown as do the ecological mechanisms that shape their distributions1,2. To provide an integrated view of the spatial and seasonal dynamics of fungi, we implemented a globally distributed standardized aerial sampling of fungal spores3. The vast majority of operational taxonomic units were detected within only one climatic zone, and the spatiotemporal patterns of species richness and community composition were mostly explained by annual mean air temperature. Tropical regions hosted the highest fungal diversity except for lichenized, ericoid mycorrhizal and ectomycorrhizal fungi, which reached their peak diversity in temperate regions. The sensitivity in climatic responses was associated with phylogenetic relatedness, suggesting that large-scale distributions of some fungal groups are partially constrained by their ancestral niche. There was a strong phylogenetic signal in seasonal sensitivity, suggesting that some groups of fungi have retained their ancestral trait of sporulating for only a short period. Overall, our results show that the hyperdiverse kingdom of fungi follows globally highly predictable spatial and temporal dynamics, with seasonality in both species richness and community composition increasing with latitude. Our study reports patterns resembling those described for other major groups of organisms, thus making a major contribution to the long-standing debate on whether organisms with a microbial lifestyle follow the global biodiversity paradigms known for macroorganisms4,5.

Habitat area and edges affect the length of trophic chains in a fragmented forest.

The food chain length represents how much energy reaches different trophic levels in food webs. Environmental changes derived from human activities have the potential to affect chain length. We explore how habitat area and edges affect chain length through: (1) a bottom-up effect of abundance ('pyramid hypothesis'); (2) the truncation of the highest trophic level ('trophic-rank hypothesis'); and (3) changes in species connectivity patterns ('connectivity hypothesis'). We built plant-leaf miner-parasitoid food webs in 19 remnants of a fragmented Chaco forest from central Argentina. On each remnant, we constructed food webs from different locations at the forest interior and edges. For each food web, we registered the abundance of species, the species richness of each trophic level, estimated the connectivity of their networks, and the average food chain length. We used structural equation models to evaluate the direct and indirect effects of habitat area and edge/interior location on food chain length mediated by species richness, abundance and connectivity. We found no direct effects of habitat area on chain length but chains were longer at forest edges than at their interior. The three mechanisms were supported by our results, although they showed different strengths. First, we found that the interior favours a bottom-up abundance effect from herbivores to parasitoids that positively affected chain length; second, we found that the forest area positively affects plant richness, which has a strong effect on the number of resources used by consumers, with a positive effect on chain length. Third, the remnant area and interior position favoured plant richness with a negative effect on the abundance of parasitoids, which had a positive effect on chain length. In general, the strongest effects on chain length were detected through changes in abundance rather than species richness although abundance was less affected by habitat fragmentation. We evaluated for the first time the effects of human-driven habitat fragmentation on the length of trophic chains in highly diverse plant-herbivore-parasitoid networks. Despite the loss of species, small habitat fragments and edges embedded in the agricultural matrix can support interaction networks, making them conservation targets in managed landscapes.

El largo de cadenas tróficas representa cuanta energía alcanza diferentes niveles tróficos en redes tróficas. Los cambios ambientales producto de las actividades humanas tienen el potencial de afectar el largo de las cadenas tróficas. Exploramos como el área de hábitat y los bordes afectan el largo de cadenas tróficas a través de: (1) un efecto ascendente de la abundancia ('hipótesis pirámide'); (2) el truncamiento del nivel trófico superior ('hipótesis de ranking trófico'); y (3) cambios en los patrones de conectividad ('hipótesis de conectividad'). Construimos redes tróficas entre plantas-minadores de hoja-parasitoides en 19 remanentes de bosque Chaqueño serrano altamente fragmentado en el centro de Argentina. Para cada remanente construimos redes tróficas en distintas ubicaciones en el borde e interior del bosque. Para cada red trófica registramos la abundancia media de las especies, la riqueza de cada nivel trófico, estimamos la conectividad de las redes y el largo de cadenas tróficas promedio. Utilizamos modelos de ecuaciones estructurales para evaluar los efectos directos e indirectos del área y la ubicación borde/interior sobre el largo de cadenas tróficas mediado por la riqueza de especies, la abundancia y la conectividad. No encontramos efectos directos del área de hábitat sobre el largo de cadenas, pero las cadenas fueron más largas en los bordes que en el interior. Los tres mecanismos propuestos fueron apoyados por los resultados, pero mostraron distinta fuerza. Primero, encontramos que el interior de los bosques favorece los efectos ascendentes de la abundancia desde los herbívoros a los parasitoides lo que afectó positivamente al largo de las cadenas; segundo, encontramos que el área de bosque afectó positivamente a la riqueza de especies, lo que tuvo un efecto positivo en el largo de cadenas. Tercero, el área de bosque remanente y la ubicación en el interior favorecieron la riqueza de plantas, influyendo negativamente en la abundancia de parasitoides lo que tuvo un efecto positivo en el largo de cadenas. En general, los efectos más fuertes sobre el largo de cadenas se detectaron a través de cambios en la abundancia más que en la riqueza, aunque la abundancia fue menos afectada por la fragmentación del hábitat que la riqueza de especies. En este estudio evaluamos por primera vez los efectos de la fragmentación del hábitat por causas humanas sobre el largo de cadenas tróficas en redes tróficas altamente diversas de plantas, herbívoros y parasitoides. A pesar de la pérdida de especies, los fragmentos pequeños y los bordes de bosque inmersos en una matriz agrícola pueden sostener redes de interacciones, convirtiéndolos en objetivos de conservación en paisajes manejados.

Plant-plant co-occurrences under a complex land-use gradient in a temperate forest.

Land-use generates multiple stress factors, and we need to understand their effects on plant-plant interactions to predict the consequences of land-use intensification. The stress-gradient hypothesis predicts that the relative strength of positive and negative interactions changes inversely under increasing environmental stress. However, the outcome of interactions also depends on stress factor's complexity, the scale of analysis, and the role of functional traits in structuring the community. We evaluated plant-plant co-occurrences in a temperate forest, aiming to identify changes in pairwise and network metrics under increasing silvopastoral use intensity. Proportionally, positive co-occurrences were more frequent under high than low use, while negative co-occurrences were more frequent under low than high. Networks of negative co-occurrences showed higher centralization under low use, while networks of positive co-occurrences showed lower modularity and higher centralization under high use. We found a partial relationship between co-occurrences and key functional traits expected to mediate facilitation and competition processes. Our results shows that the stress-gradient hypothesis predicts changes in spatial co-occurrences even when two stress factors interact in a complex way. Networks of negative co-occurrences showed a hierarchical effect of dominant species under low use intensity. But positive co-occurrence network structure partially presented the characteristics expected if the facilitation was an important mechanism characterizing the community under high disturbance intensity. The partial relationship between functional traits and co-occurrences may indicate that other factors besides biotic interactions may be structuring the observed negative spatial associations in temperate Patagonian forests.

Does fire disturbance affect ant community structure? Insights from spatial co-occurrence networks.

The coexistence of several species involves a complex mix of positive and negative interactions that can be represented as networks. As much as other ecological features, patterns of multispecies co-occurrence are susceptible to anthropogenic disturbance. In ant communities, wildfires may enhance competitive interactions by benefiting active, aggressive species, and by increasing encounter probabilities through decreased space availability. We explored ant co-occurrence patterns by analysing the macro and microscopic structure of their interaction networks in burned and unburned habitats. We built co-occurrence networks using significant aggregations and segregations between species pairs as positive and negative interactions, respectively. We described aggregate network properties and microscopic structural changes by comparing species and interactions turnover between burned and unburned sites. We found no differences in the macroscopic structure of co-occurrence networks between different fire regimes. However, we detected changes in the composition of both species and negative interactions. Interaction turnover between networks of different habitats was mostly explained by rewiring of interactions between shared species rather than by species replacement. Our results reflected changes in ant communities in response to fire although there were no changes in global structural patterns. These changes in species and negative interactions suggest modifications in species roles translated into changes in the spatial distribution of ant species. The analysis of species co-occurrence networks is a useful tool to detect and visualize patterns in ant communities and to understand the mechanisms underlying the effects of disturbance on biodiversity.

Global Spore Sampling Project: A global, standardized dataset of airborne fungal DNA.

Novel methods for sampling and characterizing biodiversity hold great promise for re-evaluating patterns of life across the planet. The sampling of airborne spores with a cyclone sampler, and the sequencing of their DNA, have been suggested as an efficient and well-calibrated tool for surveying fungal diversity across various environments. Here we present data originating from the Global Spore Sampling Project, comprising 2,768 samples collected during two years at 47 outdoor locations across the world. Each sample represents fungal DNA extracted from 24 m3 of air. We applied a conservative bioinformatics pipeline that filtered out sequences that did not show strong evidence of representing a fungal species. The pipeline yielded 27,954 species-level operational taxonomic units (OTUs). Each OTU is accompanied by a probabilistic taxonomic classification, validated through comparison with expert evaluations. To examine the potential of the data for ecological analyses, we partitioned the variation in species distributions into spatial and seasonal components, showing a strong effect of the annual mean temperature on community composition.

Forest fragmentation reduces parasitism via species loss at multiple trophic levels.

Although there is accumulating evidence from artificially assembled communities that reductions of species diversity result in diminished ecosystem functioning, it is not yet clear how real-world changes in diversity affect the flow of energy between trophic levels in multi-trophic contexts. In central Argentina, forest fragmentation has led to species loss of plants, herbivore and parasitoid insects, decline in trophic processes (herbivory and parasitism), and food web contraction. Here we examine if and how loss of parasitoid species following fragmentation causes decreased parasitism rates, by analyzing food webs of leaf miners and parasitoids from 19 forest fragments of decreasing size. We asked three questions: Do reductions in parasitoid richness following fragmentation directly or indirectly affect parasitism rate? Are changes in community parasitism rate driven by changes in the parasitism rate of individual leaf miner species, or changes in leaf miner composition, or both? Which traits of species determine the effects of food web change on parasitism rates? We found that habitat loss initiated a bottom-up cascade of extinctions from plants to leaf miners to parasitoids, with reductions in parasitoid richness ultimately driving decreases in parasitism rates. This relationship between parasitoid richness and parasitism depended on changes in the relative abundance (but not occurrence) of leaf miners such that parasitoid-rich fragments were dominated by leaf miner species that supported high rates of parasitism. Surprisingly, we found that only a small subset of species in the food web could account for much of the increase in parasitism with parasitoid richness: lepidopteran miners that attained exceptionally high densities in some fragments and their largely specialist parasitoids. How specialized a parasitoid is, and the relative abundance of leaf miners, had important effects on the diversity-parasitism rate relationship, but not other leaf miner traits including trophic breadth, body size, and mine shape. Our results show that a full understanding of the functional consequences of perturbations and species loss requires both a multi-trophic perspective and a trait-based approach, which together capture some of the biological complexity of natural systems.

Ecological network complexity scales with area.

Larger geographical areas contain more species-an observation raised to a law in ecology. Less explored is whether biodiversity changes are accompanied by a modification of interaction networks. We use data from 32 spatial interaction networks from different ecosystems to analyse how network structure changes with area. We find that basic community structure descriptors (number of species, links and links per species) increase with area following a power law. Yet, the distribution of links per species varies little with area, indicating that the fundamental organization of interactions within networks is conserved. Our null model analyses suggest that the spatial scaling of network structure is determined by factors beyond species richness and the number of links. We demonstrate that biodiversity-area relationships can be extended from species counts to higher levels of network complexity. Therefore, the consequences of anthropogenic habitat destruction may extend from species loss to wider simplification of natural communities.

The effect of natural disturbances on forest biodiversity: an ecological synthesis.

Disturbances alter biodiversity via their specific characteristics, including severity and extent in the landscape, which act at different temporal and spatial scales. Biodiversity response to disturbance also depends on the community characteristics and habitat requirements of species. Untangling the mechanistic interplay of these factors has guided disturbance ecology for decades, generating mixed scientific evidence of biodiversity responses to disturbance. Understanding the impact of natural disturbances on biodiversity is increasingly important due to human-induced changes in natural disturbance regimes. In many areas, major natural forest disturbances, such as wildfires, windstorms, and insect outbreaks, are becoming more frequent, intense, severe, and widespread due to climate change and land-use change. Conversely, the suppression of natural disturbances threatens disturbance-dependent biota. Using a meta-analytic approach, we analysed a global data set (with most sampling concentrated in temperate and boreal secondary forests) of species assemblages of 26 taxonomic groups, including plants, animals, and fungi collected from forests affected by wildfires, windstorms, and insect outbreaks. The overall effect of natural disturbances on α-diversity did not differ significantly from zero, but some taxonomic groups responded positively to disturbance, while others tended to respond negatively. Disturbance was beneficial for taxonomic groups preferring conditions associated with open canopies (e.g. hymenopterans and hoverflies), whereas ground-dwelling groups and/or groups typically associated with shady conditions (e.g. epigeic lichens and mycorrhizal fungi) were more likely to be negatively impacted by disturbance. Across all taxonomic groups, the highest α-diversity in disturbed forest patches occurred under moderate disturbance severity, i.e. with approximately 55% of trees killed by disturbance. We further extended our meta-analysis by applying a unified diversity concept based on Hill numbers to estimate α-diversity changes in different taxonomic groups across a gradient of disturbance severity measured at the stand scale and incorporating other disturbance features. We found that disturbance severity negatively affected diversity for Hill number q = 0 but not for q = 1 and q = 2, indicating that diversity-disturbance relationships are shaped by species relative abundances. Our synthesis of α-diversity was extended by a synthesis of disturbance-induced change in species assemblages, and revealed that disturbance changes the ß-diversity of multiple taxonomic groups, including some groups that were not affected at the α-diversity level (birds and woody plants). Finally, we used mixed rarefaction/extrapolation to estimate biodiversity change as a function of the proportion of forests that were disturbed, i.e. the disturbance extent measured at the landscape scale. The comparison of intact and naturally disturbed forests revealed that both types of forests provide habitat for unique species assemblages, whereas species diversity in the mixture of disturbed and undisturbed forests peaked at intermediate values of disturbance extent in the simulated landscape. Hence, the relationship between α-diversity and disturbance severity in disturbed forest stands was strikingly similar to the relationship between species richness and disturbance extent in a landscape consisting of both disturbed and undisturbed forest habitats. This result suggests that both moderate disturbance severity and moderate disturbance extent support the highest levels of biodiversity in contemporary forest landscapes.

Network topology: patterns and mechanisms in plant-herbivore and host-parasitoid food webs.

1. Biological communities are organized in complex interaction networks such as food webs, which topology appears to be non-random. Gradients, compartments, nested subsets and even combinations of these structures have been shown in bipartite networks. However, in most studies only one pattern is tested against randomness and mechanistic hypotheses are generally lacking. 2. Here we examined the topology of regional, coexisting plant-herbivore and host-parasitoid food webs to discriminate between the mentioned network patterns. We also evaluated the role of species body size, local abundance, regional frequency and phylogeny as determinants of network topology. 3. We found both food webs to be compartmented, with interaction range boundaries imposed by host phylogeny. Species degree within compartments was mostly related to their regional frequency and local abundance. Only one compartment showed an internal nested structure in the distribution of interactions between species, but species position within this compartment was unrelated to species size or abundance. 4. These results suggest that compartmentalization may be more common than previously considered, and that network structure is a result of multiple, hierarchical, non-exclusive processes.

Evaluating multiple determinants of the structure of plant-animal mutualistic networks.

The structure of mutualistic networks is likely to result from the simultaneous influence of neutrality and the constraints imposed by complementarity in species phenotypes, phenologies, spatial distributions, phylogenetic relationships, and sampling artifacts. We develop a conceptual and methodological framework to evaluate the relative contributions of these potential determinants. Applying this approach to the analysis of a plant-pollinator network, we show that information on relative abundance and phenology suffices to predict several aggregate network properties (connectance, nestedness, interaction evenness, and interaction asymmetry). However, such information falls short of predicting the detailed network structure (the frequency of pairwise interactions), leaving a large amount of variation unexplained. Taken together, our results suggest that both relative species abundance and complementarity in spatiotemporal distribution contribute substantially to generate observed network patters, but that this information is by no means sufficient to predict the occurrence and frequency of pairwise interactions. Future studies could use our methodological framework to evaluate the generality of our findings in a representative sample of study systems with contrasting ecological conditions.

Uniting pattern and process in plant-animal mutualistic networks: a review.

BACKGROUND: Ecologists and evolutionary biologists are becoming increasingly interested in networks as a framework to study plant-animal mutualisms within their ecological context. Although such focus on networks has brought about important insights into the structure of these interactions, relatively little is still known about the mechanisms behind these patterns. SCOPE: The aim in this paper is to offer an overview of the mechanisms influencing the structure of plant-animal mutualistic networks. A brief summary is presented of the salient network patterns, the potential mechanisms are discussed and the studies that have evaluated them are reviewed. This review shows that researchers of plant-animal mutualisms have made substantial progress in the understanding of the processes behind the patterns observed in mutualistic networks. At the same time, we are still far from a thorough, integrative mechanistic understanding. We close with specific suggestions for directions of future research, which include developing methods to evaluate the relative importance of mechanisms influencing network patterns and focusing research efforts on selected representative study systems throughout the world.

Habitat fragmentation and species loss across three interacting trophic levels: effects of life-history and food-web traits.

Not all species are likely to be equally affected by habitat fragmentation; thus, we evaluated the effects of size of forest remnants on trophically linked communities of plants, leaf-mining insects, and their parasitoids. We explored the possibility of differential vulnerability to habitat area reduction in relation to species-specific and food-web traits by comparing species-area regression slopes. Moreover, we searched for a synergistic effect of these traits and of trophic level. We collected mined leaves and recorded plant, leaf miner, and parasitoid species interactions in five 100-m2 transects in 19 Chaco Serrano woodland remnants in central Argentina. Species were classified into extreme categories according to body size, natural abundance, trophic breadth, and trophic level. Species-area slopes differed between groups with extreme values of natural abundance or trophic specialization. Nevertheless, synergistic effects of life-history and food-web traits were only found for trophic level and trophic breadth: area-related species loss was highest for specialist parasitoids. It has been suggested that species position within interaction webs could determine their vulnerability to extinction. Our results provide evidence that food-web parameters, such as trophic level and trophic breadth, affect species sensitivity to habitat fragmentation.

Landscape connectivity explains interaction network patterns at multiple scales.

Under a metacommunity framework, the spatial configuration of habitat fragments could determine local community structure. Yet, quantifying fragment connectivity is challenging, as it depends on multiple variables at several geographical scales. We assessed the extent to which fragment connectivity and area explain patterns in interaction structure among four herbivore guilds and their host plants in a metacommunity. We propose an integrative connectivity metric including geographic distance, neighboring fragment area and similarity in resource composition as an extension of Hanski's classic metric. We then used nonlinear models to assess whether fragment connectivity and area predicted link richness and similarity in link composition. We found that link richness was always negatively related to connectivity but at different geographic scales depending on the herbivore guild. In contrast, while link composition was also related to connectivity, the direction and strength of this relationship varied among herbivore guilds and type of link composition (qualitative or quantitative). Furthermore, focal fragment area was not an important determinant of interaction diversity in local communities. Our findings emphasize resource similarity as a novel dimension of fragment connectivity relevant in explaining interaction diversity patterns in natural trophic networks.

Unprecedented plant species loss after a decade in fragmented subtropical Chaco Serrano forests.

Current biodiversity loss is mostly caused by anthropogenic habitat loss and fragmentation, climate change, and resource exploitation. Measuring the balance of species loss and gain in remaining fragmented landscapes throughout time entails a central research challenge. We resurveyed in 2013 plant species richness in the same plots of a previous sampling conducted in 2003 across 18 forest fragments of different sizes of the Chaco Serrano forest in Argentina. While the area of these forest remnants was kept constant, their surrounding forest cover changed over this time period. We compared plant species richness of both sampling years and calculated the proportion of species loss and gain at forest edges and interiors. As in 2003, we found a positive relationship between fragment area and plant richness in 2013 and both years showed a similar slope. However, we detected a net decrease of 24% of species' richness across all forest fragments, implying an unprecedentedly high rate and magnitude of species loss driven mainly by non-woody, short-lived species. There was a higher proportion of lost and gained species at forest edges than in forest interiors. Importantly, fragment area interacted with percent change in surrounding forest cover to explain the proportion of species lost. Small forest fragments showed a relatively constant proportion of species loss regardless of any changes in surrounding forest cover, whereas in larger fragments the proportion of species lost increased when surrounding forest cover decreased. We show that despite preserving fragment area, habitat quality and availability in the surroundings is of fundamental importance in shaping extinction and immigration dynamics of plant species at any given forest remnant. Because the Chaco Serrano forest has already lost 94% of its original cover, we argue that plant extinctions will continue through the coming decades unless active management actions are taken to increase native forest areas.

Habitat fragmentation effects on trophic processes of insect-plant food webs.

Habitat fragmentation is the transformation of once-extensive landscapes into smaller isolated remnants surrounded by new types of habitat. There is ample evidence of impoverished biodiversity as a consequence of habitat fragmentation, but its most profound effects may actually result from functional changes in ecological processes such as trophic interactions. We studied the trophic processes of herbivory and parasitism in insect-plant food webs composed of hundreds of species in a fragmented woodland landscape. We recorded all plant species, collected mined leaves, and reared leafminers and parasitoids from 19 woodland remnants. Herbivory and parasitism rates were then analyzed in relation to woodland size and edge or interior location. Herbivory by leaf-mining insects and their overall parasitism rates decreased as woodland remnants became smaller For each remnant the intensity of both processes differed between edge and interior Our results provide novel evidence of the magnitude of habitat fragmentation effects, showing they can be so pervasive as to affect trophic processes of highly complex food webs and suggesting a response associated with trophic specialization of the involved organisms as much as with their trophic level.