Hierarchical compound topology uncovers complex structure of species interaction networks.

Nestedness and modularity have been found in many species interaction networks. Despite being conceptually distinct, negatively correlated and having different causes, these patterns often co-occur. A realistic but seldom investigated alternative to these simple topologies is hierarchical compound networks, in which the entire network is modular, and modules are internally nested. In compound networks, nestedness is suppressed by modularity at higher network hierarchical levels, but prevails at lower levels, within modules. The aims of this study are (i) to evaluate the prevalence of simple and hierarchical compound topologies in binary and weighted networks describing different kinds of species interactions and (ii) to probe the relationships between modularity and nestedness at different network hierarchical levels. With a procedure that discriminates between simple and compound structures, we re-analysed the topology of 142 well-studied binary networks including seed dispersal, host-parasite, pollination and plant-herbivore interactions; 68 of these also had quantitative information. Additionally, we tested the relationship between robustness and topology of binary networks and compared the robustness of networks with compound topologies to different sequences of species removals. Compound topologies were detected in 34% of binary and 71% of weighted networks of all interaction kinds. These results establish the hierarchical compound topology as a widespread network architecture, often undetected without quantitative data. Furthermore, they disentangle an apparent paradox: despite conflicting with overall nestedness, modularity usually co-occurs with high values of low-level nestedness. Nestedness progressively decreased, while modularity increased, from seed dispersal to host-parasite, pollination and plant-herbivore networks. There were no consistent differences in the robustness of networks with nested and compound topologies. However, compound topologies were especially vulnerable to removal sequences that accelerate the exclusion of entire modules. Compound topologies improve the depiction of ecological networks and differentiate ecological and evolutionary processes that operate at different hierarchical levels, with the potential to advance our understanding of network dynamics, stability and response to species loss or change. Quantitative data often reveal specialization patterns that are indistinguishable in binary networks, strongly improving the detection of modular and compound topologies.

Insect decline in Brazil: an appraisal of current evidence.

Recent reviews of data on worldwide insect decline include almost no information on Brazil. We gathered evidence from literature searches and a survey sent to researchers, to which 96 replied and 56 provided information and publications. We present 75 instances of trends recorded over an average span of 11 years for aquatic and 22 years for terrestrial insects. These include time-replicated samples and expert opinion based on long-term local collections. Most terrestrial data are for butterflies, bees and scarab beetles. Aquatic studies include several insect orders, usually sorted to genus or family. Terrestrial insects showed significantly more cases of declines than increases, both in abundance (17 : 3) and in diversity (11 : 1). In aquatic cases, no tendency was detected in abundance (2 : 2) or diversity (3 : 4), not counting cases with no trend. Differences in these results among habitats may be due to the shorter span and less change in environmental conditions in the aquatic surveys, which included sites already degraded before sampling. We offer guidelines for future long-term assessments, including resampling of legacy collection sites.

Mutual Information as a General Measure of Structure in Interaction Networks.

Entropy-based indices are long-established measures of biological diversity, nowadays used to gauge partitioning of diversity at different spatial scales. Here, we tackle the measurement of diversity of interactions among two sets of organisms, such as plants and their pollinators. Actual interactions in ecological communities are depicted as bipartite networks or interaction matrices. Recent studies concentrate on distinctive structural patterns, such as nestedness or modularity, found in different modes of interaction. By contrast, we investigate mutual information as a general measure of structure in interactive networks. Mutual information (MI) measures the degree of reciprocal matching or specialization between interacting organisms. To ascertain its usefulness as a general measure, we explore (a) analytical solutions for different models; (b) the response of MI to network parameters, especially size and occupancy; (c) MI in nested, modular, and compound topologies. MI varies with fundamental matrix parameters: dimension and occupancy, for which it can be adjusted or normalized. Apparent differences among topologies are contingent on dimensions and occupancy, rather than on topological patterns themselves. As a general measure of interaction structure, MI is applicable to conceptually and empirically fruitful analyses, such as comparing similar ecological networks along geographical gradients or among interaction modalities in mutualistic or antagonistic networks.

The Role of Evolution in Shaping Ecological Networks.

The structure of ecological networks reflects the evolutionary history of their biotic components, and their dynamics are strongly driven by ecoevolutionary processes. Here, we present an appraisal of recent relevant research, in which the pervasive role of evolution within ecological networks is manifest. Although evolutionary processes are most evident at macroevolutionary scales, they are also important drivers of local network structure and dynamics. We propose components of a blueprint for further research, emphasising process-based models, experimental evolution, and phenotypic variation, across a range of distinct spatial and temporal scales. Evolutionary dimensions are required to advance our understanding of foundational properties of community assembly and to enhance our capability of predicting how networks will respond to impending changes.

Phylogenetic trophic specialization: a robust comparison of herbivorous guilds.

Resource specialization is a key concept in ecology, but it is unexpectedly difficult to parameterize. Differences in resource availability, sampling effort and abundances preclude comparisons of incompletely sampled biotic interaction webs. Here, we extend the distance-based specialization index (DSI) that measures trophic specialization by taking resource phylogenetic relatedness and availability into account into a rescaled version, DSI*. It is a versatile metric of specialization that expands considerably the scope and applicability, hence the usefulness, of DSI. The new metric also accounts for differences in abundance and sampling effort of consumers, which enables robust comparisons among distinct guilds of consumers. It also provides an abundance threshold for the reliability of the metric for rare species, a very desirable property given the difficulty of assessing any aspect of rare species accurately. We apply DSI* to an extensive dataset on interactions between insect herbivores from four folivorous guilds and their host plants in Papua New Guinean rainforests. We demonstrate that DSI*, contrary to the original DSI, is largely independent of sample size and weakly and non-linearly related with several host specificity measures that do not adjust for plant phylogeny. Thus, DSI* provides further insights into host specificity patterns; moreover, it is robust to the number and phylogenetic diversity of plant species selected to be sampled for herbivores. DSI* can be used for a broad range of comparisons of distinct feeding guilds, geographical locations and ecological conditions. This is a key advance in elucidating the interaction structure and evolution of highly diversified systems.

Land-use intensification causes multitrophic homogenization of grassland communities.

Land-use intensification is a major driver of biodiversity loss. Alongside reductions in local species diversity, biotic homogenization at larger spatial scales is of great concern for conservation. Biotic homogenization means a decrease in ß-diversity (the compositional dissimilarity between sites). Most studies have investigated losses in local (α)-diversity and neglected biodiversity loss at larger spatial scales. Studies addressing ß-diversity have focused on single or a few organism groups (for example, ref. 4), and it is thus unknown whether land-use intensification homogenizes communities at different trophic levels, above- and belowground. Here we show that even moderate increases in local land-use intensity (LUI) cause biotic homogenization across microbial, plant and animal groups, both above- and belowground, and that this is largely independent of changes in α-diversity. We analysed a unique grassland biodiversity dataset, with abundances of more than 4,000 species belonging to 12 trophic groups. LUI, and, in particular, high mowing intensity, had consistent effects on ß-diversity across groups, causing a homogenization of soil microbial, fungal pathogen, plant and arthropod communities. These effects were nonlinear and the strongest declines in ß-diversity occurred in the transition from extensively managed to intermediate intensity grassland. LUI tended to reduce local α-diversity in aboveground groups, whereas the α-diversity increased in belowground groups. Correlations between the ß-diversity of different groups, particularly between plants and their consumers, became weaker at high LUI. This suggests a loss of specialist species and is further evidence for biotic homogenization. The consistently negative effects of LUI on landscape-scale biodiversity underscore the high value of extensively managed grasslands for conserving multitrophic biodiversity and ecosystem service provision. Indeed, biotic homogenization rather than local diversity loss could prove to be the most substantial consequence of land-use intensification.

Host-Plant Specialization Mediates the Influence of Plant Abundance on Host Use by Flower Head-Feeding Insects.

Among-population variation in host use is a common phenomenon in herbivorous insects. The simplest and most trivial explanation for such variation in host use is the among-site variation in plant species composition. Another aspect that can influence spatial variation in host use is the relative abundance of each host-plant species compared to all available hosts. Here, we used endophagous insects that develop in flower heads of Asteraceae species as a study system to investigate how plant abundance influences the pattern of host-plant use by herbivorous insects with distinct levels of host-range specialization. Only herbivores recorded on three or more host species were included in this study. In particular, we tested two related hypotheses: 1) plant abundance has a positive effect on the host-plant preference of herbivorous insects, and 2) the relative importance of plant abundance to host-plant preference is greater for herbivorous species that use a wider range of host-plant species. We analyzed 11 herbivore species in 20 remnants of Cerrado in Southeastern Brazil. For 8 out of 11 herbivore species, plant abundance had a positive influence on host use. In contrast to our expectation, both the most specialized and the most generalist herbivores showed a stronger positive effect of plant species abundance in host use. Thus, we found evidence that although the abundance of plant species is a major factor determining the preferential use of host plants, its relative importance is mediated by the host-range specialization of herbivores.

Arthropod Distribution in a Tropical Rainforest: Tackling a Four Dimensional Puzzle.

Quantifying the spatio-temporal distribution of arthropods in tropical rainforests represents a first step towards scrutinizing the global distribution of biodiversity on Earth. To date most studies have focused on narrow taxonomic groups or lack a design that allows partitioning of the components of diversity. Here, we consider an exceptionally large dataset (113,952 individuals representing 5,858 species), obtained from the San Lorenzo forest in Panama, where the phylogenetic breadth of arthropod taxa was surveyed using 14 protocols targeting the soil, litter, understory, lower and upper canopy habitats, replicated across seasons in 2003 and 2004. This dataset is used to explore the relative influence of horizontal, vertical and seasonal drivers of arthropod distribution in this forest. We considered arthropod abundance, observed and estimated species richness, additive decomposition of species richness, multiplicative partitioning of species diversity, variation in species composition, species turnover and guild structure as components of diversity. At the scale of our study (2 km of distance, 40 m in height and 400 days), the effects related to the vertical and seasonal dimensions were most important. Most adult arthropods were collected from the soil/litter or the upper canopy and species richness was highest in the canopy. We compared the distribution of arthropods and trees within our study system. Effects related to the seasonal dimension were stronger for arthropods than for trees. We conclude that: (1) models of beta diversity developed for tropical trees are unlikely to be applicable to tropical arthropods; (2) it is imperative that estimates of global biodiversity derived from mass collecting of arthropods in tropical rainforests embrace the strong vertical and seasonal partitioning observed here; and (3) given the high species turnover observed between seasons, global climate change may have severe consequences for rainforest arthropods.

Contrasting effects of land use intensity and exotic host plants on the specialization of interactions in plant-herbivore networks.

Human land use tends to decrease the diversity of native plant species and facilitate the invasion and establishment of exotic ones. Such changes in land use and plant community composition usually have negative impacts on the assemblages of native herbivorous insects. Highly specialized herbivores are expected to be especially sensitive to land use intensification and the presence of exotic plant species because they are neither capable of consuming alternative plant species of the native flora nor exotic plant species. Therefore, higher levels of land use intensity might reduce the proportion of highly specialized herbivores, which ultimately would lead to changes in the specialization of interactions in plant-herbivore networks. This study investigates the community-wide effects of land use intensity on the degree of specialization of 72 plant-herbivore networks, including effects mediated by the increase in the proportion of exotic plant species. Contrary to our expectation, the net effect of land use intensity on network specialization was positive. However, this positive effect of land use intensity was partially canceled by an opposite effect of the proportion of exotic plant species on network specialization. When we analyzed networks composed exclusively of endophagous herbivores separately from those composed exclusively of exophagous herbivores, we found that only endophages showed a consistent change in network specialization at higher land use levels. Altogether, these results indicate that land use intensity is an important ecological driver of network specialization, by way of reducing the local host range of herbivore guilds with highly specialized feeding habits. However, because the effect of land use intensity is offset by an opposite effect owing to the proportion of exotic host species, the net effect of land use in a given herbivore assemblage will likely depend on the extent of the replacement of native host species with exotic ones.

Effects of land-use intensity on arthropod species abundance distributions in grasslands.

As a rule, communities consist of few abundant and many rare species, which is reflected in the characteristic shape of species abundance distributions (SADs). The processes that shape these SADs have been a longstanding problem for ecological research. Although many studies found strong negative effects of increasing land-use intensity on diversity, few reports consider land-use effects on SADs. Arthropods (insects and spiders) were sampled on 142 grassland plots in three regions in Germany, which were managed with different modes (mowing, fertilization and/or grazing) and intensities of land use. We analysed the effect of land use on three parameters characterizing the shape of SADs: abundance decay rate (the steepness of the rank abundance curve, represented by the niche-preemption model parameter), dominance (Berger-Parker dominance) and rarity (Fisher's alpha). Furthermore, we tested the core-satellite hypothesis by comparing the species' rank within the SAD to their distribution over the land-use gradient. When data on Araneae, Cicadina, Coleoptera, Heteroptera and Orthoptera were combined, abundance decay rate increased with combined land-use intensity (including all modes). Among the single land-use modes, increasing fertilization and grazing intensity increased the decay rate of all taxa, while increasing mowing frequency significantly affected the decay rate only in interaction with fertilization. Results of single taxa differed in their details, but all significant interaction effects included fertilization intensity. Dominance generally increased with increasing fertilization and rarity decreased with increasing grazing or mowing intensity, despite small differences among taxa and regions. The majority of species found on <10% of the plots per region were generally rare (<10 individuals), which is in accordance with the core-satellite hypothesis. We found significant differences in the rarity and dominance of species between plots of low and high intensity for all three land-use modes and for the combined land-use intensity. We conclude that effects of land-use intensity on SADs lead to a stronger dominance of the most abundant species. Furthermore, species which have restricted distributions are more likely to also be rare species in the local SAD and therefore are at high risk of being lost under intensive land use.

Ecological literacy and beyond: Problem-based learning for future professionals.

Ecological science contributes to solving a broad range of environmental problems. However, lack of ecological literacy in practice often limits application of this knowledge. In this paper, we highlight a critical but often overlooked demand on ecological literacy: to enable professionals of various careers to apply scientific knowledge when faced with environmental problems. Current university courses on ecology often fail to persuade students that ecological science provides important tools for environmental problem solving. We propose problem-based learning to improve the understanding of ecological science and its usefulness for real-world environmental issues that professionals in careers as diverse as engineering, public health, architecture, social sciences, or management will address. Courses should set clear learning objectives for cognitive skills they expect students to acquire. Thus, professionals in different fields will be enabled to improve environmental decision-making processes and to participate effectively in multidisciplinary work groups charged with tackling environmental issues.

Resource-mediated indirect effects of grassland management on arthropod diversity.

Intensive land use is a driving force for biodiversity decline in many ecosystems. In semi-natural grasslands, land-use activities such as mowing, grazing and fertilization affect the diversity of plants and arthropods, but the combined effects of different drivers and the chain of effects are largely unknown. In this study we used structural equation modelling to analyse how the arthropod communities in managed grasslands respond to land use and whether these responses are mediated through changes in resource diversity or resource quantity (biomass). Plants were considered resources for herbivores which themselves were considered resources for predators. Plant and arthropod (herbivores and predators) communities were sampled on 141 meadows, pastures and mown pastures within three regions in Germany in 2008 and 2009. Increasing land-use intensity generally increased plant biomass and decreased plant diversity, mainly through increasing fertilization. Herbivore diversity decreased together with plant diversity but showed no response to changes in plant biomass. Hence, land-use effects on herbivore diversity were mediated through resource diversity rather than quantity. Land-use effects on predator diversity were mediated by both herbivore diversity (resource diversity) and herbivore quantity (herbivore biomass), but indirect effects through resource quantity were stronger. Our findings highlight the importance of assessing both direct and indirect effects of land-use intensity and mode on different trophic levels. In addition to the overall effects, there were subtle differences between the different regions, pointing to the importance of regional land-use specificities. Our study underlines the commonly observed strong effect of grassland land use on biodiversity. It also highlights that mechanistic approaches help us to understand how different land-use modes affect biodiversity.

An integrated framework to improve the concept of resource specialisation.

Resource specialisation, although a fundamental component of ecological theory, is employed in disparate ways. Most definitions derive from simple counts of resource species. We build on recent advances in ecophylogenetics and null model analysis to propose a concept of specialisation that comprises affinities among resources as well as their co-occurrence with consumers. In the distance-based specialisation index (DSI), specialisation is measured as relatedness (phylogenetic or otherwise) of resources, scaled by the null expectation of random use of locally available resources. Thus, specialists use significantly clustered sets of resources, whereas generalists use over-dispersed resources. Intermediate species are classed as indiscriminate consumers. The effectiveness of this approach was assessed with differentially restricted null models, applied to a data set of 168 herbivorous insect species and their hosts. Incorporation of plant relatedness and relative abundance greatly improved specialisation measures compared to taxon counts or simpler null models, which overestimate the fraction of specialists, a problem compounded by insufficient sampling effort. This framework disambiguates the concept of specialisation with an explicit measure applicable to any mode of affinity among resource classes, and is also linked to ecological and evolutionary processes. This will enable a more rigorous deployment of ecological specialisation in empirical and theoretical studies.

Bottom-up multitrophic effects in resprouting plants.

Severe damage often provokes compensatory resprouting of plants, which commonly modify plant morphological and phenological traits. Rapid plant growth often results in poorly defended nutrient-rich foliage, which is more susceptible to foliar-chewing herbivores. It is less known how other guilds of arthropods are affected by plant regrowth. We tested the hypotheses that clipping-induced resprouting and nutrient availability, separately and in combination, would (1) influence plant traits, (2) benefit chewing herbivores, sap-suckers, gallers, and pre-dispersal seed predators, and (3) cascade up to the third trophic level by positively affecting herbivores. Resprouted plants were morphologically and phenologically different from undamaged plants; as a result, seed predation, infestation rate, richness, and diversity of seed predators increased, and species composition was altered. Leaf consumption by chewing herbivores was four times higher on resprouted plants. The number of galls decreased, whereas the abundance of sap-sucking and leaf-chewing insects was not affected. The incidence of predators and parasitoids was also higher on resprouted plants and on plants with nutrients added, but the increase was less pronounced compared to the herbivores they feed on. Thus, the effects of resprouting, contingent on nutrient availability, can propagate simultaneously through two independent tri-trophic level pathways.

Phytophagous insect fauna tracks host plant responses to exotic grass invasion.

The high dependence of herbivorous insects on their host plants implies that plant invaders can affect these insects directly, by not providing a suitable habitat, or indirectly, by altering host plant availability. In this study, we sampled Asteraceae flower heads in cerrado remnants with varying levels of exotic grass invasion to evaluate whether invasive grasses have a direct effect on herbivore richness independent of the current disturbance level and host plant richness. By classifying herbivores according to the degree of host plant specialization, we also investigated whether invasive grasses reduce the uniqueness of the herbivorous assemblages. Herbivorous insect richness showed a unimodal relationship with invasive grass cover that was significantly explained only by way of the variation in host plant richness. The same result was found for polyphagous and oligophagous insects, but monophages showed a significant negative response to the intensity of the grass invasion that was independent of host plant richness. Our findings lend support to the hypothesis that the aggregate effect of invasive plants on herbivores tends to mirror the effects of invasive plants on host plants. In addition, exotic plants affect specialist insects differently from generalist insects; thus exotic plants affect not only the size but also the structural profile of herbivorous insect assemblages.

A large trophic quilt.

Plants and invertebrate herbivores are major constituents of terrestrial food webs. Identifying component species and tracing their interactions in highly diverse communities are a monumental task. Novotny et al. 2010 present the first broad conspectus of herbivore­plant interactions in a forest in Papua New Guinea. In more than 15 years, nearly 7000 feeding links were traced between about 200 plants and 1500 insect herbivores. Although staggering, these figures might represent only 15% of the total herbivore richness and interaction diversity in that lowland forest. Standardized comparisons also showed distinctive specialization and diversification patterns in different feeding guilds, restricting the possibility of using any single guild as surrogate for the entire assemblage.