Nico Blüthgen

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.

Specialization, constraints, and conflicting interests in mutualistic networks.

The topology of ecological interaction webs holds important information for theories of coevolution, biodiversity, and ecosystem stability . However, most previous network analyses solely counted the number of links and ignored variation in link strength. Because of this crude resolution, results vary with scale and sampling intensity, thus hampering a comparison of network patterns at different levels . We applied a recently developed quantitative and scale-independent analysis based on information theory to 51 mutualistic plant-animal networks, with interaction frequency as measure of link strength. Most networks were highly structured, deviating significantly from random associations. The degree of specialization was independent of network size. Pollination webs were significantly more specialized than seed-dispersal webs, and obligate symbiotic ant-plant mutualisms were more specialized than nectar-mediated facultative ones. Across networks, the average specialization of animal and plants was correlated, but is constrained by the ratio of plant to animal species involved. In pollination webs, rarely visited plants were on average more specialized than frequently attended ones, whereas specialization of pollinators was positively correlated with their interaction frequency. We conclude that quantitative specialization in ecological communities mirrors evolutionary trade-offs and constraints of web architecture. This approach can be easily expanded to other types of biological interactions.

How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew

Abstract. Ant-plant interactions in the canopy of a lowland Amazonian rainforest of the upper Orinoco, Venezuela, were studied using a modified commercial crane on rails (Surumoni project). Our observations show a strong correlation between plant sap exudates and both abundance of ants and co-occurrence of ant species in tree canopies. Two types of plant sap sources were compared: extrafloral nectaries (EFNs) and honeydew secretions by homopterans. EFNs were a frequent food source for ants on epiphytes (Philodendron spp., Araceae) and lianas (Dioclea, Fabaceae), but rare on canopy trees in the study area, whereas the majority of trees were host to aggregations of homopterans tended by honeydew-seeking ants (on 62% of the trees examined). These aggregations rarely occurred on epiphytes. Baited ant traps were installed on plants with EFNs and in the crowns of trees from three common genera, including trees with and without ant-tended homopterans: Goupia glabra (Celastraceae), Vochysia spp. (Vochysiaceae), and Xylopia spp. (Annonaceae). The number of ant workers per trap was significantly higher on plants offering one of the two plant sap sources than on trees without such resources. Extrafloral nectaries were used by a much broader spectrum of ant species and genera than honeydew, and co-occurrence of ant species (in traps) was significantly higher on plants bearing EFNs than on trees. Homopteran honeydew (Coccidae and Membracidae), on the other hand, was mostly monopolised by a single ant colony per tree. Homopteran-tending ants were generally among the most dominant ants in the canopy. The most prominent genera were Azteca, Dolichoderus (both Dolichoderinae), Cephalotes, Pheidole, Crematogaster (all Myrmicinae), and Ectatomma (Ponerinae). Potential preferences were recorded between ant and homopteran species, and also between ant-homopteran associations and tree genera. We hypothesize that the high availability of homopteran honeydew provides a key resource for ant mosaics, where dominant ant colonies and species maintain mutually exclusive territories on trees. In turn, we propose that for nourishment of numerous ants of lower competitive capacity, Philodendron and other sources of EFNs might be particularly important.

Specialization of mutualistic interaction networks decreases toward tropical latitudes.

Species-rich tropical communities are expected to be more specialized than their temperate counterparts. Several studies have reported increasing biotic specialization toward the tropics, whereas others have not found latitudinal trends once accounting for sampling bias or differences in plant diversity. Thus, the direction of the latitudinal specialization gradient remains contentious. With an unprecedented global data set, we investigated how biotic specialization between plants and animal pollinators or seed dispersers is associated with latitude, past and contemporary climate, and plant diversity. We show that in contrast to expectation, biotic specialization of mutualistic networks is significantly lower at tropical than at temperate latitudes. Specialization was more closely related to contemporary climate than to past climate stability, suggesting that current conditions have a stronger effect on biotic specialization than historical community stability. Biotic specialization decreased with increasing local and regional plant diversity. This suggests that high specialization of mutualistic interactions is a response of pollinators and seed dispersers to low plant diversity. This could explain why the latitudinal specialization gradient is reversed relative to the latitudinal diversity gradient. Low mutualistic network specialization in the tropics suggests higher tolerance against extinctions in tropical than in temperate communities.

COMPETITION FOR COMPOSITION: LESSONS FROM NECTAR-FEEDING ANT COMMUNITIES

Studies of the relationship between the composition of nectar and its consumers often focus on single or very few species, thus ignoring dynamics in diverse assemblages. Conversely, most documented patterns of nectarivore communities have not been linked to nectar quality measures. In a study of nectar-foraging ant communities in an Australian rain forest, we found that nectar source partitioning between consumers may be driven by two factors: (1) variation in nectar composition preferences mediated by taste and physiological requirements, and (2) severe asymmetrical competitive interactions within the community. Ant communities are strongly shaped by competitive hierarchies. When foraging for extrafloral and floral nectar sources, wound sap, and homopteran honeydew, competitively superior weaver-ants (Oecophylla smaragdina) showed a significant preference for nectar composition, whereas most other common community members were nonselective. Nectars frequently used by O. smaragdina were characterized by s...

Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality

Many experiments have shown that loss of biodiversity reduces the capacity of ecosystems to provide the multiple services on which humans depend. However, experiments necessarily simplify the complexity of natural ecosystems and will normally control for other important drivers of ecosystem functioning, such as the environment or land use. In addition, existing studies typically focus on the diversity of single trophic groups, neglecting the fact that biodiversity loss occurs across many taxa and that the functional effects of any trophic group may depend on the abundance and diversity of others. Here we report analysis of the relationships between the species richness and abundance of nine trophic groups, including 4,600 above- and below-ground taxa, and 14 ecosystem services and functions and with their simultaneous provision (or multifunctionality) in 150 grasslands. We show that high species richness in multiple trophic groups (multitrophic richness) had stronger positive effects on ecosystem services than richness in any individual trophic group; this includes plant species richness, the most widely used measure of biodiversity. On average, three trophic groups influenced each ecosystem service, with each trophic group influencing at least one service. Multitrophic richness was particularly beneficial for ‘regulating’ and ‘cultural’ services, and for multifunctionality, whereas a change in the total abundance of species or biomass in multiple trophic groups (the multitrophic abundance) positively affected supporting services. Multitrophic richness and abundance drove ecosystem functioning as strongly as abiotic conditions and land-use intensity, extending previous experimental results to real-world ecosystems. Primary producers, herbivorous insects and microbial decomposers seem to be particularly important drivers of ecosystem functioning, as shown by the strong and frequent positive associations of their richness or abundance with multiple ecosystem services. Our results show that multitrophic richness and abundance support ecosystem functioning, and demonstrate that a focus on single groups has led to researchers to greatly underestimate the functional importance of biodiversity.

Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition

Abstract Global change, especially land‐use intensification, affects human well‐being by impacting the delivery of multiple ecosystem services (multifunctionality). However, whether biodiversity loss is a major component of global change effects on multifunctionality in real‐world ecosystems, as in experimental ones, remains unclear. Therefore, we assessed biodiversity, functional composition and 14 ecosystem services on 150 agricultural grasslands differing in land‐use intensity. We also introduce five multifunctionality measures in which ecosystem services were weighted according to realistic land‐use objectives. We found that indirect land‐use effects, i.e. those mediated by biodiversity loss and by changes to functional composition, were as strong as direct effects on average. Their strength varied with land‐use objectives and regional context. Biodiversity loss explained indirect effects in a region of intermediate productivity and was most damaging when land‐use objectives favoured supporting and cultural services. In contrast, functional composition shifts, towards fast‐growing plant species, strongly increased provisioning services in more inherently unproductive grasslands.

The same, but different: pollen foraging in honeybee and bumblebee colonies

Like many other bees worldwide, honeybees and bumblebees are threatened by human-induced disturbances. Yet some species decline and others thrive, likely due to different foraging strategies. As little is known about how resource intake translates into nutrients available to colonies, our study aimed to better understand how differences in foraging strategies may affect colony health by relating differences in pollen spectra collected to differences in nutrient composition. The Apis and Bombus colonies studied were all located at the same site, but nevertheless differed in the spectra of plant species visited for pollen collection and the quality of pollen collected. Bumblebees generally collected pollen with significantly higher pollen protein content and more essential amino acids. Unlike honeybees that tend to exploit large resource patches, bumblebees thus seem to select the “better” pollen and to focus on quality instead of quantity.

Landscape simplification filters species traits and drives biotic homogenization

Biodiversity loss can affect the viability of ecosystems by decreasing the ability of communities to respond to environmental change and disturbances. Agricultural intensification is a major driver of biodiversity loss and has multiple components operating at different spatial scales: from in-field management intensity to landscape-scale simplification. Here we show that landscape-level effects dominate functional community composition and can even buffer the effects of in-field management intensification on functional homogenization, and that animal communities in real-world managed landscapes show a unified response (across orders and guilds) to both landscape-scale simplification and in-field intensification. Adults and larvae with specialized feeding habits, species with shorter activity periods and relatively small body sizes are selected against in simplified landscapes with intense in-field management. Our results demonstrate that the diversity of land cover types at the landscape scale is critical for maintaining communities, which are functionally diverse, even in landscapes where in-field management intensity is high.

Interannual variation in land-use intensity enhances grassland multidiversity

Significance Land-use intensification is a major threat to biodiversity. So far, however, studies on biodiversity impacts of land-use intensity (LUI) have been limited to a single or few groups of organisms and have not considered temporal variation in LUI. Therefore, we examined total ecosystem biodiversity in grasslands varying in LUI with a newly developed index called multidiversity, which integrates the species richness of 49 different organism groups ranging from bacteria to birds. Multidiversity declined strongly with increasing LUI, but changing LUI across years increased multidiversity, particularly of rarer species. We conclude that encouraging farmers to change the intensity of their land use over time could be an important strategy to maintain high biodiversity in grasslands. Although temporal heterogeneity is a well-accepted driver of biodiversity, effects of interannual variation in land-use intensity (LUI) have not been addressed yet. Additionally, responses to land use can differ greatly among different organisms; therefore, overall effects of land-use on total local biodiversity are hardly known. To test for effects of LUI (quantified as the combined intensity of fertilization, grazing, and mowing) and interannual variation in LUI (SD in LUI across time), we introduce a unique measure of whole-ecosystem biodiversity, multidiversity. This synthesizes individual diversity measures across up to 49 taxonomic groups of plants, animals, fungi, and bacteria from 150 grasslands. Multidiversity declined with increasing LUI among grasslands, particularly for rarer species and aboveground organisms, whereas common species and belowground groups were less sensitive. However, a high level of interannual variation in LUI increased overall multidiversity at low LUI and was even more beneficial for rarer species because it slowed the rate at which the multidiversity of rare species declined with increasing LUI. In more intensively managed grasslands, the diversity of rarer species was, on average, 18% of the maximum diversity across all grasslands when LUI was static over time but increased to 31% of the maximum when LUI changed maximally over time. In addition to decreasing overall LUI, we suggest varying LUI across years as a complementary strategy to promote biodiversity conservation.