Jason M. Tylianakis

Habitat modification alters the structure of tropical host–parasitoid food webs

Global conversion of natural habitats to agriculture has led to marked changes in species diversity and composition. However, it is less clear how habitat modification affects interactions among species. Networks of feeding interactions (food webs) describe the underlying structure of ecological communities, and might be crucially linked to their stability and function. Here, we analyse 48 quantitative food webs for cavity-nesting bees, wasps and their parasitoids across five tropical habitat types. We found marked changes in food-web structure across the modification gradient, despite little variation in species richness. The evenness of interaction frequencies declined with habitat modification, with most energy flowing along one or a few pathways in intensively managed agricultural habitats. In modified habitats there was a higher ratio of parasitoid to host species and increased parasitism rates, with implications for the important ecosystem services, such as pollination and biological control, that are performed by host bees and wasps. The most abundant parasitoid species was more specialized in modified habitats, with reduced attack rates on alternative hosts. Conventional community descriptors failed to discriminate adequately among habitats, indicating that perturbation of the structure and function of ecological communities might be overlooked in studies that do not document and quantify species interactions. Altered interaction structure therefore represents an insidious and functionally important hidden effect of habitat modification by humans.

Functional group diversity of bee pollinators increases crop yield

Niche complementarity is a commonly invoked mechanism underlying the positive relationship between biodiversity and ecosystem functioning, but little empirical evidence exists for complementarity among pollinator species. This study related differences in three functional traits of pollinating bees (flower height preference, daily time of flower visitation and within-flower behaviour) to the seed set of the obligate cross-pollinated pumpkin Cucurbita moschata Duch. ex Poir. across a land-use intensity gradient from tropical rainforest and agroforests to grassland in Indonesia. Bee richness and abundance changed with habitat variables and we used this natural variation to test whether complementary resource use by the diverse pollinator community enhanced final yield. We found that pollinator diversity, but not abundance, was positively related to seed set of pumpkins. Bees showed species-specific spatial and temporal variation in flower visitation traits and within-flower behaviour, allowing for classification into functional guilds. Diversity of functional groups explained even more of the variance in seed set (r2=45%) than did species richness (r2=32%) highlighting the role of functional complementarity. Even though we do not provide experimental, but rather correlative evidence, we can link spatial and temporal complementarity in highly diverse pollinator communities to pollination success in the field, leading to enhanced crop yield without any managed honeybees.

LANDSCAPE CONSTRAINTS ON FUNCTIONAL DIVERSITY OF BIRDS AND INSECTS IN TROPICAL AGROECOSYSTEMS

In this paper, we analyze databases [corrected] on birds and insects to assess patterns of functional diversity in human-dominated landscapes in the tropics. A perspective from developed landscapes is essential for understanding remnant natural ecosystems, because most species experience their surroundings at spatial scales beyond the plot level, and spillover between natural and managed ecosystems is common. Agricultural bird species have greater habitat and diet breadth than forest species. Based on a global data base, bird assemblages in tropical agroforest ecosystems were composed of disproportionately more frugivorous and nectarivorous, but fewer insectivorous bird species compared with forest. Similarly, insect predators of plant-feeding arthropods were more diverse in Ecuadorian agroforest and forest compared with rice and pasture, while, in Indonesia, bee diversity was also higher in forested habitats. Hence, diversity of insectivorous birds and insect predators as well as bee pollinators declined with agricultural transformation. In contrast, with increasing agricultural intensification, avian pollinators and seed dispersers initially increase then decrease in proportion. It is well established that the proximity of agricultural habitats to forests has a strong influence on the functional diversity of agroecosystems. Community similarity is higher among agricultural systems than in natural habitats and higher in simple than in complex landscapes for both birds and insects, so natural communities, low-intensity agriculture, and heterogeneous landscapes appear to be critical in the preservation of beta diversity. We require a better understanding of the relative role of landscape composition and the spatial configuration of landscape elements in affecting spillover of functionally important species across managed and natural habitats. This is important for data-based management of tropical human-dominated landscapes sustaining the capacity of communities to reorganize after disturbance and to ensure ecological functioning.

IMPROVED FITNESS OF APHID PARASITOIDS RECEIVING RESOURCE SUBSIDIES

The availability of nonhost resource subsidies affects the ability of parasitoids to overcome egg and time limitation and maximize lifetime reproductive success. We combined field and laboratory experiments to examine the effects of floral resource subsidies on the reproductive fitness of aphid parasitoids. Under controlled laboratory conditions, sugar resources significantly increased longevity and potential fecundity (egg load) in the endoparasitoids Aphidius rhopalosiphi and Diaeretiella rapae (Hymenoptera: Aphidiidae). Laboratory microcosm experiments showed that increased potential fecundity translated into significantly higher realized fecundity (i.e., rates of aphid parasitism) by A. rhopalosiphi receiving resource subsidies. Mechanisms of enhanced realized fecundity also operated under natural field conditions. Replicated field experiments on cultivated wheat, with host density controlled by experimental placement of aphids, showed that, in general, proximity to floral resource patches significantly increased rates of parasitism. Parasitism rates declined exponentially with increasing distance from floral patches, reaching zero beyond 14 m. Increased potential fecundity reduces the chances of parasitoids becoming egg-limited, whereas increased longevity reduces the chances of parasitoids becoming time-limited during host oviposition. Although the plasticity of egg load and longevity observed under varying conditions of resource availability is probably more relevant to parasitoid evolution, the individual fitness benefits from ephemeral resource patches are certainly important in the ecological enhancement of biological control agents.

Food webs: Reconciling the structure and function of biodiversity

The global biodiversity crisis concerns not only unprecedented loss of species within communities, but also related consequences for ecosystem function. Community ecology focuses on patterns of species richness and community composition, whereas ecosystem ecology focuses on fluxes of energy and materials. Food webs provide a quantitative framework to combine these approaches and unify the study of biodiversity and ecosystem function. We summarise the progression of food-web ecology and the challenges in using the food-web approach. We identify five areas of research where these advances can continue, and be applied to global challenges. Finally, we describe what data are needed in the next generation of food-web studies to reconcile the structure and function of biodiversity.

SPATIOTEMPORAL VARIATION IN THE DIVERSITY OF HYMENOPTERA ACROSS A TROPICAL HABITAT GRADIENT

Understanding global biodiversity patterns requires analyses at multiple spatial and temporal scales, across a variety of different habitat types. We used a highly replicated study in coastal Ecuador to examine simultaneously for the first time spatial and temporal species turnover and the contribution of five different habitat types (rice, pasture, coffee agroforests, abandoned coffee agroforests, and native forest fragments) to regional diversity in the tropics, using the experimental placement of standardized nesting structures for bees and wasps. There was notable overlap in the communities of different habitat types, indicating that even intensively managed land can provide a valuable contribution to the overall biodiversity of the landscape mosaic. Importantly, there was a significant effect of habitat type on temporal variation in diversity. While intensive cropping systems such as rice and pasture exhibited higher diversity in certain months, greater species turnover through time in the abandoned coffee and forest plots accounted for the higher overall diversity in these habitats. Overall, spatial and temporal turnover explained 38.6% and 23.1%, respectively, of partitioned regional species richness. A quantitative analysis revealed that the relative habitat specificity of Hymenoptera decreased with increasing habitat disturbance.

Biodiversity, Species Interactions and Ecological Networks in a Fragmented World

Biodiversity is organised into complex ecological networks of interacting species in local ecosystems, but our knowledge about the effects of habitat fragmentation on such systems remains limited. We consider the effects of this key driver of both local and global change on both mutualistic and antagonistic systems at different levels of biological organisation and spatiotemporal scales. There is a complex interplay of patterns and processes related to the variation and influence of spatial, temporal and biotic drivers in ecological networks. Species traits (e.g. body size, dispersal ability) play an important role in determining how networks respond to fragment size and isolation, edge shape and permeability, and the quality of the surrounding landscape matrix. Furthermore, the perception of spatial scale (e.g. environmental grain) and temporal effects (time lags, extinction debts) can differ markedly among species, network modules and trophic levels, highlighting the need to develop a more integrated perspective that considers not just nodes, but the structural role and strength of species interactions (e.g. as hubs, spatial couplers and determinants of connectance, nestedness and modularity) in response to habitat fragmentation. Many challenges remain for improving our understanding: the likely importance of specialisation, functional redundancy and trait matching has been largely overlooked. The potentially critical effects of apex consumers, abundant species and super-generalists on network changes and evolutionary dynamics also need to be addressed in future research. Ultimately, spatial and ecological networks need to be combined to explore the effects of dispersal, colonisation, extinction and habitat fragmentation on network structure and coevolutionary dynamics. Finally, we need to embed network approaches more explicitly within applied ecology in general, because they offer great potential for improving on the current species-based or habitat-centric approaches to our management and conservation of biodiversity in the face of environmental change.

Resource Heterogeneity Moderates the Biodiversity-Function Relationship in Real World Ecosystems

Numerous recent studies have tested the effects of plant, pollinator, and predator diversity on primary productivity, pollination, and consumption, respectively. Many have shown a positive relationship, particularly in controlled experiments, but variability in results has emphasized the context-dependency of these relationships. Complementary resource use may lead to a positive relationship between diversity and these processes, but only when a diverse array of niches is available to be partitioned among species. Therefore, the slope of the diversity-function relationship may change across differing levels of heterogeneity, but empirical evaluations of this pattern are lacking. Here we examine three important functions/properties in different real world (i.e., nonexperimental) ecosystems: plant biomass in German grasslands, parasitism rates across five habitat types in coastal Ecuador, and coffee pollination in agroforestry systems in Indonesia. We use general linear and structural equation modeling to demonstrate that the effect of diversity on these processes is context dependent, such that the slope of this relationship increases in environments where limiting resources (soil nutrients, host insects, and coffee flowers, respectively) are spatially heterogeneous. These real world patterns, combined with previous experiments, suggest that biodiversity may have its greatest impact on the functioning of diverse, naturally heterogeneous ecosystems.

Specialization and Rarity Predict Nonrandom Loss of Interactions from Mutualist Networks

Untangling the Web Interspecific interactions link species within complex trophic and nontrophic webs (see the Perspective by Lewinsohn and Cagnolo). Theoretical work has suggested that certain characteristics of species, or even interactions, may predispose them to extinction from a network. Aizen et al. (p. 1486) provide empirical evidence that plant-pollinator interactions are lost nonrandomly following habitat reduction in isolated hills in the Argentine pampas. Some types of interaction were more vulnerable to disruption than others, particularly when the specialization of the interacting was high and when the interactions were infrequent. Stouffer et al. (p. 1489) applied network theory to predict the dynamical importance of species across different food webs. Characteristic three-node motifs were identified, and species were characterized according to the relative frequencies with which they occupied unique positions within the motifs. These relative frequencies and the dynamic importance of the motifs were then used to identify a species-level importance within a food web. In the sierras of Argentina, specialized mutualistic plant-pollinator relationships increase vulnerability to habitat loss. The loss of interactions from mutualistic networks could foreshadow both plant and animal species extinctions. Yet, the characteristics of interactions that predispose them to disruption are largely unknown. We analyzed 12 pollination webs from isolated hills (“sierras”), in Argentina, ranging from tens to thousands of hectares. We found evidence of nonrandom loss of interactions with decreasing sierra size. Low interaction frequency and high specialization between interacting partners contributed additively to increase the vulnerability of interactions to disruption. Interactions between generalists in the largest sierras were ubiquitous across sierras, but many of them lost their central structural role in the smallest sierras. Thus, particular configurations of interaction networks, along with unique ecological relations and evolutionary pathways, could be lost forever after habitat reduction.

Diversity, ecosystem function, and stability of parasitoid-host interactions across a tropical habitat gradient.

Global biodiversity decline has prompted great interest in the effects of habitat modification and diversity on the functioning and stability of ecosystem processes. However, the applicability of previous modeled or mesocosm community studies to real diverse communities in different habitats remains ambiguous. We exposed standardized nesting resources for naturally occurring communities of cavity-nesting bees and wasps and their parasitoids in coastal Ecuador, to test the effects of host and parasitoid diversity on an ecosystem function (parasitism rates) and temporal variability in this function. In accordance with predictions of complementary host use, parasitism rates increased with increasing diversity, not simply abundance, of parasitoids. In contrast, parasitism decreased with increasing host diversity, possibly due to positive prey interactions or increased probability of selecting unpalatable species. Temporal variability in parasitism was lower in plots with high mean parasitoid diversity and higher in plots with temporally variable host and parasitoid diversity. These effects of diversity on parasitism and temporal stability in parasitism rates were sufficiently strong to be visible across five different habitat types, representing a gradient of increasing anthropogenic modification. Habitat type did not directly affect parasitism rates, but host and parasitoid diversity and abundance were higher in highly modified habitats, and parasitoid diversity was positively correlated with rates of parasitism. The slope of the richness-parasitism relationship did not vary significantly across habitats, although that for Simpsons diversity was significant only in rice and pasture. We also show that pooling data over long time periods, as in previous studies, can blur the effect of diversity on parasitism rates, and the appropriate spatiotemporal scale of study must be considered.