Mark Emmerson

Identification of 100 fundamental ecological questions

Summary 1. Fundamental ecological research is both intrinsically interesting and provides the basic knowledge required to answer applied questions of importance to the management of the natural world. The 100th anniversary of the British Ecological Society in 2013 is an opportune moment to reflect on the current status of ecology as a science and look forward to high-light priorities for future work.

Consistent patterns and the idiosyncratic effects of biodiversity in marine ecosystems

Revealing the consequences of species extinctions for ecosystem function has been a chief research goal and has been accompanied by enthusiastic debate. Studies carried out predominantly in terrestrial grassland and soil ecosystems have demonstrated that as the number of species in assembled communities increases, so too do certain ecosystem processes, such as productivity, whereas others such as decomposition can remain unaffected. Diversity can influence aspects of ecosystem function, but questions remain as to how generic the patterns observed are, and whether they are the product of diversity, as such, or of the functional roles and traits that characterize species in ecological systems. Here we demonstrate variable diversity effects for species representative of marine coastal systems at both global and regional scales. We provide evidence for an increase in complementary resource use as diversity increases and show strong evidence for diversity effects in naturally assembled communities at a regional scale. The variability among individual species responses is consistent with a positive but idiosyncratic pattern of ecosystem function with increased diversity.

UNDERSTANDING AND PREDICTING ECOLOGICAL DYNAMICS: ARE MAJOR SURPRISES INEVITABLE

Ecological surprises, substantial and unanticipated changes in the abundance of one or more species that result from previously unsuspected processes, are a common outcome of both experiments and observations in community and population ecology. Here, we give examples of such surprises along with the results of a survey of well-established field ecologists, most of whom have encountered one or more surprises over the course of their careers. Truly surprising results are common enough to require their consideration in any reasonable effort to characterize nature and manage natural resources. We classify surprises as dynamic-, pattern-, or intervention-based, and we speculate on the common processes that cause ecological systems to so often surprise us. A long-standing and still growing concern in the ecological literature is how best to make predictions of future population and community dynamics. Although most work on this subject involves statistical aspects of data analysis and modeling, the frequency and nature of ecological surprises imply that uncertainty cannot be easily tamed through improved analytical procedures, and that prudent management of both exploited and conserved communities will require precautionary and adaptive management approaches.

Functional identity and diversity of animals predict ecosystem functioning better than species-based indices

Drastic biodiversity declines have raised concerns about the deterioration of ecosystem functions and have motivated much recent research on the relationship between species diversity and ecosystem functioning. A functional trait framework has been proposed to improve the mechanistic understanding of this relationship, but this has rarely been tested for organisms other than plants. We analysed eight datasets, including five animal groups, to examine how well a trait-based approach, compared with a more traditional taxonomic approach, predicts seven ecosystem functions below- and above-ground. Trait-based indices consistently provided greater explanatory power than species richness or abundance. The frequency distributions of single or multiple traits in the community were the best predictors of ecosystem functioning. This implies that the ecosystem functions we investigated were underpinned by the combination of trait identities (i.e. single-trait indices) and trait complementarity (i.e. multi-trait indices) in the communities. Our study provides new insights into the general mechanisms that link biodiversity to ecosystem functioning in natural animal communities and suggests that the observed responses were due to the identity and dominance patterns of the trait composition rather than the number or abundance of species per se.

Agricultural intensification and biodiversity partitioning in European landscapes comparing plants, carabids, and birds

Effects of agricultural intensification (AI) on biodiversity are often assessed on the plot scale, although processes determining diversity also operate on larger spatial scales. Here, we analyzed the diversity of vascular plants, carabid beetles, and birds in agricultural landscapes in cereal crop fields at the field (n = 1350), farm (n = 270), and European-region (n = 9) scale. We partitioned diversity into its additive components alpha, beta, and gamma, and assessed the relative contribution of beta diversity to total species richness at each spatial scale. AI was determined using pesticide and fertilizer inputs, as well as tillage operations and categorized into low, medium, and high levels. As AI was not significantly related to landscape complexity, we could disentangle potential AI effects on local vs. landscape community homogenization. AI negatively affected the species richness of plants and birds, but not carabid beetles, at all spatial scales. Hence, local AI was closely correlated to beta diversity on larger scales up to the farm and region level, and thereby was an indicator of farm- and region-wide biodiversity losses. At the scale of farms (12.83-20.52%) and regions (68.34-80.18%), beta diversity accounted for the major part of the total species richness for all three taxa, indicating great dissimilarity in environmental conditions on larger spatial scales. For plants, relative importance of alpha diversity decreased with AI, while relative importance of beta diversity on the farm scale increased with AI for carabids and birds. Hence, and in contrast to our expectations, AI does not necessarily homogenize local communities, presumably due to the heterogeneity of farming practices. In conclusion, a more detailed understanding of AI effects on diversity patterns of various taxa and at multiple spatial scales would contribute to more efficient agri-environmental schemes in agroecosystems.

Perturbations to trophic interactions and the stability of complex food webs.

The pattern of predator–prey interactions is thought to be a key determinant of ecosystem processes and stability. Complex ecological networks are characterized by distributions of interaction strengths that are highly skewed, with many weak and few strong interactors present. Theory suggests that this pattern promotes stability as weak interactors dampen the destabilizing potential of strong interactors. Here, we present an experimental test of this hypothesis and provide empirical evidence that the loss of weak interactors can destabilize communities in nature. We ranked 10 marine consumer species by the strength of their trophic interactions. We removed the strongest and weakest of these interactors from experimental food webs containing >100 species. Extinction of strong interactors produced a dramatic trophic cascade and reduced the temporal stability of key ecosystem process rates, community diversity and resistance to changes in community composition. Loss of weak interactors also proved damaging for our experimental ecosystems, leading to reductions in the temporal and spatial stability of ecosystem process rates, community diversity, and resistance. These results highlight the importance of conserving species to maintain the stabilizing pattern of trophic interactions in nature, even if they are perceived to have weak effects in the system.

Weak interactions, omnivory and emergent food-web properties

Empirical studies have shown that, in real ecosystems, species–interaction strengths are generally skewed in their distribution towards weak interactions. Some theoretical work also suggests that weak interactions, especially in omnivorous links, are important for the local stability of a community at equilibrium. However, the majority of theoretical studies use uniform distributions of interaction strengths to generate artificial communities for study. We investigate the effects of the underlying interaction–strength distribution upon the return time, permanence and feasibility of simple Lotka–Volterra equilibrium communities. We show that a skew towards weak interactions promotes local and global stability only when omnivory is present. It is found that skewed interaction strengths are an emergent property of stable omnivorous communities, and that this skew towards weak interactions creates a dynamic constraint maintaining omnivory. Omnivory is more likely to occur when omnivorous interactions are skewed towards weak interactions. However, a skew towards weak interactions increases the return time to equilibrium, delays the recovery of ecosystems and hence decreases the stability of a community. When no skew is imposed, the set of stable omnivorous communities shows an emergent distribution of skewed interaction strengths. Our results apply to both local and global concepts of stability and are robust to the definition of a feasible community. These results are discussed in the light of empirical data and other theoretical studies, in conjunction with their broader implications for community assembly.

The relationship between agricultural intensification and biological control: experimental tests across Europe

Agricultural intensification can affect biodiversity and related ecosystem services such as biological control, but large-scale experimental evidence is missing. We examined aphid pest populations in cereal fields under experimentally reduced densities of (1) ground-dwelling predators (-G), (2) vegetation-dwelling predators and parasitoids (-V), (3) a combination of (1) and (2) (-G-V), compared with open-fields (control), in contrasting landscapes with low vs. high levels of agricultural intensification (AI), and in five European regions. Aphid populations were 28%, 97%, and 199% higher in -G, -V, and -G-V treatments, respectively, compared to the open fields, indicating synergistic effects of both natural-enemy groups. Enhanced parasitoid: host and predator: prey ratios were related to reduced aphid population density and population growth. The relative importance of parasitoids and vegetation-dwelling predators greatly differed among European regions, and agricultural intensification affected biological control and aphid density only in some regions. This shows a changing role of species group identity in diverse enemy communities and a need to consider region-specific landscape management.

On the dimensionality of ecological stability

Ecological stability is touted as a complex and multifaceted concept, including components such as variability, resistance, resilience, persistence and robustness. Even though a complete appreciation of the effects of perturbations on ecosystems requires the simultaneous measurement of these multiple components of stability, most ecological research has focused on one or a few of those components analysed in isolation. Here, we present a new view of ecological stability that recognises explicitly the non-independence of components of stability. This provides an approach for simplifying the concept of stability. We illustrate the concept and approach using results from a field experiment, and show that the effective dimensionality of ecological stability is considerably lower than if the various components of stability were unrelated. However, strong perturbations can modify, and even decouple, relationships among individual components of stability. Thus, perturbations not only increase the dimensionality of stability but they can also alter the relationships among components of stability in different ways. Studies that focus on single forms of stability in isolation therefore risk underestimating significantly the potential of perturbations to destabilise ecosystems. In contrast, application of the multidimensional stability framework that we propose gives a far richer understanding of how communities respond to perturbations.

Press perturbations and indirect effects in real food webs

The prediction of the effects of disturbances in natural systems is limited by the general lack of knowledge on the strength of species interactions, i.e., the effect of one species on the population growth rate of another, and by the uncertainty of the effects that may be manifested via indirect pathways within the food web. Here we explored the consequences of changes in species populations for the remaining species within nine exceptionally well-characterized empirical food webs, for which, unlike the vast majority of other published webs, feeding links have been fully quantified. Using the inverse of the Jacobian matrix, we found that perturbations to species with few connections have larger net effects (considering both direct and indirect pathways between two species) on the rest of the food web than do disturbances to species that are highly connected. For 40% of predator-prey links, predators had positive net effects on prey populations, due to the predominance of indirect interactions. Our results highlight the fundamental, but often counterintuitive, role of indirect effects for the maintenance of food web complexity and biodiversity.