Lindsay A. Turnbull

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.

JANZEN‐CONNELL EFFECTS ARE WIDESPREAD AND STRONG ENOUGH TO MAINTAIN DIVERSITY IN GRASSLANDS

Crop rotation schemes are believed to work by preventing specialist soil-borne pests from depressing the future yields of similar crops. In ecology, such negative plant-soil feedbacks may be viewed as a type of Janzen-Connell effect, which promotes species coexistence and diversity by preventing the same species from repeatedly occupying a particular site. In a controlled greenhouse experiment with 24 plant species and using soils from established field monocultures, we reveal community-wide soil-based Janzen-Connell effects between the three major functional groups of plants in temperate European grasslands. The effects are much stronger and more prevalent if plants are grown in interspecific competition. Using several soil treatments (gamma irradiation, activated carbon, fungicide, fertilizer) we show that the mechanism of the negative feedback is the buildup of soil pathogens which reduce the competitive ability of nearly all species when grown on soils they have formerly occupied. We further show that the magnitude of the change in competitive outcome is sufficient to stabilize observed fitness differences between functional groups in reasonably large communities. The generality and strength of this negative feedback suggests that Janzen-Connell effects have been underestimated as drivers of plant diversity in temperate ecosystems.

Land‐use intensity and the effects of organic farming on biodiversity: a hierarchical meta‐analysis

Summary The benefits of organic farming to biodiversity in agricultural landscapes continue to be hotly debated, emphasizing the importance of precisely quantifying the effect of organic vs. conventional farming. We conducted an updated hierarchical meta‐analysis of studies that compared biodiversity under organic and conventional farming methods, measured as species richness. We calculated effect sizes for 184 observations garnered from 94 studies, and for each study, we obtained three standardized measures reflecting land‐use intensity. We investigated the stability of effect sizes through time, publication bias due to the ‘file drawer’ problem, and consider whether the current literature is representative of global organic farming patterns. On average, organic farming increased species richness by about 30%. This result has been robust over the last 30 years of published studies and shows no sign of diminishing. Organic farming had a greater effect on biodiversity as the percentage of the landscape consisting of arable fields increased, that is, it is higher in intensively farmed regions. The average effect size and the response to agricultural intensification depend on taxonomic group, functional group and crop type. There is some evidence for publication bias in the literature; however, our results are robust to its impact. Current studies are heavily biased towards northern and western Europe and North America, while other regions with large areas of organic farming remain poorly investigated. Synthesis and applications. Our analysis affirms that organic farming has large positive effects on biodiversity compared with conventional farming, but that the effect size varies with the organism group and crop studied, and is greater in landscapes with higher land‐use intensity. Decisions about where to site organic farms to maximize biodiversity will, however, depend on the costs as well as the potential benefits. Current studies have been heavily biased towards agricultural systems in the developed world. We recommend that future studies pay greater attention to other regions, in particular, areas with tropical, subtropical and Mediterranean climates, in which very few studies have been conducted.

Natural Enemies Drive Geographic Variation in Plant Defenses

Plant Anti-Insect Armaments Because individual plants are unable to relocate, they are subject to extreme selection by the insects feeding upon them. One means by which plants suppress herbivory is to produce toxic compounds to deter feeding (see the Perspective by Hare). Agrawal et al. (p. 113) compared pesticide–treated or untreated evening primroses. Over 5 years of pesticide treatment, the production of defensive chemicals in the fruit reduced and flowering times shifted, and the primroses competitive ability against dandelions improved. Züst et al. (p. 116) examined large-scale geographic patterns in a polymorphic chemical defense locus in the model plant Arabidopsis thaliana and found that it is matched by changes in the relative abundance of two specialist aphids. Thus, herbivory has strong and immediate effects on the local genotypic composition of plants and traits associated with herbivore resistance. A field study demonstrates that specialist aphid feeders cause changes in the defenses mounted by plants. Plants defend themselves against attack by natural enemies, and these defenses vary widely across populations. However, whether communities of natural enemies are a sufficiently potent force to maintain polymorphisms in defensive traits is largely unknown. Here, we exploit the genetic resources of Arabidopsis thaliana, coupled with 39 years of field data on aphid abundance, to (i) demonstrate that geographic patterns in a polymorphic defense locus (GS-ELONG) are strongly correlated with changes in the relative abundance of two specialist aphids; and (ii) demonstrate differential selection by the two aphids on GS-ELONG, using a multigeneration selection experiment. We thereby show a causal link between variation in abundance of the two specialist aphids and the geographic pattern at GS-ELONG, which highlights the potency of natural enemies as selective forces.

Using knockout mutants to reveal the growth costs of defensive traits

We used a selection of Arabidopsis thaliana mutants with knockouts in defence genes to demonstrate growth costs of trichome development and glucosinolate production. Four of the seven defence mutants had significantly higher size-standardized growth rates (SGRs) than the wild-type in early life, although this benefit declined as plants grew larger. SGR is known to be a good predictor of success under high-density conditions, and we confirmed that mutants with higher growth rates had a large advantage when grown in competition. Despite the lack of differences in flowering-time genes, the mutants differed in flowering time, a trait that strongly correlated with early growth rate. Aphid herbivory decreased plant growth rate and increased flowering time, and aphid population growth rate was closely coupled to the growth rate of the host plant. Small differences in early SGR thus had cascading effects on both flowering time and herbivore populations.

Coexistence, niches and biodiversity effects on ecosystem functioning.

General principles from coexistence theory are often invoked to explain how and why mixtures of species outperform monocultures. However, the complementarity and selection effects commonly measured in biodiversity experiments do not precisely quantify the niche and relative fitness differences that govern species coexistence. Given this lack of direct correspondence, how can we know whether species-rich mixtures are stable and that the benefits of diversity will therefore persist? We develop a resource-based included-niche model in which plant species have asymmetric access to a nested set of belowground resource pools. We use the model to show that positive complementarity effects arise from stabilising niche differences, but do not necessarily lead to stable coexistence and hence can be transient. In addition, these transient complementarity effects occur in the model when there is no complementary resource use among species. Including a trade-off between uptake rates and the size of the resource pool stabilised interactions and led to persistent complementarity coupled with weak or negative selection effects, consistent with results from the longest-running field biodiversity experiments. We suggest that future progress requires a greater mechanistic understanding of the links between ecosystem functions and their underlying biological processes.

Different but equal: the implausible assumption at the heart of neutral theory

1.The core assumption of neutral theory is that all individuals in a community have equal fitness regardless of species, and regardless of the species composition of the community. But, real communities consist of species exhibiting large trait differences; hence these differences must be subject to perfect fitness-equalizing trade-offs for neutrality to hold. 2.Here we explain that perfect equalizing trade-offs are extremely unlikely to occur in reality, because equality of fitness among species is destroyed by: (i) any deviation in the functional form of the trade-off away from the one special form that gives equal fitness; (ii) spatial or temporal variation in performance; (iii) random species differences in performance. 3.In the absence of the density-dependent processes stressed by traditional niche-based community ecology, communities featuring small amounts of (i) or (ii) rapidly lose trait variation, becoming dominated by species with similar traits, and exhibit substantially lower species richness compared to the neutral case. Communities featuring random interspecific variation in traits (iii) lose all but a few fortuitous species. 4.Thus neutrality should be viewed, a priori, as a highly improbable explanation for the long-term co-occurrence of measurably different species within ecological communities. In contrast, coexistence via niche structure and density dependence, is robust to species differences in baseline fitness, and so remains plausible. 5.We conclude that: (i) co-occurring species will typically exhibit substantial differences in baseline fitness even when (imperfect) equalizing trade-offs have been taken into account; (ii) therefore, communities must be strongly niche structured, otherwise they would lose both trait variation and species richness; (iii) nonetheless, even in strongly niche-structured communities, it is possible that the abundance of species with similar traits are at least partially free to drift.

Biology, chance, or history? The predictable reassembly of temperate grassland communities

Many studies have examined invasion resistance in plant communities, but few have explored the mechanisms of invasion and how subsequent community reassembly affects community functioning. Using natural dispersal and deliberate seed addition into grassland communities with different compositional and richness histories, we show that invaders establish in a nonrandom manner due to negative effects of resident functional groups on invading species from the same functional group. Invaders hence complement communities with originally low richness levels. Consequently, communities converge toward similar levels of species richness, high functional richness, and evenness, but not always maximum productivity. Invasion processes are faster but qualitatively similar when the effect of chance, in the form of dispersal stochasticity, is reduced by seed addition. Thus, dispersal limitation may influence community assembly, but it does not override functionally predictable assembly mechanisms. Some of the most productive communities prior to invasion are unstable in the face of invasion, leading to decreased productivity following invasion. We suggest that invasion into such communities occurs possibly because a pathogen-free niche is available rather than a resource niche. Thus, pathogens in addition to resource niches may be important biological drivers of community assembly.

Linking the influence and dependence of people on biodiversity across scales

Biodiversity enhances many of natures benefits to people, including the regulation of climate and the production of wood in forests, livestock forage in grasslands and fish in aquatic ecosystems. Yet people are now driving the sixth mass extinction event in Earths history. Human dependence and influence on biodiversity have mainly been studied separately and at contrasting scales of space and time, but new multiscale knowledge is beginning to link these relationships. Biodiversity loss substantially diminishes several ecosystem services by altering ecosystem functioning and stability, especially at the large temporal and spatial scales that are most relevant for policy and conservation.

The costs and benefits of fast living

Growth rates play a fundamental role in many areas of biology (Q. Rev. Biol., 67, 1992, 283; Life History Invariants. Some Explorations of Symmetry in Evolutionary Biology, 1993; Philos. Trans. R. Soc. Lond. B Biol. Sci., 351, 1996, 1341; Plant Strategies, Vegetation Processes, and Ecosystem Properties, 2002; Trends Ecol. Evol., 18, 2003, 471; Q. Rev. Biol., 78, 2003, 23; J. Ecol., 95, 2007, 926.) but the cost and benefits of different growth rates are notoriously difficult to quantify (Q. Rev. Biol., 72, 1997, 149; Funct. Ecol., 17, 2003, 328). This is because (1) growth rate typically declines with size and yet the most widely used growth measure - relative growth rate or RGR (conventionally measured as the log of the ratio of successive sizes divided by the time interval) - is not size-corrected and so confounds growth and size, (2) organisms have access to different amounts of resource and (3) it is essential to allow for the long-term benefits of larger size. Here we experimentally demonstrate delayed costs and benefits of rapid growth in seven plant species using a novel method to calculate size-corrected RGR. In control treatments, fast-growing plants benefited from increased reproduction the following year; however, fast-growing plants subjected to an experimental stress treatment (defoliation) showed strongly reduced survival and reproduction the following year. Importantly, when growth was estimated using the classical RGR measure, no costs or benefits were found. These results support the idea that life-history trade-offs have a dominant role in life-history and ecological theory and that the widespread failure to detect them is partly due to methodological shortcomings.