Trait adaptation enhances species coexistence and reduces bistability in an intraguild predation module.

Disentangling how species coexist in an intraguild predation (IGP) module is a great step toward understanding biodiversity conservation in complex natural food webs. Trait variation enabling individual species to adjust to ambient conditions may facilitate coexistence. However, it is still unclear how coadaptation of all species within the IGP module, constrained by complex trophic interactions and trade-offs among species-specific traits, interactively affects species coexistence and population dynamics. We developed an adaptive IGP model allowing prey and predator species to mutually adjust their species-specific defensive and offensive strategies to each other. We investigated species persistence, the temporal variation of population dynamics, and the occurrence of bistability in IGP models without and with trait adaptation along a gradient of enrichment represented by carrying capacity of the basal prey for different widths and speeds of trait adaptation within each species. Results showed that trait adaptation within multiple species greatly enhanced the coexistence of all three species in the module. A larger width of trait adaptation facilitated species coexistence independent of the speed of trait adaptation at lower enrichment levels, while a sufficiently large and fast trait adaptation promoted species coexistence at higher enrichment levels. Within the oscillating regime, increasing the speed of trait adaptation reduced the temporal variability of biomasses of all species. Finally, species coadaptation strongly reduced the presence of bistability and promoted the attractor with all three species coexisting. These findings resolve the contradiction between the widespread occurrence of IGP in nature and the theoretical predictions that IGP should only occur under restricted conditions and lead to unstable population dynamics, which broadens the mechanisms presumably underlying the maintenance of IGP modules in nature. Generally, this study demonstrates a decisive role of mutual adaptation among complex trophic interactions, for enhancing interspecific diversity and stabilizing food web dynamics, arising, for example, from intraspecific diversity.

A sterol-mediated gleaner-opportunist trade-off underlies the evolution of grazer resistance to cyanobacteria.

The human-caused proliferation of cyanobacteria severely impacts consumers in freshwater ecosystems. Toxicity is often singled out as the sole trait to which consumers can adapt, even though cyanobacteria are not necessarily toxic and the lack of nutritionally critical sterols in cyanobacteria is known to impair consumers. We studied the relative significance of toxicity and dietary sterol deficiency in driving the evolution of grazer resistance to cyanobacteria in a large lake with a well-documented history of eutrophication and oligotrophication. Resurrecting decades-old Daphnia genotypes from the sediment allowed us to show that the evolution and subsequent loss of grazer resistance to cyanobacteria involved an adaptation to changes in both toxicity and dietary sterol availability. The adaptation of Daphnia to changes in cyanobacteria abundance revealed a sterol-mediated gleaner-opportunist trade-off. Genotypes from peak-eutrophic periods showed a higher affinity for dietary sterols at the cost of a lower maximum growth rate, whereas genotypes from more oligotrophic periods showed a lower affinity for dietary sterols in favour of a higher maximum growth rate. Our data corroborate the significance of sterols as limiting nutrients in aquatic food webs and highlight the applicability of the gleaner-opportunist trade-off for reconstructing eco-evolutionary processes.

The joint effects of salt and 6PPD contamination on a freshwater herbivore.

Using sodium chloride (NaCl) for de-icing roads is known to have severe consequences on freshwater organisms when washed into water bodies. N-(1,3-dimethylbutyl)-N'-phenyl-p-phenylenediamine, also known as 6PPD, is an antiozonant mainly found in automobile tire rubber to prevent ozone mediated cracking or wear-out. Especially the ozonated derivate, 6PPD-quinone, which is washed into streams after storm events, has been found to be toxic for coho salmon. Studies on other freshwater organisms could not confirm those findings, pointing towards distinct species-specific differences. Storm events result in greater run-offs from all water-soluble contaminants into freshwater bodies, potentially enhancing the concentrations of both chloride and 6PPD during winter. Here we show that these two contaminants have synergistic negative effects on the population growth of the rotifer Brachionus calyciflorus, a common freshwater herbivore. Hence, while only high concentrations of 6PPD and even higher concentrations of 6PPD-quinone, beyond environmentally relevant concentrations, had lethal effects on rotifers, the addition of NaCl enhanced the sensitivity of the rotifers towards the application of 6PPD so that their negative effects were more pronounced at lower concentrations. Similarly, 6PPD increased the lethal effect of NaCl. Our results support the species-specific toxicity of 6PPD and demonstrate a synergistic effect of the antiozonant on the toxicity of other environmentally relevant stressors, such as road salt contamination.

Self-organised pattern formation increases local diversity in metacommunities.

Self-organised formation of spatial patterns is known from a variety of different ecosystems, yet little is known about how these patterns affect the diversity of communities. Here, we use a food chain model in which autotroph diversity is described by a continuous distribution of a trait that affects both growth and defence against heterotrophs. On isolated patches, diversity is always lost over time due to stabilising selection, and the local communities settle on one of two alternative stable community states that are characterised by a dominance of either defended or undefended species. In a metacommunity context, dispersal can destabilise these states and complex spatio-temporal patterns in the species' abundances emerge. The resulting biomass-trait feedback increases local diversity by an order of magnitude compared to scenarios without self-organised pattern formation, thereby maintaining the ability of communities to adapt to potential future changes in biotic or abiotic environmental conditions.

Intraspecific trait variation alters the outcome of competition in freshwater ciliates.

Trait variation among heterospecific and conspecific organisms may substantially affect community and food web dynamics. While the relevance of competition and feeding traits have been widely studied for different consumer species, studies on intraspecific differences are more scarce, partly owing to difficulties in distinguishing different clones of the same species. Here, we investigate how intraspecific trait variation affects the competition between the freshwater ciliates Euplotes octocarinatus and Coleps hirtus in a nitrogen-limited chemostat system. The ciliates competed for the microalgae Cryptomonas sp. (Cry) and Navicula pelliculosa (Nav), and the bacteria present in the cultures over a period of 33 days. We used monoclonal Euplotes and three different Coleps clones (Col 1, Col 2, and Col 3) in the experiment that could be distinguished by a newly developed rDNA-based molecular assay based on the internal transcribed spacer (ITS) regions. While Euplotes feeds on Cry and on bacteria, the Coleps clones cannot survive on bacteria alone but feed on both Cry and Nav with clone-specific rates. Experimental treatments comprised two-species mixtures of Euplotes and one or all of the three different Coleps clones, respectively. We found intraspecific variation in the traits "selectivity" and "maximum ingestion rate" for the different algae to significantly affect the competitive outcome between the two ciliate species. As Nav quickly escaped top-down control and likely reached a state of low food quality, ciliate competition was strongly determined by the preference of different Coleps clones for Cry as opposed to feeding on Nav. In addition, the ability of Euplotes to use bacteria as an alternative food source strengthened its persistence once Cry was depleted. Hence, trait variation at both trophic levels codetermined the population dynamics and the outcome of species competition.

Dietary lipid quality mediates salt tolerance of a freshwater keystone herbivore.

Salinization of freshwater ecosystems is a growing hazard for organisms and ecosystem functioning worldwide. In northern latitudes, road salt that is being transported into water bodies can cause year-round increases in lake salinity levels. Exploring the environmental factors driving the susceptibility of freshwater zooplankton to road salt is crucial for assessing the impact of salinization on food web processes. We studied the role of essential lipids, i.e., sterols and long-chain polyunsaturated fatty acids (PUFAs), in mediating salt tolerance of the freshwater keystone herbivore Daphnia. Sterols and PUFAs are involved in regulating ion permeability of biological membranes and thus we hypothesized that the susceptibility to salt is affected by the dietary sterol and PUFA supply. Life history experiments revealed opposing effects of sterol and PUFA supplementation on salt tolerance, i.e., tolerance increased upon sterol supplementation but decreased upon PUFA supplementation, which is consistent with their proposed impact on membrane permeability. Our results suggest that the susceptibility of freshwater zooplankton to salinization strongly depends on the dietary lipid supply and thus the phytoplankton community composition. Hence, trophic state related differences in the phytoplankton community composition need to be considered when assessing the consequences of salinization for freshwater ecosystem functioning.

The effects of functional diversity on biomass production, variability, and resilience of ecosystem functions in a tritrophic system.

Diverse communities can adjust their trait composition to altered environmental conditions, which may strongly influence their dynamics. Previous studies of trait-based models mainly considered only one or two trophic levels, whereas most natural system are at least tritrophic. Therefore, we investigated how the addition of trait variation to each trophic level influences population and community dynamics in a tritrophic model. Examining the phase relationships between species of adjacent trophic levels informs about the strength of top-down or bottom-up control in non-steady-state situations. Phase relationships within a trophic level highlight compensatory dynamical patterns between functionally different species, which are responsible for dampening the community temporal variability. Furthermore, even without trait variation, our tritrophic model always exhibits regions with two alternative states with either weak or strong nutrient exploitation, and correspondingly low or high biomass production at the top level. However, adding trait variation increased the basin of attraction of the high-production state, and decreased the likelihood of a critical transition from the high- to the low-production state with no apparent early warning signals. Hence, our study shows that trait variation enhances resource use efficiency, production, stability, and resilience of entire food webs.

Modelling inducible defences in predator-prey interactions: assumptions and dynamical consequences of three distinct approaches.

Inducible defences against predation are widespread in the natural world, allowing prey to economise on the costs of defence when predation risk varies over time or is spatially structured. Through interspecific interactions, inducible defences have major impacts on ecological dynamics, particularly predator-prey stability and phase lag. Researchers have developed multiple distinct approaches, each reflecting assumptions appropriate for particular ecological communities. Yet, the impact of inducible defences on ecological dynamics can be highly sensitive to the modelling approach used, making the choice of model a critical decision that affects interpretation of the dynamical consequences of inducible defences. Here, we review three existing approaches to modelling inducible defences: Switching Function, Fitness Gradient and Optimal Trait. We assess when and how the dynamical outcomes of these approaches differ from each other, from classic predator-prey dynamics and from commonly observed eco-evolutionary dynamics with evolving, but non-inducible, prey defences. We point out that the Switching Function models tend to stabilise population dynamics, and the Fitness Gradient models should be carefully used, as the difference with evolutionary dynamics is important. We discuss advantages of each approach for applications to ecological systems with particular features, with the goal of providing guidelines for future researchers to build on.

Trait adaptation promotes species coexistence in diverse predator and prey communities.

Species can adjust their traits in response to selection which may strongly influence species coexistence. Nevertheless, current theory mainly assumes distinct and time-invariant trait values. We examined the combined effects of the range and the speed of trait adaptation on species coexistence using an innovative multispecies predator-prey model. It allows for temporal trait changes of all predator and prey species and thus simultaneous coadaptation within and among trophic levels. We show that very small or slow trait adaptation did not facilitate coexistence because the stabilizing niche differences were not sufficient to offset the fitness differences. In contrast, sufficiently large and fast trait adaptation jointly promoted stable or neutrally stable species coexistence. Continuous trait adjustments in response to selection enabled a temporally variable convergence and divergence of species traits; that is, species became temporally more similar (neutral theory) or dissimilar (niche theory) depending on the selection pressure, resulting over time in a balance between niche differences stabilizing coexistence and fitness differences promoting competitive exclusion. Furthermore, coadaptation allowed prey and predator species to cluster into different functional groups. This equalized the fitness of similar species while maintaining sufficient niche differences among functionally different species delaying or preventing competitive exclusion. In contrast to previous studies, the emergent feedback between biomass and trait dynamics enabled supersaturated coexistence for a broad range of potential trait adaptation and parameters. We conclude that accounting for trait adaptation may explain stable and supersaturated species coexistence for a broad range of environmental conditions in natural systems when the absence of such adaptive changes would preclude it. Small trait changes, coincident with those that may occur within many natural populations, greatly enlarged the number of coexisting species.

Diversity, functional similarity, and top-down control drive synchronization and the reliability of ecosystem function.

The concept that diversity promotes reliability of ecosystem function depends on the pattern that community-level biomass shows lower temporal variability than species-level biomasses. However, this pattern is not universal, as it relies on compensatory or independent species dynamics. When in contrast within-trophic level synchronization occurs, variability of community biomass will approach population-level variability. Current knowledge fails to integrate how species richness, functional distance between species, and the relative importance of predation and competition combine to drive synchronization at different trophic levels. Here we clarify these mechanisms. Intense competition promotes compensatory dynamics in prey, but predators may at the same time increasingly synchronize, under increasing species richness and functional similarity. In contrast, predators and prey both show perfect synchronization under strong top-down control, which is promoted by a combination of low functional distance and high net growth potential of predators. Under such conditions, community-level biomass variability peaks, with major negative consequences for reliability of ecosystem function.