When can higher-order interactions produce stable coexistence?

Most ecological models are based on the assumption that species interact in pairs. Diverse communities, however, can have higher-order interactions, in which two or more species jointly impact the growth of a third species. A pitfall of the common pairwise approach is that it misses the higher-order interactions potentially responsible for maintaining natural diversity. Here, we explore the stability properties of systems where higher-order interactions guarantee that a specified set of abundances is a feasible equilibrium of the dynamics. Even these higher-order interactions which lead to equilibria do not necessarily produce stable coexistence. Instead, these systems are more likely to be stable when the pairwise interactions are weak or facilitative. Correlations between the pairwise and higher-order interactions, however, do permit robust coexistence even in diverse systems. Our work not only reveals the challenges in generating stable coexistence through higher-order interactions but also uncovers interaction patterns that can enable diversity.

Stability of consumer-resource interactions in periodic environments.

Periodic fluctuations in abiotic conditions are ubiquitous across a range of temporal scales and regulate the structure and function of ecosystems through dynamic biotic responses that are adapted to these external forces. Research has suggested that certain environmental signatures may play a crucial role in the maintenance of biodiversity and the stability of food webs, while others argue that coupled oscillators ought to promote chaos. As such, numerous uncertainties remain regarding the intersection of temporal environmental patterns and biological responses, and we lack a general understanding of the implications for food web stability. Alarmingly, global change is altering the nature of both environmental rhythms and biological rates. Here, we develop a general theory for how continuous periodic variation in productivity, across temporal scales, influences the stability of consumer-resource interactions: a fundamental building block of food webs. Our results suggest that consumer-resource dynamics under environmental forcing are highly complex and depend on asymmetries in both the speed of forcing relative to underlying dynamics and in local stability properties. These asymmetries allow for environmentally driven stabilization under fast forcing, relative to underlying dynamics, as well as extremely complex and unstable dynamics at slower periodicities. Our results also suggest that changes in naturally occurring periodicities from climate change may lead to precipitous shifts in dynamics and stability.

Life-history speed, population disappearances and noise-induced ratchet effects.

Nature is replete with variation in the body sizes, reproductive output and generation times of species that produce life-history responses known to vary from small and fast to large and slow. Although researchers recognize that life-history speed likely dictates fundamental processes in consumer-resource interactions like productivity and stability, theoretical work remains incomplete in this critical area. Here, we examine the role of life-history speed on consumer-resource interactions by using a well-used mathematical approach that manipulates the speed of the consumer's growth rate in a consumer-resource interaction. Importantly, this approach holds the isocline geometry intact, allowing us to assess the impacts of altered life-history speed on stability (coefficient of variation, CV) without changing the underlying qualitative dynamics. Although slowing life history can be initially stabilizing, we find that in stochastic settings slowing ultimately drives highly destabilizing population disappearances, especially under reddened noise. Our results suggest that human-driven reddening of noise may decrease species stability because the autocorrelation of red noise enlarges the period and magnitude of perturbations, overwhelming a species' natural compensatory responses via a ratchet-like effect. This ratchet-like effect then pushes species' population dynamics far away from equilibria, which can lead to precipitous local extinction.

Managing aquatic habitat structure for resilient trophic interactions.

Structural habitat (the three-dimensional arrangement of physical matter, abiotic and biotic, at a location) is a foundational element for the resilience and maintenance of biodiversity, yet anthropogenic development is driving the global simplification of aquatic environments. Resource managers regularly seek to conserve aquatic food webs by increasing structural habitat complexity with expected benefits to fisheries; however, the global effectiveness of such actions is unclear. Our synthesis and theoretical analyses found that the response of a consumer-resource interaction (predatory sportfish and forage fish prey) to the addition of prey refuge habitat differed among systems with low and high rates of biomass transfer from resource to consumer (i.e., biomass potential); stabilization was not the rule. Greater prey refuge habitat availability tended to stabilize systems characterized by high biomass potential while simultaneously increasing consumer densities. In contrast, increasing prey refuge habitat availability in systems characterized by low biomass potential tended to mute energy transfer and moved consumer densities toward local extinction. Importantly, biomass potential and prey refuge can have antagonistic effects on stability and relative consumer densities, and it is therefore important to consider the local conditions of a system when using habitat manipulation as a management measure. Further development of our context-dependent perspective to whole food webs, and across different environments, may help to guide structural habitat management to better restore and protect aquatic ecosystems.

Nutrient identity modifies the destabilising effects of eutrophication in grasslands.

Nutrient enrichment can simultaneously increase and destabilise plant biomass production, with co-limitation by multiple nutrients potentially intensifying these effects. Here, we test how factorial additions of nitrogen (N), phosphorus (P) and potassium with essential nutrients (K+) affect the stability (mean/standard deviation) of aboveground biomass in 34 grasslands over 7 years. Destabilisation with fertilisation was prevalent but was driven by single nutrients, not synergistic nutrient interactions. On average, N-based treatments increased mean biomass production by 21-51% but increased its standard deviation by 40-68% and so consistently reduced stability. Adding P increased interannual variability and reduced stability without altering mean biomass, while K+ had no general effects. Declines in stability were largest in the most nutrient-limited grasslands, or where nutrients reduced species richness or intensified species synchrony. We show that nutrients can differentially impact the stability of biomass production, with N and P in particular disproportionately increasing its interannual variability.

Riparian buffers maintain aquatic trophic structure in agricultural landscapes.

Local and regional habitat conditions associated with agricultural activity can fundamentally alter aquatic ecosystems. Increased nutrient inputs, channelization and reduced riparian habitat both upstream and locally contribute to the degradation of stream ecosystems and their function. Here, we examine stream food webs in watersheds that feed into Lake Erie to determine the effects of agricultural land cover on major food web energy pathways and trophic structure. Given that higher agricultural intensity can increase nutrient runoff and reduce the riparian zone and litter in-fall into streams, we predicted that generalist fish would derive less energy from the terrestrial pathway and become more omnivorous. Consistent with these predictions, we show that both mean terrestrial energy use and trophic position of the resident top consumer, creek chub (Semotilus atromaculatus), decrease with local agricultural intensity but not with watershed-level agriculture intensity. These findings suggest that local riparian buffers can maintain trophic structure even in the face of high whole-watershed agricultural intensity.

Cascading effects of predators on algal size structure.

The presence of edible and inedible prey species in a food web can influence the strength that nutrients (bottom-up) or herbivores (top-down) have on primary production. In boreal peatlands, wetter more nutrient-rich conditions associated with ongoing climate change are expanding consumer access to aquatic habitat and promoting sources of primary production (i.e., algae) that are susceptible to trophic regulation. Here, we used an in situ mesocosm experiment to evaluate the consequences of enhanced nutrient availability and food-web manipulation (herbivore and predator exclusion) on algal assemblage structure in an Alaskan fen. Owing to the potential for herbivores to selectively consume edible algae (small cells) in favor of more resistant forms, we predicted that the proportion of less-edible algae (large cells) would determine the strength of top-down or bottom-up effects. Consistent with these expectations, we observed an increase in algal-cell size in the presence of herbivores (2-tiered food web) that was absent in the presence of a trophic cascade (3-tiered food web), suggesting that predators indirectly prevented morphological changes in the algal assemblage by limiting herbivory. Increases in algal-cell size with herbivory were driven by a greater proportion of filamentous green algae and nitrogen-fixing cyanobacteria, whose size and morphological characteristics mechanically minimize consumption. While consumer-driven shifts in algal assemblage structure were significant, they did not prevent top-down regulation of biofilm development by herbivores. Our findings show that increasing wet periods in northern peatlands will provide new avenues for trophic regulation of algal production, including directly through consumption and indirectly via a trophic cascade.

Letter: Trophic interactions regulate peatland carbon cycling.

Peatlands are the most efficient natural ecosystems for long-term storage of atmospheric carbon. Our understanding of peatland carbon cycling is based entirely on bottom-up controls regulated by low nutrient availability. Recent studies have shown that top-down controls through predator-prey dynamics can influence ecosystem function, yet this has not been evaluated in peatlands to date. Here, we used a combination of nutrient enrichment and trophic-level manipulation to test the hypothesis that interactions between nutrient availability (bottom-up) and predation (top-down) influence peatland carbon fluxes. Elevated nutrients stimulated bacterial biomass and organic matter decomposition. In the absence of top-down regulation, carbon dioxide (CO2 ) respiration driven by greater decomposition was offset by elevated algal productivity. Herbivores accelerated CO2 emissions by removing algal biomass, while predators indirectly reduced CO2 emissions by muting herbivory in a trophic cascade. This study demonstrates that trophic interactions can mitigate CO2 emissions associated with elevated nutrient levels in northern peatlands.

Landscape modification and nutrient-driven instability at a distance.

Almost 50 years ago, Michael Rosenzweig pointed out that nutrient addition can destabilise food webs, leading to loss of species and reduced ecosystem function through the paradox of enrichment. Around the same time, David Tilman demonstrated that increased nutrient loading would also be expected to cause competitive exclusion leading to deleterious changes in food web diversity. While both concepts have greatly illuminated general diversity-stability theory, we currently lack a coherent framework to predict how nutrients influence food web stability across a landscape. This is a vitally important gap in our understanding, given mounting evidence of serious ecological disruption arising from anthropogenic displacement of resources and organisms. Here, we combine contemporary theory on food webs and meta-ecosystems to show that nutrient additions are indeed expected to drive loss in stability and function in human-impacted regions. Our models suggest that destabilisation is more likely to be caused by the complete loss of an equilibrium due to edible plant species being competitively excluded. In highly modified landscapes, spatial nutrient transport theory suggests that such instabilities can be amplified over vast distances from the sites of nutrient addition. Consistent with this theoretical synthesis, the empirical frequency of these distant propagating ecosystem imbalances appears to be growing. This synthesis of theory and empirical data suggests that human modification of the Earth is strongly connecting distantly separated ecosystems, causing rapid, expansive and costly nutrient-driven instabilities over vast areas of the planet. Similar to existing food web theory, the corollary to this spatial nutrient theory is that slowing down spatial nutrient pathways can be a potent means of stabilising degraded ecosystems.

Winter in water: differential responses and the maintenance of biodiversity.

The ecological consequences of winter in freshwater systems are an understudied but rapidly emerging research area. Here, we argue that winter periods of reduced temperature and light (and potentially oxygen and resources) could play an underappreciated role in mediating the coexistence of species. This may be especially true for temperate and subarctic lakes, where seasonal changes in the thermal environment might fundamentally structure species interactions. With climate change already shortening ice-covered periods on temperate and polar lakes, consideration of how winter conditions shape biotic interactions is urgently needed. Using freshwater fishes in northern temperate lakes as a case study, we demonstrate how physiological trait differences (e.g. thermal preference, light sensitivity) drive differential behavioural responses to winter among competing species. Specifically, some species have a higher capacity for winter activity than others. Existing and new theory is presented to argue that such differential responses to winter can promote species coexistence. Importantly, if winter is a driver of niche differences that weaken competition between, relative to within species, then shrinking winter periods could threaten coexistence by tipping the scales in favour of certain sets of species over others.

Supply and demand drive a critical transition to dysfunctional fisheries.

There is growing awareness of the need for fishery management policies that are robust to changing environmental, social, and economic pressures. Here we use conventional bioeconomic theory to demonstrate that inherent biological constraints combined with nonlinear supply-demand relationships can generate threshold effects due to harvesting. As a result, increases in overall demand due to human population growth or improvement in real income would be expected to induce critical transitions from high-yield/low-price fisheries to low-yield/high-price fisheries, generating severe strains on social and economic systems as well as compromising resource conservation goals. As a proof of concept, we show that key predictions of the critical transition hypothesis are borne out in oceanic fisheries (cod and pollock) that have experienced substantial increase in fishing pressure over the past 60 y. A hump-shaped relationship between price and historical harvest returns, well demonstrated in these empirical examples, is particularly diagnostic of fishery degradation. Fortunately, the same heuristic can also be used to identify reliable targets for fishery restoration yielding optimal bioeconomic returns while safely conserving resource abundance.

Consumer trophic positions respond variably to seasonally fluctuating environments.

The effects of environmental seasonality on food web structure have been notoriously understudied in empirical ecology. Here, we focus on seasonal changes in one key attribute of a food web, consumer trophic position. We ask whether fishes inhabiting tropical river-floodplain ecosystems behave as seasonal omnivores, by shifting their trophic positions in relation to the annual flood pulse, or whether they feed at the same trophic position all year, as much empirical work implicitly assumes. Using dietary data from the Tonle Sap Lake, Cambodia, and a literature review, we find evidence that some fishes, especially small piscivores, increased consumption of invertebrates and/or plant material during the wet season, as predicted. However, nitrogen stable isotope (δ15 N) data for 26 Tonle Sap fishes, spanning a broader range of functional groups, uncovered high variation in seasonal trophic position responses among species (0 to ±0.52 trophic positions). Based on these findings, species respond to the flood pulse differently. Diverse behavioral responses to seasonality, underpinned by spatiotemporal variation at multiple scales, could be central for rerouting matter and energy flow in these dynamic ecosystems. Seasonally flexible foraging behaviors warrant further study given their potential influence on food web dynamics in a range of fluctuating environments.

Homogenization of freshwater lakes: Recent compositional shifts in fish communities are explained by gamefish movement and not climate change.

Globally, lake fish communities are being subjected to a range of scale-dependent anthropogenic pressures, from climate change to eutrophication, and from overexploitation to species introductions. As a consequence, the composition of these communities is being reshuffled, in most cases leading to a surge in taxonomic similarity at the regional scale termed homogenization. The drivers of homogenization remain unclear, which may be a reflection of interactions between various environmental changes. In this study, we investigate two potential drivers of the recent changes in the composition of freshwater fish communities: recreational fishing and climate change. Our results, derived from 524 lakes of Ontario, Canada sampled in two periods (1965-1982 and 2008-2012), demonstrate that the main contributors to homogenization are the dispersal of gamefish species, most of which are large predators. Alternative explanations relating to lake habitat (e.g., area, phosphorus) or variations in climate have limited explanatory power. Our analysis suggests that human-assisted migration is the primary driver of the observed compositional shifts, homogenizing freshwater fish community among Ontario lakes and generating food webs dominated by gamefish species.

Potential oscillators and keystone modules in food webs.

Food web theory suggests that the placement of a weak interaction is critical such that under some conditions even one well-placed weak interaction can stabilise multiple strong interactions. This theory suggests that complex stable webs may be built from pivotal weak interactions such that the removal of even one to a few keystone interactions can have significant cascading impacts on whole system diversity and structure. However, the connection between weak interactions, derived from the theory of modular food web components, and keystone species, derived from empirical results, is not yet well understood. Here, we develop numerical techniques to detect potential oscillators hidden in complex food webs, and show that, both in random and real food webs, keystone consumer-resource interactions often operate to stabilise them. Alarmingly, this result suggests that nature frequently may be dangerously close to precipitous change with even the loss of one or a few weakly interacting species.

On the prevalence and dynamics of inverted trophic pyramids and otherwise top-heavy communities.

Classically, biomass partitioning across trophic levels was thought to add up to a pyramidal distribution. Numerous exceptions have, however, been noted including complete pyramidal inversions. Elevated levels of biomass top-heaviness (i.e. high consumer/resource biomass ratios) have been reported from Arctic tundra communities to Brazilian phytotelmata, and in species assemblages as diverse as those dominated by sharks and ants. We highlight two major pathways for creating top-heaviness, via: (1) endogenous channels that enhance energy transfer across trophic boundaries within a community and (2) exogenous pathways that transfer energy into communities from across spatial and temporal boundaries. Consumer-resource models and allometric trophic network models combined with niche models reveal the nature of core mechanisms for promoting top-heaviness. Outputs from these models suggest that top-heavy communities can be stable, but they also reveal sources of instability. Humans are both increasing and decreasing top-heaviness in nature with ecological consequences. Current and future research on the drivers of top-heaviness can help elucidate fundamental mechanisms that shape the architecture of ecological communities and govern energy flux within and between communities. Questions emerging from the study of top-heaviness also usefully draw attention to the incompleteness and inconsistency by which ecologists often establish definitional boundaries for communities.

Blinded by the light? Nearshore energy pathway coupling and relative predator biomass increase with reduced water transparency across lakes.

Habitat coupling is a concept that refers to consumer integration of resources derived from different habitats. This coupling unites fundamental food web pathways (e.g., cross-habitat trophic linkages) that mediate key ecological processes such as biomass flows, nutrient cycling, and stability. We consider the influence of water transparency, an important environmental driver in aquatic ecosystems, on habitat coupling by a light-sensitive predator, walleye (Sander vitreus), and its prey in 33 Canadian lakes. Our large-scale, across-lake study shows that the contribution of nearshore carbon (δ13C) relative to offshore carbon (δ13C) to walleye is higher in less transparent lakes. To a lesser degree, the contribution of nearshore carbon increased with a greater proportion of prey in nearshore compared to offshore habitats. Interestingly, water transparency and habitat coupling predict among-lake variation in walleye relative biomass. These findings support the idea that predator responses to changing conditions (e.g., water transparency) can fundamentally alter carbon pathways, and predator biomass, in aquatic ecosystems. Identifying environmental factors that influence habitat coupling is an important step toward understanding spatial food web structure in a changing world.

Daphnia inhibits the emergence of spatial pattern in a simple consumer-resource system.

Spatial self-organization can occur in many ecosystems with important effects on food web dynamics and the maintenance of biodiversity. The consumer-resource interaction is known to generate spatial patterning, but only a few empirical studies have investigated the effect of the consumer on resource distribution. Here we report results from a large aquatic mesocosm experiment used to investigate the effect of the consumer Daphnia magna on the distribution of its resource, the green algae Chlorella vulgaris. We maintained large tanks with capacity for 26 ,000 L with either algae or both algae and Daphnia in different temperature conditions. We found that the presence of D. magna inhibited spatial structure in algal distribution that arose as a consequence of increasing temperature. We conjecture that this homogenization effect might be caused by a combination of high mobility combined with high rates of algal consumption by Daphnia. Our study emphasizes the importance of both local constraints on growth and behavioral responses in either promoting or suppressing spatial self-organization in natural populations.

Effects of differential habitat warming on complex communities.

Food webs unfold across a mosaic of micro and macro habitats, with each habitat coupled by mobile consumers that behave in response to local environmental conditions. Despite this fundamental characteristic of nature, research on how climate change will affect whole ecosystems has overlooked (i) that climate warming will generally affect habitats differently and (ii) that mobile consumers may respond to this differential change in a manner that may fundamentally alter the energy pathways that sustain ecosystems. This reasoning suggests a powerful, but largely unexplored, avenue for studying the impacts of climate change on ecosystem functioning. Here, we use lake ecosystems to show that predictable behavioral adjustments to local temperature differentials govern a fundamental structural shift across 54 food webs. Data show that the trophic pathways from basal resources to a cold-adapted predator shift toward greater reliance on a cold-water refuge habitat, and food chain length increases, as air temperatures rise. Notably, cold-adapted predator behavior may substantially drive this decoupling effect across the climatic range in our study independent of warmer-adapted species responses (for example, changes in near-shore species abundance and predator absence). Such modifications reflect a flexible food web architecture that requires more attention from climate change research. The trophic pathway restructuring documented here is expected to alter biomass accumulation, through the regulation of energy fluxes to predators, and thus potentially threatens ecosystem sustainability in times of rapid environmental change.

A role for brain size and cognition in food webs.

Predators tend to be large and mobile, enabling them to forage in spatially distinct food web compartments (e.g. littoral and pelagic aquatic macrohabitats). This feature can stabilise ecosystems when predators are capable of rapid behavioural response to changing resource conditions in distinct habitat compartments. However, what provides this ability to respond behaviourally has not been quantified. We hypothesised that predators require increased cognitive abilities to occupy their position in a food web, which puts pressure to increase brain size. Consistent with food web theory, we found that fish relative brain size increased with increased ability to forage across macrohabitats and increased relative trophic positions in a lacustrine food web, indicating that larger brains may afford the cognitive capacity to exploit various habitats flexibly, thus contributing to the stability of whole food webs.