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.

A bioenergetic framework for aboveground terrestrial food webs.

Bioenergetic approaches have been greatly influential for understanding community functioning and stability and predicting effects of environmental changes on biodiversity. These approaches use allometric relationships to establish species' trophic interactions and consumption rates and have been successfully applied to aquatic ecosystems. Terrestrial ecosystems, where body mass is less predictive of plant-consumer interactions, present inherent challenges that these models have yet to meet. Here, we discuss the processes governing terrestrial plant-consumer interactions and develop a bioenergetic framework integrating those processes. Our framework integrates bioenergetics specific to terrestrial plants and their consumers within a food web approach while also considering mutualistic interactions. Such a framework is poised to advance our understanding of terrestrial food webs and to predict their responses to environmental changes.

Species portfolio effects dominate seasonal zooplankton stabilization within a large temperate lake.

Portfolio effects (PEs) in ecology refer to the suite of phenomenon where the temporal variation of aggregate ecosystem properties (i.e., abundance) is lower than that of their ecosystem components. An example of this is where differential responses of species to environmental variation generate stability at higher levels of ecological organization (e.g., local community, metapopulation, metacommunity). Most of the research examining such PEs has focused on spatial or interannual variation of ecosystems; however, as global change continues to alter seasonality and ecosystem functioning, understanding the underlying food web structures that help maintain stability at multiple spatial and temporal scales is critical to managing ecological systems. Recent advances investigating diversity-stability relationships has led to the development of frameworks that incorporate a metacommunity perspective which allows for the partitioning of PEs across organizational scales (i.e., local community, metapopulation, cross-community, metacommunity) from local population dynamics (total). This partitioning yields insights into the mechanisms that generate observed PEs in nature. Here, we employed one of these recently developed frameworks on a temporally (1986-1999, 2008-2019) and spatially (five sampling stations, local communities) extensive data set of zooplankton abundance (e.g., density) within a large temperate lake to investigate how temporal (seasonal) and spatial (among site) PEs influence stability within the zooplankton metacommunity. We found that seasonal asynchrony of different zooplankton species within local communities and across communities generated the vast majority of stabilization, while spatial (i.e., metapopulation) dynamics were more synchronous and contributed little to overall system stability. Furthermore, significantly positive diversity-asynchrony relationships at the total, local- and cross-community scales were found as asynchrony was positively correlated with local Shannon diversity. Last, a comparison of PEs over the time periods, during which significant local and global changes (i.e., climate warming, invasive species) have occurred suggests that PEs may be eroding, as increasingly synchronous dynamics and declining diversity in recent years have led to a rise in metacommunity variability. We end by arguing for the critical importance of understanding seasonally driven stabilizing mechanisms as local and global changes threaten to fundamentally alter seasonal signals with potentially strong implications for the structures that lend stability to ecosystems.

Subsidy accessibility drives asymmetric food web responses.

Global change is fundamentally altering flows of natural and anthropogenic subsidies across space and time. After a pointed call for research on subsidies in the 1990s, an industry of empirical work has documented the ubiquitous role subsidies play in ecosystem structure, stability, and function. Here, we argue that physical constraints (e.g., water temperature) and species traits can govern a species' accessibility to resource subsidies, which has been largely overlooked in the subsidy literature. We examined the input of a high-quality, point-source anthropogenic subsidy (aquaculture feed) into a recipient freshwater lake food web. Using a combined bio-tracer approach, we detect a gradient in accessibility of the anthropogenic subsidy within the surrounding food web driven by the thermal preferences of three constituent species, effectively rewiring the recipient lake food web. Because aquaculture is predicted to increase significantly in coming decades to support growing human populations, and global change is altering temperature regimes, then this form of food web alteration may be expected to occur frequently. We argue that subsidy accessibility is a key characteristic of recipient food web interactions that must be considered when trying to understand the impacts of subsidies on ecosystem stability and function under continued global change.

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.

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.

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.

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.

Food web rewiring in a changing world.

Climate change is asymmetrically altering environmental conditions in space, from local to global scales, creating novel heterogeneity. Here, we argue that this novel heterogeneity will drive mobile generalist consumer species to rapidly respond through their behaviour in ways that broadly and predictably reorganize - or rewire - food webs. We use existing theory and data from diverse ecosystems to show that the rapid behavioural responses of generalists to climate change rewire food webs in two distinct and critical ways. First, mobile generalist species are redistributing into systems where they were previously absent and foraging on new prey, resulting in topological rewiring - a change in the patterning of food webs due to the addition or loss of connections. Second, mobile generalist species, which navigate between habitats and ecosystems to forage, will shift their relative use of differentially altered habitats and ecosystems, causing interaction strength rewiring - changes that reroute energy and carbon flows through existing food web connections and alter the food web's interaction strengths. We then show that many species with shared traits can exhibit unified aggregate behavioural responses to climate change, which may allow us to understand the rewiring of whole food webs. We end by arguing that generalists' responses present a powerful and underutilized approach to understanding and predicting the consequences of climate change and may serve as much-needed early warning signals for monitoring the looming impacts of global climate change on entire ecosystems.

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.

Evidence of indiscriminate fishing effects in one of the world's largest inland fisheries.

While human impacts like fishing have altered marine food web composition and body size, the status of the world's important tropical inland fisheries remains largely unknown. Here, we look for signatures of human impacts on the indiscriminately fished Tonle Sap fish community that supports one of the world's largest freshwater fisheries. By analyzing a 15-year time-series (2000-2015) of fish catches for 116 species obtained from an industrial-scale 'Dai' fishery, we find: (i) 78% of the species exhibited decreasing catches through time; (ii) downward trends in catches occurred primarily in medium to large-bodied species that tend to occupy high trophic levels; (iii) a relatively stable or increasing trend in catches of small-sized species, and; (iv) a decrease in the individual fish weights and lengths for several common species. Because total biomass of the catch has remained remarkably resilient over the last 15 years, the increase in catch of smaller species has compensated for declines in larger species. Our finding of sustained production but altered community composition is consistent with predictions from recent indiscriminate theory, and gives a warning signal to fisheries managers and conservationists that the species-rich Tonle Sap is being affected by heavy indiscriminate fishing pressure.

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.

Context-dependent interactions and the regulation of species richness in freshwater fish.

Species richness is regulated by a complex network of scale-dependent processes. This complexity can obscure the influence of limiting species interactions, making it difficult to determine if abiotic or biotic drivers are more predominant regulators of richness. Using integrative modeling of freshwater fish richness from 721 lakes along an 11o latitudinal gradient, we find negative interactions to be a relatively minor independent predictor of species richness in lakes despite the widespread presence of predators. Instead, interaction effects, when detectable among major functional groups and 231 species pairs, were strong, often positive, but contextually dependent on environment. These results are consistent with the idea that negative interactions internally structure lake communities but do not consistently 'scale-up' to regulate richness independently of the environment. The importance of environment for interaction outcomes and its role in the regulation of species richness highlights the potential sensitivity of fish communities to the environmental changes affecting lakes globally.