Functional traits of predators and decomposer prey determine context dependency in trophic control over ecosystems.

Research Highlight: Piccoli, G. C. d. O., Antiqueira, P. A. P., Srivastava, D. S., & Romero, G. Q. (2024). Trophic cascades within and across ecosystems: The role of anti-predatory defences, predator type and detritus quality. Journal of Animal Ecology, 00, 1-14. https://doi.org/10.1111/1365-2656.14063. Ecosystem functioning is controlled by the interplay between bottom-up supply of limiting nutrients and top-down animal feedback effects. However, the degree of animal versus nutrient control is context-dependent. A key challenge lies in characterizing this context dependency which is hypothesized to depend on differences in animal functional traits. Reporting on an important experiment, Piccoli et al. (2014) evaluate how interactions among functionally different predators and decomposer prey create context dependency in top-down control of a model system-tropical bromeliad tank ecosystems. Bromeliad plants hold water in their tanks supporting microcosm ecosystems containing terrestrial and aquatic insect larvae and arachnids. The ecosystems are supported by nutrients in plant litter that rains down from forest canopies into the tanks. Nutrients are released after litter is decomposed by a functionally diverse community of larval insect decomposers that differ in feeding mode and antipredator defence strategy. This decomposer community is preyed upon by an exclusively narrowly ranging aquatic insect larval predator and widely ranging spider predator that crosses between the aquatic and surrounding terrestrial ecosystems. Experimental manipulation of the animal community to test for the degree of control by predators mediated by the functionally diverse prey community included four treatments: (i) a control with the detritivores composing different function groups but without predators, (ii) the cross-ecosystem spider predator added, (iii) the purely aquatic damselfly larvae predator added and (iv) both predator types added to capture their interacting effect on ecosystem function (decomposition, nutrient release, and plant growth). Notably, the study resolved the causal pathways and strengths of direct and indirect control using structural equation modelling. These findings reveal how context dependency arises due to different capacities of the predators alone and together to overcome prey defences and control their abundances, with attendant cascading effects that diminished as well as enhanced decomposition and nutrient release to support bromeliad plant production. The study reveals that predators have a decided, albeit qualitatively and quantitatively different, hand in shaping the degree of bottom-up control through feedback effect on the release of limiting nutrients. This ground-breaking study provides a way forward in understanding the mechanisms determining context dependency in the control over ecosystem functioning.

Plant mycorrhizal associations mediate the zoogeochemical effects of calving subsidies by a forest ungulate.

Animals interact with and impact ecosystem biogeochemical cycling-processes known as zoogeochemistry. While the deposition of various animal materials (e.g. carcasses and faeces) has been shown to create nutrient hotspots and alter nutrient cycling and storage, the inputs from parturition (i.e. calving) have yet to be explored. We examine the effects of ungulate parturition, which often occurs synchronously during spring green-up and therefore aligns with increased plant nitrogen demand in temperate biomes. Impacts of zoogeochemical inputs are likely context-dependent, where differences in material quality, quantity and the system of deposition modulate their impacts. Plant mycorrhizal associations, especially, create different nutrient-availability contexts, which can modify the effects of nutrient inputs. We, therefore, hypothesize that mycorrhizal associations modulate the consequences of parturition on soil nutrient dynamics and nitrogen pools. We established experimental plots that explore the potential of two kinds of zoogeochemical inputs deposited at ungulate parturition (placenta and natal fluid) in forest microsites dominated by either ericoid mycorrhizal (ErM) or ectomycorrhizal (EcM) plants. We assess how these inputs affect rates of nutrient cycling and nitrogen content in various ecosystem pools, using isotope tracers to track the fate of nitrogen inputs into plant and soil pools. Parturition treatments accelerate nutrient cycling processes and increase nitrogen contents in the plant leaf, stem and fine root pools. The ecosystem context strongly modulates these effects. Microsites dominated by ErM plants mute parturition treatment impacts on most nutrient cycling processes and plant pools. Both plant-fungal associations are, however, equally efficient at retaining nitrogen, although retention of nitrogen in the parturition treatment plots was more than two times lower than in control plots. Our results highlight the potential importance of previously unexamined nitrogen inputs from animal inputs, such as those from parturition, in contributing to fine-scale heterogeneity in nutrient cycling and availability. Animal inputs should therefore be considered, along with their interactions with plant mycorrhizal associations, in terms of how zoogeochemical dynamics collectively affect nutrient heterogeneity in ecosystems.

Cascading effects of a disease outbreak in a remote protected area.

Disease outbreaks induced by humans increasingly threaten wildlife communities worldwide. Like predators, pathogens can be key top-down forces in ecosystems, initiating trophic cascades that may alter food webs. An outbreak of mange in a remote Andean protected area caused a dramatic population decline in a mammalian herbivore (the vicuña), creating conditions to test the cascading effects of disease on the ecological community. By comparing a suite of ecological measurements to pre-disease baseline records, we demonstrate that mange restructured tightly linked trophic interactions previously driven by a mammalian predator (the puma). Following the mange outbreak, scavenger (Andean condor) occurrence in the ecosystem declined sharply and plant biomass and cover increased dramatically in predation refuges where herbivory was historically concentrated. The evidence shows that a disease-induced trophic cascade, mediated by vicuña density, could supplant the predator-induced trophic cascade, mediated by vicuña behaviour, thereby transforming the Andean ecosystem.

The context dependence of non-consumptive predator effects.

Non-consumptive predator effects (NCEs) are now widely recognised for their capacity to shape ecosystem structure and function. Yet, forecasting the propagation of these predator-induced trait changes through particular communities remains a challenge. Accordingly, focusing on plasticity in prey anti-predator behaviours, we conceptualise the multi-stage process by which predators trigger direct and indirect NCEs, review and distil potential drivers of contingencies into three key categories (properties of the prey, predator and setting), and then provide a general framework for predicting both the nature and strength of direct NCEs. Our review underscores the myriad factors that can generate NCE contingencies while guiding how research might better anticipate and account for them. Moreover, our synthesis highlights the value of mapping both habitat domains and prey-specific patterns of evasion success ('evasion landscapes') as the basis for predicting how direct NCEs are likely to manifest in any particular community. Looking ahead, we highlight two key knowledge gaps that continue to impede a comprehensive understanding of non-consumptive predator-prey interactions and their ecosystem consequences; namely, insufficient empirical exploration of (1) context-dependent indirect NCEs and (2) the ways in which direct and indirect NCEs are shaped interactively by multiple drivers of context dependence.

Species in ecosystems and all that jazz.

Ecosystem ecologists explore how different kinds of species fit together to drive ecosystem processes such as nutrient cycling and productivity. This research is motivated by theories that assume that the suite of traits that characterize a species' form determines its function, that these traits have become fixed over evolutionary time, and that ensuing ecosystem process are not resilient to environmental change. Here, I explore new research that re-evaluates this theory. Recent results suggest that functional traits are malleable, enabling species to rapidly respond and adapt to each other as environmental conditions change with predictable effects on ecosystem processes. These basic research findings suggest that species adaptations may impart in ecosystems an inherent capacity to weather environmental changes, thereby offering deeper understanding about which biological attributes protect ecological functions and which are needed to restore damaged ecosystems.

Carnivore conservation needs evidence-based livestock protection.

Carnivore predation on livestock often leads people to retaliate. Persecution by humans has contributed strongly to global endangerment of carnivores. Preventing livestock losses would help to achieve three goals common to many human societies: preserve nature, protect animal welfare, and safeguard human livelihoods. Between 2016 and 2018, four independent reviews evaluated >40 years of research on lethal and nonlethal interventions for reducing predation on livestock. From 114 studies, we find a striking conclusion: scarce quantitative comparisons of interventions and scarce comparisons against experimental controls preclude strong inference about the effectiveness of methods. For wise investment of public resources in protecting livestock and carnivores, evidence of effectiveness should be a prerequisite to policy making or large-scale funding of any method or, at a minimum, should be measured during implementation. An appropriate evidence base is needed, and we recommend a coalition of scientists and managers be formed to establish and encourage use of consistent standards in future experimental evaluations.

Invertebrate functional traits and terrestrial nutrient cycling: Insights from a global meta-analysis.

Functional traits are useful for characterizing variation in community and ecosystem dynamics. Most advances in trait-based ecology to date centre on plant functional traits, although there is an increasing recognition that animal traits are also key contributors to processes operating at the community or ecosystem scale. Terrestrial invertebrates are incredibly diverse and ubiquitous animals with important roles in nutrient cycling. Despite their widespread influence on ecosystem processes, we currently lack a synthetic understanding of how invertebrate functional traits affect terrestrial nutrient cycling. We present a meta-analysis of 511 paired observations from 122 papers that examined how invertebrate functional traits affected litter decomposition rates, nitrogen pools and litter C:N ratios. Based on the available data, we specifically assessed the effects of feeding mode (bioturbation, detritus shredding, detritus grazing, leaf chewing, leaf piercing, ambush predators, active hunting predators) and body size (macro- and micro-invertebrates) on nutrient cycling. The effects of invertebrates on terrestrial nutrient cycling varied according to functional trait. The inclusion of both macro- (≥2 mm) and micro-invertebrates (<2 mm) increased litter decomposition by 20% and 19%, respectively. All detritivorous feeding modes enhanced litter decomposition rates, with bioturbators, detritus shredders and detritus grazers increasing decomposition by 28%, 22% and 15%, respectively. Neither herbivore feeding mode (e.g. leaf chewers and leaf piercers) nor predator hunting mode (ambush and active hunting) affected decomposition. We also revealed that bioturbators and detritus grazers increased soil nitrogen availability by 99% and 70%, respectively, and that leaf-chewing herbivores had a weak effect on litterfall stoichiometry via reducing C:N ratios by 11%. Although functional traits might be useful predictors of ecosystem processes, our findings suggest context-dependent effects of invertebrate traits on terrestrial nutrient cycling. Detritivore functional traits (i.e. bioturbators, detritus shredders and detritus grazers) are more consistent with increased rates of nutrient cycling, whereas our currently characterized predator and herbivore traits are less predictive. Future research is needed to identify, standardize and deliberately study the impacts of invertebrate functional traits on nutrient cycling in hopes of revealing the key functional traits governing ecosystem functioning worldwide.

A methodological roadmap to quantify animal-vectored spatial ecosystem subsidies.

Energy, nutrients and organisms move over landscapes, connecting ecosystems across space and time. Meta-ecosystem theory investigates the emerging properties of local ecosystems coupled spatially by these movements of organisms and matter, by explicitly tracking exchanges of multiple substances across ecosystem borders. To date, meta-ecosystem research has focused mostly on abiotic flows-neglecting biotic nutrient flows. However, recent work has indicated animals act as spatial nutrient vectors when they transport nutrients across landscapes in the form of excreta, egesta and their own bodies. Partly due to its high level of abstraction, there are few empirical tests of meta-ecosystem theory. Furthermore, while animals may be viewed as important mediators of ecosystem functions, better integration of tools is needed to develop predictive insights of their relative roles and impacts on diverse ecosystems. We present a methodological roadmap that explains how to do such integration by discussing how to combine insights from movement, foraging and ecosystem ecology to develop a coherent understanding of animal-vectored nutrient transport on meta-ecosystems processes. We discuss how the slate of newly developed technologies and methods-tracking devices, mechanistic movement models, diet reconstruction techniques and remote sensing-that when integrated have the potential to advance the quantification of animal-vectored nutrient flows and increase the predictive power of meta-ecosystem theory. We demonstrate that by integrating novel and established tools of animal ecology, ecosystem ecology and remote sensing, we can begin to identify and quantify animal-mediated nutrient translocation by large animals. We also provide conceptual examples that show how our proposed integration of methodologies can help investigate ecosystem impacts of large animal movement. We conclude by describing practical advancements to understanding cross-ecosystem contributions of animals on the move. Understanding the mechanisms by which animals shape ecosystem dynamics is important for ongoing conservation, rewilding and restoration initiatives around the world, and for developing more accurate models of ecosystem nutrient budgets. Our roadmap will enable ecologists to better qualify and quantify animal-mediated nutrient translocation for animals on the move.

The economics of conservation debt: a natural capital approach to revealed valuation of ecological dynamics.

Some species are valued for their direct usefulness to society, through immediate financial returns from market activities such as harvesting or ecotourism. But many are valued for their passive usefulness, i.e., their mere existence contributes to supporting, regulating or cultural environmental services that support human well-being. Hence, there is inherent social value to conserving such species as natural assets. However, such species are seldom priced as natural assets, and thus not accounted for in sustainability wealth measures because deriving non-market prices is challenging. We overcome this limitation by presenting a new approach for natural asset pricing of species with passive value that can be incorporated into national sustainability wealth accounting. We explicitly consider the relationship between prevailing institutions, species interactions, and ecosystem dynamics. Our approach is illustrated with the case of threatened woodland caribou in the Alberta Oil Sands. We show that conservation can be considered an investment while destructive activities can lead to a loss or conservation debt; and forgoing destructive activities can be considered a capital gain, increasing future wealth. Our approach reveals that caribou conservation in Alberta is leading to a conservation debt on the order of CA$800 million.

Opposite effects of daytime and nighttime warming on top-down control of plant diversity.

Ecological analyses of climate warming explore how rising mean temperature will affect the species composition of communities and their associated functioning. Experimentation usually presumes that warming arises from simultaneous increase in daily maximum (daytime) and minimum (nighttime) temperatures. Yet evidence shows that mean warming arises largely from increasing nighttime temperatures. We report on a 3-yr experiment that compared the effects of daytime and nighttime warming on a community comprising herbaceous plants, grasshopper herbivores and predatory spiders. We warmed experimental mesocosms 3-4°C above ambient control treatments during the daytime (06:00-18:00 h) or nighttime (18:00-06:00 h). Daytime warming caused spiders to seek a thermal refuge low in the plant canopy and away from grasshopper prey, which allowed grasshoppers to spend more time feeding on a competitively dominant plant species. Nighttime had the opposite effect, where spider activity increased causing grasshoppers to reduce feeding. Two consecutive years of daytime warming resulted in a suppression of the competitive dominant plant and increased the diversity and evenness of the plant community, whereas nighttime warming had opposite effects. These results show that ignoring the nuanced effects of asymmetrical warming may lead to inaccurate conclusions about the net effects of climate change on ecosystems.

Eco-Evolutionary Dynamics: The Predator-Prey Adaptive Play and the Ecological Theater.

The emerging field of eco-evolutionary dynamics has demonstrated that both ecological and evolutionary processes can occur contemporaneously. Ecological interactions, such as between predator and prey, are important focal areas where an eco-evolutionary perspective can advance understanding about phenotypically plastic and adaptive evolutionary responses. In predator-prey interactions, both species reciprocally respond and adapt to each other in order to simultaneously ensure resource consumption and predation avoidance. Here we sketch out a way to help unify experimental and analytical approaches to both eco-evolutionary dynamics and predator-prey interactions, with a specific focus on terrestrial systems. We discuss the need to view predator-prey eco-evolutionary dynamics as a perpetually adaptive interplay with constantly shifting pressures and feedbacks, rather than viewing it as driving a set evolutionary trajectory. We then outline our perspective on how to understand eco-evolutionary patterns in a predator-prey context. We propose initiating insight by distinguishing phenotypic plasticity against genetic change (i.e., "molecular reductionism") and further applying a landscape-scale perspective (i.e., "landscape holism"). We believe that studying predator-prey interactions under an eco-evolutionary lens can provide insights into how general and, consequently, predictable species' evolutionary responses are to their contemporary environments.

Applying population and community ecology theory to advance understanding of belowground biogeochemistry.

Approaches to quantifying and predicting soil biogeochemical cycles mostly consider microbial biomass and community composition as products of the abiotic environment. Current numerical approaches then primarily emphasise the importance of microbe-environment interactions and physiology as controls on biogeochemical cycles. Decidedly less attention has been paid to understanding control exerted by community dynamics and biotic interactions. Yet a rich literature of theoretical and empirical contributions highlights the importance of considering how variation in microbial population ecology, especially biotic interactions, is related to variation in key biogeochemical processes like soil carbon formation. We demonstrate how a population and community ecology perspective can be used to (1) understand the impact of microbial communities on biogeochemical cycles and (2) reframe current theory and models to include more detailed microbial ecology. Through a series of simulations we illustrate how density dependence and key biotic interactions, such as competition and predation, can determine the degree to which microbes regulate soil biogeochemical cycles. The ecological perspective and model simulations we present lay the foundation for developing empirical research and complementary models that explore the diversity of ecological mechanisms that operate in microbial communities to regulate biogeochemical processes.

Predator community composition is linked to soil carbon retention across a human land use gradient.

Soil carbon (C) storage is a major component of the carbon cycle. Consensus holds that soil C uptake and storage is regulated by plant-microbe-soil interactions. However, the contribution of animals in aboveground food webs to this process has been overlooked. Using insights from prior long-term experimentation in an old-field ecosystem and mathematical modeling, we predicted that the amount of soil C retention within a field should increase with the proportion of active hunting predators comprising the aboveground community of active hunting and sit-and-wait predators. This comes about because predators with different hunting modes have different cascading effects on plants. Our test of the prediction revealed that the composition of the arthropod predator community and associated cascading effects on the plant community explained 41% of variation in soil C retention among 15 old fields across a human land use gradient. We also evaluated the potential for several other candidate factors to explain variation in soil C retention among fields, independent of among-field variation in the predator community. These included live plant biomass, insect herbivore community composition, soil arthropod decomposer community composition, degree of land use development around the fields, field age, and soil texture. None of these candidate variables significantly explained soil C retention among the fields. The study offers a generalizable understanding of the pathways through which arthropod predator community composition can contribute to old-field ecosystem carbon storage. This insight helps support ongoing efforts to understand and manage the effects of anthropogenic land use change on soil C storage.

Toward a community ecology of landscapes: predicting multiple predator-prey interactions across geographic space.

Community ecology was traditionally an integrative science devoted to studying interactions between species and their abiotic environments in order to predict species' geographic distributions and abundances. Yet for philosophical and methodological reasons, it has become divided into two enterprises: one devoted to local experimentation on species interactions to predict community dynamics; the other devoted to statistical analyses of abiotic and biotic information to describe geographic distribution. Our goal here is to instigate thinking about ways to reconnect the two enterprises and thereby return to a tradition to do integrative science. We focus specifically on the community ecology of predators and prey, which is ripe for integration. This is because there is active, simultaneous interest in experimentally resolving the nature and strength of predator-prey interactions as well as explaining patterns across landscapes and seascapes. We begin by describing a conceptual theory rooted in classical analyses of non-spatial food web modules used to predict species interactions. We show how such modules can be extended to consideration of spatial context using the concept of habitat domain. Habitat domain describes the spatial extent of habitat space that predators and prey use while foraging, which differs from home range, the spatial extent used by an animal to meet all of its daily needs. This conceptual theory can be used to predict how different spatial relations of predators and prey could lead to different emergent multiple predator-prey interactions such as whether predator consumptive or non-consumptive effects should dominate, and whether intraguild predation, predator interference or predator complementarity are expected. We then review the literature on studies of large predator-prey interactions that make conclusions about the nature of multiple predator-prey interactions. This analysis reveals that while many studies provide sufficient information about predator or prey spatial locations, and thus meet necessary conditions of the habitat domain conceptual theory for drawing conclusions about the nature of the predator-prey interactions, several studies do not. We therefore elaborate how modern technology and statistical approaches for animal movement analysis could be used to test the conceptual theory, using experimental or quasi-experimental analyses at landscape scales.

Global synthesis suggests that food web connectance correlates to invasion resistance.

Biological invasions are a key component of global change, and understanding the drivers of global invasion patterns will aid in assessing and mitigating the impact of invasive species. While invasive species are most often studied in the context of one or two trophic levels, in reality species invade communities comprised of complex food webs. The complexity and integrity of the native food web may be a more important determinant of invasion success than the strength of interactions between a small subset of species within a larger food web. Previous efforts to understand the relationship between food web properties and species invasions have been primarily theoretical and have yielded mixed results. Here, we present a synthesis of empirical information on food web connectance and species invasion success gathered from different sources (estimates of food web connectance from the primary literature and estimates of invasion success from the Global Invasive Species Database as well as the primary literature). Our results suggest that higher-connectance food webs tend to host fewer invaders and exert stronger biotic resistance compared to low-connectance webs. We argue that while these correlations cannot be used to infer a causal link between food web connectance and habitat invasibility, the promising findings beg for further empirical research that deliberately tests for relationships between food web connectance and invasion.

Temperature dependence of predation stress and the nutritional ecology of a generalist herbivore.

Prey at risk of predation may experience stress and respond physiologically by altering their metabolic rates. Theory predicts that such physiological changes should alter prey nutrient demands from N-rich to C-rich macronutrients and shift the balance between maintenance and growth/reproduction. Theory further suggests that for ectotherms, temperature stands to exacerbate this stress. Yet, the interactive effects of predation stress and temperature stress on diet, metabolism, and survival of ectotherms are not well known. This knowledge gap was addressed with a laboratory study in which wild juvenile grasshoppers were collected, assigned to one of three groups, and raised at three different temperatures. All grasshoppers had access to equal quantities of two diets composed of opposite carbohydrate : protein ratios. Half of the individuals in each temperature group were exposed to predation risk cues from spider predators, while the other half were kept in risk free conditions. Grasshoppers consumed more carbohydrates when exposed to predation risk, but consumption favored greater protein intake as temperature increased. Moreover, the difference in carbohydrate intake between risk cue and risk free treatments diminished as temperature increased. Furthermore, variability between individual consumption patterns both within and between treatments decreased markedly as temperature increased, suggesting that higher temperatures promote more consistent individual consumption behaviors. Grasshoppers grew faster and larger as temperature increased, which translated into higher survival rates at higher temperatures. Warmer grasshoppers also did not alter their metabolic rates in response to predation risk cues, in contrast to colder grasshoppers. Digestive efficiency increased with temperature as well -- further indicating that lower temperatures were much more stressful than higher temperatures for grasshoppers. The study shows that physiological responses of ectothermic herbivores to predation stress are highly plastic and temperature dependent, with higher temperatures promoting increased protein intake, growth, development, survival, and digestive efficiency relative to colder temperatures. These findings help to reconcile why dietary responses (proportion of protein vs. carbohydrate intake) to predation stress may vary among different prey taxa studied previously.

Intraspecific differences in plant chemotype determine the structure of arthropod food webs.

It is becoming increasingly appreciated that the structure and functioning of ecological food webs are controlled by the nature and level of plant chemicals. It is hypothesized that intraspecific variation in plant chemical resistance, in which individuals of a host-plant population exhibit genetic differences in their chemical contents (called 'plant chemotypes'), may be an important determinant of variation in food web structure and functioning. We evaluated this hypothesis using field assessments and plant chemical assays in the tansy plant Tanacetum vulgare L. (Asteraceae). We examined food webs in which chemotypes of tansy plants are the resource for two specialized aphids, their predators and mutualistic ants. The density of the ant-tended aphid Metopeurum fuscoviride was significantly higher on particular chemotypes (borneol) than others. Clear chemotype preferences between predators were also detected. Aphid specialist seven-spotted ladybird beetles (Coccinella septempunctata) were more often found on camphor plants, while significantly higher numbers of the polyphagous nursery web spider (Pisaura mirabilis) were observed on borneol plants. The analysis of plant chemotype effects on the arthropod community clearly demonstrates a range of possible outcomes between plant-aphid-predator networks. The findings help to offer a deeper insight into how one important factor--plant chemical content--influences which species coexist within a food web on a particular host plant and the nature of their trophic linkages.

Trophic cascade alters ecosystem carbon exchange.

Trophic cascades--the indirect effects of carnivores on plants mediated by herbivores--are common across ecosystems, but their influence on biogeochemical cycles, particularly the terrestrial carbon cycle, are largely unexplored. Here, using a (13)C pulse-chase experiment, we demonstrate how trophic structure influences ecosystem carbon dynamics in a meadow system. By manipulating the presence of herbivores and predators, we show that even without an initial change in total plant or herbivore biomass, the cascading effects of predators in this system begin to affect carbon cycling through enhanced carbon fixation by plants. Prolonged cascading effects on plant biomass lead to slowing of carbon loss via ecosystem respiration and reallocation of carbon among plant aboveground and belowground tissues. Consequently, up to 1.4-fold more carbon is retained in plant biomass when carnivores are present compared with when they are absent, owing primarily to greater carbon storage in grass and belowground plant biomass driven largely by predator nonconsumptive (fear) effects on herbivores. Our data highlight the influence that the mere presence of predators, as opposed to direct consumption of herbivores, can have on carbon uptake, allocation, and retention in terrestrial ecosystems.