Foraging rates from metabarcoding: Predators have reduced functional responses in wild, diverse prey communities.

Functional responses describe foraging rates across prey densities and underlie many fundamental ecological processes. Most functional response knowledge comes from simplified lab experiments, but we do not know whether these experiments accurately represent foraging in nature. In addition, the difficulty of conducting multispecies functional response experiments means that it is unclear whether interaction strengths are weakened in the presence of multiple prey types. We developed a novel method to estimate wild predators' foraging rates from metabarcoding data and use this method to present functional responses for wild wolf spiders foraging on 27 prey families. These field functional responses were considerably reduced compared to lab functional responses. We further find that foraging is sometimes increased in the presence of other prey types, contrary to expectations. Our novel method for estimating field foraging rates will allow researchers to determine functional responses for wild predators and address long-standing questions about foraging in nature.

Temperature and predators as interactive drivers of community properties.

The effects of warming on ecological communities emerge from a range of potentially asymmetric impacts on individual physiology and development. Understanding these responses, however, is limited by our ability to connect mechanisms or emergent patterns across the many processes that drive variation in demography. Further complicating this understanding is the gain or loss of predators to many communities, which may interact with changes in temperature to drive community change. Here we conducted a factorial warming and predation experiment to test generalized predictions about responses to warming. We used microcosms with a range of protists, rotifers, and a gastrotrich, with and without the predator Actinosphaerium, to assess changes in diversity, body size, function, and composition in response to warming. We find that community respiration and predator:prey biovolume ratios peak at intermediate temperatures, while species richness declined with temperature. We also found that overall biomass increased with species richness, driven by the effect of temperature on richness. There was little evidence of an interaction between predation and temperature change, likely because the predator was mostly limited to the intermediate temperatures. Overall, our results suggest that general predictions about community change are still challenging to make but may benefit by considering multiple dimensions of community patterns in an integrated way.

Viral Chemotaxis of Paramecium Bursaria Altered by Algal Endosymbionts.

Chemotaxis is widespread across many taxa and often aids resource acquisition or predator avoidance. Species interactions can modify the degree of movement facilitated by chemotaxis. In this study, we investigated the influence of symbionts on Paramecium bursaria's chemotactic behavior toward chloroviruses. To achieve this, we performed choice experiments using chlorovirus and control candidate attractors (virus stabilization buffer and pond water). We quantified the movement of Paramecia grown with or without algal and viral symbionts toward each attractor. All Paramecia showed some chemotaxis toward viruses, but cells without algae and viruses showed the most movement toward viruses. Thus, the endosymbiotic algae (zoochlorellae) appeared to alter the movement of Paramecia toward chloroviruses, but it was not clear that ectosymbiotic viruses (chlorovirus) also had this effect. The change in behavior was consistent with a change in swimming speed, but a change in attraction remains possible. The potential costs and benefits of chemotactic movement toward chloroviruses for either the Paramecia hosts or its symbionts remain unclear.

Lessons from Chloroviruses: the Complex and Diverse Roles of Viruses in Food Webs.

Viruses can have large effects on the ecological communities in which they occur. Much of this impact comes from the mortality of host cells, which simultaneously alters microbial community composition and causes the release of matter that can be used by other organisms. However, recent studies indicate that viruses may be even more deeply integrated into the functioning of ecological communities than their effect on nutrient cycling suggests. In particular, chloroviruses, which infect chlorella-like green algae that typically occur as endosymbionts, participate in three types of interactions with other species. Chlororviruses (i) can lure ciliates from a distance, using them as a vector; (ii) depend on predators for access to their hosts; and (iii) get consumed as a food source by, at least, a variety of protists. Therefore, chloroviruses both depend on and influence the spatial structures of communities as well as the flows of energy through those communities, driven by predator-prey interactions. The emergence of these interactions are an eco-evolutionary puzzle, given the interdependence of these species and the many costs and benefits that these interactions generate.

Intraguild predation is increased in areas of low prey diversity in a generalist predator community.

Niche differentiation and intraguild predation (IGP) can allow ecologically similar species to coexist, although it is unclear which coexistence mechanism predominates in consumer communities. Until now, a limited ability to quantify diets from metabarcoding data has precluded the use of sequencing data to determine the relative importance of these mechanisms. Here, we pair a recent metabarcoding quantification approach with stable isotope analysis to examine diet composition in a wolf spider community. We compare the prevalence of resource partitioning and IGP in these spiders and test whether factors that influence foraging performance, including individual identity, morphology, prey community and environmental conditions, can explain variation in diet composition and IGP. Extensive IGP is likely the primary coexistence mechanism in this community, and other factors to which foraging variation is often attributed do not explain diet composition and IGP here. Rather, IGP increases as prey diversity decreases. Foragers are driven to IGP where resource niches are limited. We highlight the need to examine how drivers of predator-prey interaction strengths translate into foraging in natural systems.

Predator feeding rates may often be unsaturated under typical prey densities.

Predator feeding rates (described by their functional response) must saturate at high prey densities. Although thousands of manipulative functional response experiments show feeding rate saturation at high densities under controlled conditions, it remains unclear how saturated feeding rates are at natural prey densities. The general degree of feeding rate saturation has important implications for the processes determining feeding rates and how they respond to changes in prey density. To address this, we linked two databases-one of functional response parameters and one on mass-abundance scaling-through prey mass to calculate a feeding rate saturation index. We find that: (1) feeding rates may commonly be unsaturated and (2) the degree of saturation varies with predator and prey taxonomic identities and body sizes, habitat, interaction dimension and temperature. These results reshape our conceptualisation of predator-prey interactions in nature and suggest new research on the ecological and evolutionary implications of unsaturated feeding rates.

The consumption of viruses returns energy to food chains.

Viruses impact host cells and have indirect effects on ecosystem processes. Plankton such as ciliates can reduce the abundance of virions in water, but whether virus consumption translates into demographic consequences for the grazers is unknown. Here, we show that small protists not only can consume viruses they also can grow and divide given only viruses to eat. Moreover, the ciliate Halteria sp. foraging on chloroviruses displays dynamics and interaction parameters that are similar to other microbial trophic interactions. These results suggest that the effect of viruses on ecosystems extends beyond (and in contrast to) the viral shunt by redirecting energy up food chains.

Stochasticity directs adaptive evolution toward nonequilibrium evolutionary attractors.

Stochastic processes such as genetic drift may hinder adaptation, but the effect of such stochasticity on evolution via its effect on ecological dynamics is poorly understood. Here we evaluate patterns of adaptation in a population subject to variation in demographic stochasticity. We show that stochasticity can alter population dynamics and lead to evolutionary outcomes that are not predicted by classic eco-evolutionary modeling approaches. We also show, however, that these outcomes are governed by nonequilibrium evolutionary attractors-these are maxima in lifetime reproductive success when stochasticity keeps the ecological system away from the deterministic equilibrium. These NEEAs alter the path of evolution but are not visible through the equilibrium lens that underlies much evolutionary theory. Our results reveal that considering population processes during transient periods can greatly improve our understanding of the path and pace of evolution.

FoRAGE database: A compilation of functional responses for consumers and parasitoids.

Functional responses, the relationships between consumer foraging rate and resource (prey) density, provide key insights into consumer-resource interactions while also being a major driver of population dynamics and food web structure. We present a global database of 2598 standardized functional responses and parameters extracted from the published literature. We refit the functional responses with a Type II model using standardized methods and report the fitted parameters along with data on experimental conditions, consumer and resource taxonomy and type, as well as the habitat and dimensionality of the foraging interaction. The consumer and resource species covered here are taxonomically diverse, from protozoans filtering algae to wasps parasitizing moth larvae to wolves hunting moose. The FoRAGE (Functional Responses from Around the Globe in all Ecosystems) database (doi: 10.5063/DB807S) is a living data set that will be updated periodically as new functional responses are published. Data are released under a CC-By-NC-SA license, and credit should be given to this paper when referring to this specific version of the data release.

Quantifying predator functional responses under field conditions reveals interactive effects of temperature and interference with sex and stage.

Predator functional responses describe predator feeding rates and are central to predator-prey theory. Originally defined as the relationship between predator feeding rates and prey densities, it is now well known that functional responses are shaped by a multitude of factors. However, much of our knowledge about how these factors influence functional responses is based on laboratory studies that are generally logistically constrained to examining only a few factors simultaneously and that have unclear links to the conditions organisms experience in the field. We apply an observational approach for measuring functional responses to understand how sex/stage differences, temperature and predator densities interact to influence the functional response of zebra jumping spiders on midges under natural conditions. We used field surveys of jumping spiders to infer their feeding rates and examine the relationships between feeding rates, sex/stage, midge density, predator density and temperature using generalized additive models. We then used the relationships supported by the models to fit parametric functional responses to the data. We find that feeding rates of zebra jumping spiders follow some expectations from previous laboratory studies such as increasing feeding rates with body size and decreasing feeding rates with predator densities. However, in contrast to previous results, our results also show a lack of temperature response in spider feeding rates and differential decreases in the feeding rates of females and juveniles with densities of different spider sexes/stages. Our results illustrate the multidimensional nature of functional responses in natural settings and reveal how factors influencing functional responses can interact with one another through behaviour and morphology. Further studies investigating the influence of multiple mechanisms on predator functional responses under field conditions will increase our understanding of the drivers of predator-prey interaction strengths and their consequences for communities and ecosystems.

An Empiricist's Guide to Using Ecological Theory.

AbstractA scientific understanding of the biological world arises when ideas about how nature works are formalized, tested, refined, and then tested again. Although the benefits of feedback between theoretical and empirical research are widely acknowledged by ecologists, this link is still not as strong as it could be in ecological research. This is in part because theory, particularly when expressed mathematically, can feel inaccessible to empiricists who may have little formal training in advanced math. To address this persistent barrier, we provide a general and accessible guide that covers the basic, step-by-step process of how to approach, understand, and use ecological theory in empirical work. We first give an overview of how and why mathematical theory is created, then outline four specific ways to use both mathematical and verbal theory to motivate empirical work, and finally present a practical tool kit for reading and understanding the mathematical aspects of ecological theory. We hope that empowering empiricists to embrace theory in their work will help move the field closer to a full integration of theoretical and empirical research.

Towards an integrative view of virus phenotypes.

Understanding how phenotypes emerge from genotypes is a foundational goal in biology. As challenging as this task is when considering cellular life, it is further complicated in the case of viruses. During replication, a virus as a discrete entity (the virion) disappears and manifests itself as a metabolic amalgam between the virus and the host (the virocell). Identifying traits that unambiguously constitute a virus's phenotype is straightforward for the virion, less so for the virocell. Here, we present a framework for categorizing virus phenotypes that encompasses both virion and virocell stages and considers functional and performance traits of viruses in the context of fitness. Such an integrated view of virus phenotype is necessary for comprehensive interpretation of viral genome sequences and will advance our understanding of viral evolution and ecology.

Catalysis of Chlorovirus Production by the Foraging of Bursaria truncatella on Paramecia bursaria Containing Endosymbiotic Algae.

Chloroviruses are large viruses that replicate in chlorella-like green algae and normally exist as mutualistic endosymbionts (referred to as zoochlorellae) in protists such as Paramecium bursaria. Chlorovirus populations rise and fall in indigenous waters through time; however, the factors involved in these virus fluctuations are still under investigation. Chloroviruses attach to the surface of P. bursaria but cannot infect their zoochlorellae hosts because the viruses cannot reach the zoochlorellae as long as they are in the symbiotic phase. Predators of P. bursaria, such as copepods and didinia, can bring chloroviruses into contact with zoochlorellae by disrupting the paramecia, which results in an increase in virus titers in microcosm experiments. Here, we report that another predator of P. bursaria, Bursaria truncatella, can also increase chlorovirus titers. After two days of foraging on P. bursaria, B. truncatella increased infectious chlorovirus abundance about 20 times above the controls. Shorter term foraging (3 h) resulted in a small increase of chlorovirus titers over the controls and more foraging generated more chloroviruses. Considering that B. truncatella does not release viable zoochlorellae either during foraging or through fecal pellets, where zoochlorellae could be infected by chlorovirus, we suggest a third pathway of predator virus catalysis. By engulfing the entire protist and digesting it slowly, virus replication can occur within the predator and some of the virus is passed out through a waste vacuole. These results provide additional support for the hypothesis that predators of P. bursaria are important drivers of chlorovirus population sizes and dynamics.

Thermal adaptation in a holobiont accompanied by phenotypic changes in an endosymbiont.

How and if organisms can adapt to changing temperatures has drastic consequences for the natural world. Thermal adaptation involves finding a match between temperatures permitting growth and the expected temperature distribution of the environment. However, if and how this match is achieved, and how tightly linked species change together, is poorly understood. Paramecium bursaria is a ciliate that has a tight physiological interaction with endosymbiotic green algae (zoochlorellae). We subjected a wild population of P. bursaria to a cold and warm climate (20 and 32℃) for ∼300 generations. We then measured the thermal performance curve (TPC) for intrinsic rate of growth (rmax ) for these evolved lines across temperatures. We also evaluated number and size of the zoochlorellae populations within paramecia cells. TPCs for warm-adapted populations were shallower and broader than TPCs of cold-adapted populations, indicating that the warm populations adapted by moving along a thermal generalist/specialist trade off rather than right-shifting the TPC. Zoochlorellae populations within cold-adapted paramecia had fewer and larger zoochlorellae than hot-adapted paramecia, indicating phenotypic shifts in the endosymbiont accompany thermal adaptation in the host. Our results provide new and novel insight into how species involved in complex interactions will be affected by continuing increasing global temperatures.

Estimating predator functional responses using the times between prey captures.

Predator functional responses describe predator feeding rates and are central to predator-prey theory. Ecologists have measured thousands of predator functional responses using the same basic experimental method. However, this design is ill-suited to address many current questions regarding functional responses. We derive a new experimental design and statistical analysis that quantifies functional responses using the times between a predators' feeding events requiring only one or a few trials. We examine the feasibility of the experimental method and analysis using simulations to assess the ability of the statistical model to estimate functional response parameters and perform a proof-of-concept experiment estimating the functional responses of two individual jumping spiders. Our simulations show that the statistical method reliably estimates functional response parameters. Our proof-of-concept experiment illustrates that the method provides reasonable estimates of functional response parameters. By virtue of the fewer number of trials required to measure a functional response, the method derived here promises to expand the questions that can be addressed using functional response experiments and the systems in which they can be measured. Thus, we hope that our method will refine our understanding of functional responses and predator-prey interactions more generally.

Trophic cascades alter eco-evolutionary dynamics and body size evolution.

Trait evolution in predator-prey systems can feed back to the dynamics of interacting species as well as cascade to impact the dynamics of indirectly linked species (eco-evolutionary trophic cascades; EETCs). A key mediator of trophic cascades is body mass, as it both strongly influences and evolves in response to predator-prey interactions. Here, we use Gillespie eco-evolutionary models to explore EETCs resulting from top predator loss and mediated by body mass evolution. Our four-trophic-level food chain model uses allometric scaling to link body mass to different functions (ecological pleiotropy) and is realistically parameterized from the FORAGE database to mimic the parameter space of a typical freshwater system. To track real-time changes in selective pressures, we also calculated fitness gradients for each trophic level. As predicted, top predator loss generated alternating shifts in abundance across trophic levels, and, depending on the nature and strength in changes to fitness gradients, also altered trajectories of body mass evolution. Although more distantly linked, changes in the abundance of top predators still affected the eco-evolutionary dynamics of the basal producers, in part because of their relatively short generation times. Overall, our results suggest that impacts on top predators can set off transient EETCs with the potential for widespread indirect impacts on food webs.

Detecting the Signature of Body Mass Evolution in the Broad-Scale Architecture of Food Webs.

AbstractBody mass-based links between predator and prey are fundamental to the architecture of food webs. These links determine who eats whom across trophic levels and strongly influence the population abundance, flow of energy, and stability properties of natural communities. Body mass links scale up to create predator-prey mass relationships across species, but the origin of these relationships is unclear. Here I show that predator-prey mass relationships are consistent with the idea that body mass evolves to maximize a dependable supply of resource uptake. I used a global database of ~2,100 predator-prey links and a mechanistic optimization model to correctly predict the slope of the predator-prey mass scaling relationships across species generally and for nine taxonomic subsets. The model also predicted cross-group variation in the heights of the body mass relationships, providing an integrated explanation for mass relationships and their variation across taxa. The results suggest that natural selection on body mass at the local scale is detectable in ecological organization at the macro scale.

Using patterns in prey DNA digestion rates to quantify predator diets.

Dietary metabarcoding-the process of taxonomic identification of food species from DNA in consumer guts or faeces-has been rapidly adopted by ecologists to gain insights into biocontrol, invasive species and the structure of food webs. However, an outstanding issue with metabarcoding is the semi-quantitative nature of the data it provides: because metabarcoding is likely to produce false negatives for some prey more often than for other prey, we cannot infer relative frequencies of prey in the diet. To correct for this, we can adjust detected prey frequencies using DNA detectability half-lives unique to each predator-prey combination. Because the feeding experiments required to deduce these half-lives are time- and resource-intensive, our ability to weight the frequency of observations using their detectability has thus far been limited to systems with just a few prey. Here, we present a meta-analysis of 24 spider prey DNA half-lives and show that these half-lives are predictable given predator and prey mass, predator family, digestion temperature and DNA amplicon length. We further provide a new technique for weighting observations with half-lives, which allows not just for the ranking of prey in the diet, but reveals the proportion of the diet each prey comprises. Lastly, we apply this method to published dietary metabarcoding data to calculate half-lives and proportion of the predator's diet for 35 prey families, demonstrating that this technique can generate improved understanding of diets in real, diverse systems.

Temperature alters the shape of predator-prey cycles through effects on underlying mechanisms.

BACKGROUND: Predicting the effects of climate warming on the dynamics of ecological systems requires understanding how temperature influences birth rates, death rates and the strength of species interactions. The temperature dependance of these processes-which are the underlying mechanisms of ecological dynamics-is often thought to be exponential or unimodal, generally supported by short-term experiments. However, ecological dynamics unfold over many generations. Our goal was to empirically document shifts in predator-prey cycles over the full range of temperatures that can possibly support a predator-prey system and then to uncover the effect of temperature on the underlying mechanisms driving those changes. METHODS: We measured the population dynamics of the Didinium-Paramecium predator-prey system across a wide range of temperatures to reveal systematic changes in the dynamics of the system. We then used ordinary differential equation fitting to estimate parameters of a model describing the dynamics, and used these estimates to assess the long-term temperature dependance of all the underlying mechanisms. RESULTS: We found that predator-prey cycles shrank in state space from colder to hotter temperatures and that both cycle period and amplitude varied with temperature. Model parameters showed mostly unimodal responses to temperature, with one parameter (predator mortality) increasing monotonically with temperature and one parameter (predator conversion efficiency) invariant with temperature. Our results indicate that temperature can have profound, systematic effects on ecological dynamics, and these can arise through diverse and simultaneous changes in multiple underlying mechanisms. Predicting the effects of temperature on ecological dynamics may require additional investigation into how the underlying drivers of population dynamics respond to temperature beyond a short-term, acute response.

Trade-offs between morphology and thermal niches mediate adaptation in response to competing selective pressures.

The effects of climate change-such as increased temperature variability and novel predators-rarely happen in isolation, but it is unclear how organisms cope with multiple stressors simultaneously. To explore this, we grew replicate Paramecium caudatum populations in either constant or variable temperatures and exposed half to predation. We then fit thermal performance curves (TPCs) of intrinsic growth rate (r max) for each replicate population (N = 12) across seven temperatures (10°C-38°C). TPCs of P. caudatum exposed to both temperature variability and predation responded only to one or the other (but not both), resulting in unpredictable outcomes. These changes in TPCs were accompanied by changes in cell morphology. Although cell volume was conserved across treatments, cells became narrower in response to temperature variability and rounder in response to predation. Our findings suggest that predation and temperature variability produce conflicting pressures on both thermal performance and cell morphology. Lastly, we found a strong correlation between changes in cell morphology and TPC parameters in response to predation, suggesting that responses to opposing selective pressures could be constrained by trade-offs. Our results shed new light on how environmental and ecological pressures interact to elicit changes in characteristics at both the individual and population levels. We further suggest that morphological responses to interactive environmental forces may modulate population-level responses, making prediction of long-term responses to environmental change challenging.