Behaviourally mediated indirect effects: interference competition increases predation mortality in foraging redshanks

1. The effect of competition for a limiting resource on the population dynamics of competitors is usually assumed to operate directly through starvation, yet may also affect survival indirectly through behaviourally mediated effects that affect risk of predation. Thus, competition can affect more than two trophic levels, and we aim here to provide an example of this. 2. We show that the foraging success of redshanks Tringa totanus (L.) foraging on active prey was highest in the front of flocks, whereas this was not the case for redshanks foraging on inactive prey. Also, when foraging on active prey, foraging success in a flock decreased as more birds passed through a patch, while overall foraging success was not lower on subsequent visits to the same patch. Thus, redshanks foraging on active prey suffered from interference competition, whereas this was not the case for redshanks foraging on inactive prey. 3. This interference competition led to differences in activity: redshanks attaining a lower foraging success had a higher walking rate. Greater activity was associated with wider flock spacing and shorter distances to cover, which has previously been shown to increase predation risk and mortality from sparrowhawks Accipiter nisus (L.). 4. We conclude that behavioural adaptations of prey species can lead to interference competition in foraging redshanks, and thus can affect their predation risk and mortality through increased activity. This study is one of the first to show how interference competition can be a mechanism for behaviourally mediated indirect effects, and provides further evidence for the suggestion that a single species occupying an intermediate trophic level may be simultaneously top-down controlled by a predator and bottom-up controlled by a behavioural response of its prey.     

Predator diversity and environmental change modify the strengths of trophic and nontrophic interactions

Understanding the dependence of species interaction strengths on environmental factors and species diversity is crucial to predict community dynamics and persistence in a rapidly changing world. Nontrophic (e.g. predator interference) and trophic components together determine species interaction strengths, but the effects of environmental factors on these two components remain largely unknown. This impedes our ability to fully understand the links between environmental drivers and species interactions. Here, we used a dynamical modelling framework based on measured predator functional responses to investigate the effects of predator diversity, prey density, and temperature on trophic and nontrophic interaction strengths within a freshwater food web. We found that (i) species interaction strengths cannot be predicted from trophic interactions alone, (ii) nontrophic interaction strengths vary strongly among predator assemblages, (iii) temperature has opposite effects on trophic and nontrophic interaction strengths, and (iv) trophic interaction strengths decrease with prey density, whereas the dependence of nontrophic interaction strengths on prey density is concave up. Interestingly, the qualitative impacts of temperature and prey density on the strengths of trophic and nontrophic interactions were independent of predator identity, suggesting a general pattern. Our results indicate that taking multiple environmental factors and the nonlinearity of density‐dependent species interactions into account is an important step towards a better understanding of the effects of environmental variations on complex ecological communities. The functional response approach used in this study opens new avenues for (i) the quantification of the relative importance of the trophic and nontrophic components in species interactions and (ii) a better understanding how environmental factors affect these interactions and the dynamics of ecological communities.     

The influence of the invasive black bullhead Ameiurus melas on the predatory efficiency of pike Esox lucius L.

The influence of the invasive black bullhead Ameiurus melas on the predatory efficiency of the pike Esox lucius was investigated using an additive experimental design. Pike predatory success on 0+ years roach Rutilus rutilus was significantly reduced in the presence of black bullhead. Among the different hypotheses that may explain such a pattern, the hypothesis of direct competition between pike and black bullhead was not verified, as black bullhead hardly fed on roach. Similarly, pike predatory efficiency did not decrease with turbidity, rejecting therefore the hypothesis of an indirect effect through black bullhead-generated turbidity. Therefore, the reduced predatory efficiency of pike was probably related to behavioural interference between pike and black bullhead. These laboratory results confirm the potential negative impact of black bullhead on native European fauna, with a particular emphasis on pike, which is a top predator considered as vulnerable in some European regions.     

Predation risk tradeoffs in prey: effects on energy and behaviour

The complexity of behavioural interactions in predator-prey systems has recently begun to capture trait-effects, or non-lethal effects, of predators on prey via induced behavioural changes. Non-lethal predation effects play crucial roles in shaping population and community dynamics, particularly by inducing changes to foraging, movement and reproductive behaviours of prey. Prey exhibit trade-offs in behaviours while minimizing predation risk. We use a novel evolutionary ecosystem simulation EcoSim to study such behavioural interactions and their effects on prey populations, thereby addressing the need for integrating multiple layers of complexity in behavioural ecology. EcoSim allows complex intra- and inter-specific interactions between behaviourally and genetically unique individuals called predators and prey, as well as complex predator-prey dynamics and coevolution in a tri-trophic and spatially heterogeneous world. We investigated the effects of predation risk on prey energy budgets and fitness. Results revealed that energy budgets, life history traits, allocation of energy to movements and fitness-related actions differed greatly between prey subjected to low-predation risk and high-predation risk. High-predation risk suppressed prey foraging activity, increased total movement and decreased reproduction relative to low-risk. We show that predation risk alone induces behavioural changes in prey which drastically affect population and community dynamics, and when interpreted within the evolutionary context of our simulation indicate that genetic changes accompanying coevolution have long-term effects on prey adaptability to the absence of predators.     

A shift from exploitation to interference competition with increasing density affects population and community dynamics

Intraspecific competition influences population and community dynamics and occurs via two mechanisms. Exploitative competition is an indirect effect that occurs through use of a shared resource and depends on resource availability. Interference competition occurs by obstructing access to a resource and may not depend on resource availability. Our study tested whether the strength of interference competition changes with protozoa population density. We grew experimental microcosms of protozoa and bacteria under different combinations of protozoan density and basal resource availability. We then solved a dynamic predator–prey model for parameters of the functional response using population growth rates measured in our experiment. As population density increased, competition shifted from exploitation to interference, and competition was less dependent on resource levels. Surprisingly, the effect of resources was weakest when competition was the most intense. We found that at low population densities, competition was largely exploitative and resource availability had a large effect on population growth rates, but the effect of resources was much weaker at high densities. This shift in competitive mechanism could have implications for interspecific competition, trophic interactions, community diversity, and natural selection. We also tested whether this shift in the mechanism of competition with protozoa density affected the structure of the bacterial prey community. We found that both resources and protozoa density affected the structure of the bacterial prey community, suggesting that competitive mechanism may also affect trophic interactions.     

No change in subordinate butterflyfish diets following removal of behaviourally dominant species

Direct interference interactions between species are often mediated by aggression and related to resource use. Interference interactions are frequently asymmetric, whereby one species wins the majority of interactions; however, the effect of this asymmetry on the diet of subordinate species has not received the same attention as the impact of interference on habitat use. Here we experimentally evaluated whether release from asymmetric interference led to increased use of a preferred dietary resource by subordinate species, using coral-feeding butterflyfishes as a model system. Following experimental removal of the behaviourally dominant species, we found no change in diet breadth or foraging on the preferred resource by subordinate species. Our results suggest that release from asymmetric interspecific interference does not necessarily result in changes to subordinate species’ diets, at least not over the course of our study. Rather, consistently asymmetric interactions may contribute to behavioural conditioning of subordinate species, meaning that even in the absence of dominants, subordinate individuals maintain established feeding patterns. Additionally, our results suggest that antagonistic interactions between butterflyfishes may have contributed to niche partitioning and conservatism over evolutionary time scales.

     

Differences in prey personality mediate trophic cascades

Functional trait approaches in ecology chiefly assume the mean trait value of a population adequately predicts the outcome of species interactions. Yet this assumption ignores substantial trait variation among individuals within a population, which can have a profound effect on community structure and function. We explored individual trait variation through the lens of animal personality to test whether among‐individual variation in prey behavior mediates trophic interactions. We quantified the structure of personalities within a population of generalist grasshoppers and examined, through a number of field and laboratory‐based experiments, how personality types could impact tri‐trophic interactions in a food chain. Unlike other studies of this nature, we used spatial habitat domains to evaluate how personality types mechanistically map to behaviors relevant in predator–prey dynamics and found shy and bold individuals differed in both their habitat use and foraging strategy under predation risk by a sit‐and‐wait spider predator. In the field‐based mesocosm portion of our study, we found experimental populations of personality types differed in their trophic impact, demonstrating that prey personality can mediate trophic cascades. We found no differences in respiration rates or body size between personality types used in the mesocosm experiment, indicating relative differences in trophic impact were not due to variation in prey physiology but rather variation in behavioral strategies. Our work demonstrates how embracing the complexity of individual trait variation can offer mechanistically richer understanding of the processes underlying trophic interactions.     

Behavioural syndrome in a solitary predator is independent of body size and growth rate

Models explaining behavioural syndromes often focus on state-dependency, linking behavioural variation to individual differences in other phenotypic features. Empirical studies are, however, rare. Here, we tested for a size and growth-dependent stable behavioural syndrome in the juvenile-stages of a solitary apex predator (pike, Esox lucius), shown as repeatable foraging behaviour across risk. Pike swimming activity, latency to prey attack, number of successful and unsuccessful prey attacks was measured during the presence/absence of visual contact with a competitor or predator. Foraging behaviour across risks was considered an appropriate indicator of boldness in this solitary predator where a trade-off between foraging behaviour and threat avoidance has been reported. Support was found for a behavioural syndrome, where the rank order differences in the foraging behaviour between individuals were maintained across time and risk situation. However, individual behaviour was independent of body size and growth in conditions of high food availability, showing no evidence to support the state-dependent personality hypothesis. The importance of a combination of spatial and temporal environmental variation for generating growth differences is highlighted.     

Frequency-dependent community dynamics driven by sexual interactions

Research in community ecology has tended to focus on trophic interactions (e.g., predation, resource competition) as driving forces of community dynamics, and sexual interactions have often been overlooked. Here we discuss how sexual interactions can affect community dynamics, especially focusing on frequency-dependent dynamics of horizontal communities (i.e., communities of competing species in a single ecological guild). By combining mechanistic and phenomenological models of competition, we place sexual reproduction into the framework of modern coexistence theory. First, we review how population dynamics of two species competing for two resources can be represented by the Lotka–Volterra competition model as well as frequency dynamics, and how niche differentiation and overlap produce negative and positive frequency-dependence (i.e., stable coexistence and priority effect), respectively. Then, we explore two situations where sexual interactions change the frequency-dependence in community dynamics: (1) reproductive interference, that is, negative interspecific interactions due to incomplete species recognition in mating trials, can promote positive frequency-dependence and (2) density-dependent intraspecific adaptation load, that is, reduced population growth rates due to adaptation to intraspecific sexual (or social) interactions, produces negative frequency-dependence. We show how reproductive interference and density-dependent intraspecific adaptation load can decrease and increase niche differences in the framework of modern coexistence theory, respectively. Finally, we discuss future empirical and theoretical approaches for studying how sexual interactions and related phenomena (e.g., reproductive interference, intraspecific adaptation load, and sexual dimorphism) driven by sexual selection and conflict can affect community dynamics.     

Behavioral interference and facilitation in the foraging cycle shape the functional response

Individual forager behaviors should affect per capita intakerates and thereby population and consumer-resource properties.We consider and incorporate conspecific facilitation and interferenceduring the separate foraging-cycle stages in a functional responsemodel that links individual behavioral interactions with consumer-resourceprocesses. Our analyses suggest that failing to properly considerand include all effects of behavioral interactions on foraging-cyclestage performances may either over- or underestimate effectsof interactions on the shape of both functional responses andpredator zero-growth isoclines. Incorporation of prey- and predator-dependentinteractions among foragers in the model produces predator isoclineswith potentials for highly complex consumer-resource dynamics.Facilitation and interference during the foraging cycle aretherefore suggested as potent behavioral mechanisms to causepatterns of community dynamics. We emphasize that correct estimationsof interaction-mediated foraging-cycle efficiencies should beconsidered in empirical and theoretical attempts to furtherour understanding of the mechanistic link between social behaviorsand higher order processes.     

Interspecific behavioural interference and range dynamics: current insights and future directions

Novel biotic interactions in shifting communities play a key role in determining the ability of species' ranges to track suitable habitat. To date, the impact of biotic interactions on range dynamics have predominantly been studied in the context of interactions between different trophic levels or, to a lesser extent, exploitative competition between species of the same trophic level. Yet, both theory and a growing number of empirical studies show that interspecific behavioural interference, such as interspecific territorial and mating interactions, can slow down range expansions, preclude coexistence, or drive local extinction, even in the absence of resource competition. We conducted a systematic review of the current empirical research into the consequences of interspecific behavioural interference on range dynamics. Our findings demonstrate there is abundant evidence that behavioural interference by one species can impact the spatial distribution of another. Furthermore, we identify several gaps where more empirical work is needed to test predictions from theory robustly. Finally, we outline several avenues for future research, providing suggestions for how interspecific behavioural interference could be incorporated into existing scientific frameworks for understanding how biotic interactions influence range expansions, such as species distribution models, to build a stronger understanding of the potential consequences of behavioural interference on the outcome of future range dynamics.     

What do the empty stomachs of northern pike (<Emphasis Type="Italic">Esox lucius</Emphasis>) reveal? Insights from carbon (δ<Superscript>13</Superscript>C) and nitrogen (δ<Superscript>15</Superscript>N) stable isotopes

The frequency of individuals with empty stomachs (FES) can vary greatly among northern pike populations. However, the FES has only seldom been analyzed in this species and its meaning is still not fully understood. It has been suggested that a high FES may reflect a strongly piscivorous behaviour while low FES could reflect a higher utilization of invertebrates. We compared the stomach contents and the trophic position of northern pike in 16 populations of individuals feeding mainly on fish or benthic invertebrates. We tested the hypothesis that northern pike with empty stomachs or with fish in their stomachs have a higher trophic position than individuals feeding on invertebrates. Carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotope signatures were used to estimate the trophic position of individuals. We found no significant difference in the trophic position among piscivores, invertebrate feeders, and northern pike with empty stomachs. The average trophic position of northern pike was high (mean ± SD = 4.3 ± 0.4, n = 66) and was correlated with total length. These results indicate that, although invertebrates could be an important part of the diet of northern pike in Canadian Shield lakes, fish are still the dominant prey. Hence, feeding on invertebrates in our study lakes would reflect an opportunistic rather than a specialized feeding strategy.     

Piscivore efficiency and refuging prey: the importance of predator search mode

In predator-prey interactions, the efficiency of the predator is dependent on characteristics of both the predator and the prey, as well as the structure of the environment. In a field enclosure experiment, we tested the effects of a prey refuge on predator search mode, predator efficiency and prey behaviour. Replicated enclosures containing young of the year (0+) and 1-year-old (1+) perch were stocked with 3 differentially sized individuals of either of 2 piscivorous species, perch (Perca fluviatilis), pike (Esox lucius) or no piscivorous predators. Each enclosure contained an open predator area with three small vegetation patches, and a vegetated absolute refuge for the prey. We quantified the behaviour of the predators and the prey simultaneously, and at the end of the experiment the growth of the predators and the mortality and habitat use of the prey were estimated. The activity mode of both predator species was stationary. Perch stayed in pairs in the vegetation patches whereas pike remained solitary and occupied the corners of the enclosure. The largest pike individuals stayed closest to the prey refuge whereas the smallest individuals stayed farthest away from the prey refuge, indicating size-dependent interference among pike. Both size classes of prey showed stronger behavioural responses to pike than to perch with respect to refuge use, distance from refuge and distance to the nearest predator. Prey mortality was higher in the presence of pike than in the presence of perch. Predators decreased in body mass in all treatments, and perch showed a relatively stronger decrease in body mass than pike during the experiment. Growth differences of perch and pike, and mortality differences of prey caused by predation, can be explained by predator morphology, predator attack efficiency and social versus interference behaviour of the predators. These considerations suggest that pike are more efficient piscivores around prey refuges such as the littoral zones of lakes, whereas perch have previously been observed to be more efficient in open areas, such as in the pelagic zones of lakes.     

Effects of social group size on information transfer and task allocation

Summary Social animals exchange information during social interaction. The rate of interaction and, hence, the rate of information exchange, typically changes with density and density may be affected by the size of the social group. We investigate models in which each individual may be engaged in one of several tasks. For example, the different tasks could represent alternative foraging locations exploited by an ant colony. An individual's decision about which task to pursue depends both on environmental stimuli and on interactions among individuals. We examine how group size affects the allocation of individuals among the various tasks. Analysis of the models shows the following. (1) Simple interactions among individuals with limited ability to process information can lead to group behaviour that closely approximates the predictions of evolutionary optimality models, (2) Because per capita rates of social interaction may increase with group size, larger groups may be more efficient than smaller ones at tracking a changing environment, (3) Group behaviour is determined both by each individual's interaction with environmental stimuli and by social exchange of information. To keep these processes in balance across a range of group sizes, organisms are predicted to regulate per capita rates of social interaction and (4) Stochastic models show, at least in some cases, that the results described here occur even in small groups of approximately ten individuals.     

Using behavioural and state variables to identify proximate causes of population change in a seabird

Changes in animal population size are driven by the interactions between intrinsic processes and extrinsic forces, and identifying the proximate mechanisms behind population change remains a fundamental question in ecology. Here we report on how measuring behavioural and state proxies of food availability among populations experiencing different growth rates can be used to rapidly identify proximate drivers of population trends. In recent decades, the Cape gannet Morus capensis has shown a major distributional shift with historically large colonies in Namibia decreasing rapidly, whilst numbers at South African colonies have increased, suggesting contrasting environmental conditions in the two regions. We compared per capita growth rates of five of the six extant colonies with foraging range (using miniaturised Global Positioning System loggers), foraging work rate, food delivery rates and body condition of breeding adults. We found significant associations between the rate of population change, individual behaviour, energetic gain and body condition that indicate that recent population changes are associated with extrinsic effects. This study shows that behavioural and state data can be used to identify important drivers of population change, and their cost-effectiveness ensures that they are an appealing option for measuring the health of animal populations in numerous situations.     

Glacial clay affects foraging performance in a Patagonian fish and cladoceran

Climate change is altering temperatures and precipitation patterns all over the world. In Patagonia, Argentina, predicted increase in precipitation together with rapidly melting glaciers increase the surface runoff, and thereby the transport of suspended solids to recipient lakes. Suspended solids affect the visual conditions in the water which in turn restricts visual foraging. The native fish Aplochiton zebra Jenyns, and its filter-feeding cladoceran prey, Daphnia commutata Ekman, were subjected to foraging experiments at three turbidity levels. A. zebra foraging rate was substantially reduced at naturally occurring turbidity levels and the filtering rate of D. commutata was reduced at the highest turbidity level. This indicates that Daphnia may be partly released from predation from A. zebra at the same time as it can maintain relatively high feeding rates as turbidity increases. Lower foraging rates at the same time as the metabolic demand increases, through increased temperatures, may result in larger effects on A. zebra than could be expected from increases in turbidity or temperature alone. Turbidity may, as an indirect effect of climate change, decrease planktivore foraging rates and thereby alter the interaction strength between trophic levels.     

互利关系和植物多样性对节肢动物群落不同营养级的影响路径和强度

食物网中的上行效应和下行效应对于群落的动态和生态系统功能有十分重要的影响,旨在探讨互利关系和植物多样性对节肢动物群落中食物网不同营养级之间的影响。通过随机裂区试验方法,分别设置了3种蚂蚁-紫胶虫互利关系处理(有互利关系、无互利关系和自然对照)以及3种植物多样性处理(单一种植、2树种混植和3树种混植),于2016年8月和9月分两次用手捡法、网扫法和震落法采集试验地寄主植物上所有的节肢动物,并按照不同营养级将其分类。利用结构方程模型分析方法对不同营养级之间的相互作用的路径和强度进行了比较,结果显示:1)互利关系对捕食者和消费者均有显著的下行作用,有互利关系处理下蚂蚁对捕食者的路径强度要强于自然对照组,互利关系对捕食者的影响要强于对消费者的影响。2)植物多样性会通过影响植物的生物量而对消费者和捕食者产生显著的上行效应影响,这种影响会随着营养级的升高而显著减小。3)消费者主要受植物多样性的上行效应影响,而捕食者主要受互利关系的下行效应影响。有互利关系的食物网结构更加复杂,营养级之间的相互作用更为显著。探讨了以蚂蚁-紫胶虫互利关系为核心作用的紫胶林生态系统中互利关系和植物多样性对节肢动物食物网中各营养级的影响,揭示了上行效应和下行效应对各营养级的作用途径和强度,其结果有一定的理论参考价值。     

Effects of brown and turbid water on piscivore–prey fish interactions along a visibility gradient

1. Environmental changes such as eutrophication and increasing inputs of humic matter (brownification) may have strong effects on predator–prey interactions in lakes through a reduction in the visual conditions affecting foraging behaviour of visually oriented predators. 2. In this experiment, we studied the effects of visual range (25–200 cm) in combination with optically deteriorating treatments (algae, clay or brown humic water) on predator–prey interactions between pike (Esox lucius) and roach (Rutilus rutilus). We measured effects on reaction distance and strike distance for pike and escape distance for roach, when pike individuals were exposed to free‐swimming roach as well as to roach held in a glass cylinder. 3. We found that reaction distance decreased with decreasing visual range caused by increasing levels of algae, clay or humic matter. The effect of reaction distance was stronger in turbid water (clay, algae) than in the brown water treatment. 4. Strike distance was neither affected by visual range nor by optical treatment, but we found shorter strike distances when pike attacked roach using visual cues only (roach held in a cylinder) compared to when pike could use multiple senses (free‐swimming roach). Escape distance for roach was longer in turbid than in brown water treatments. 5. Changes in environmental drivers, such as eutrophication and brownification, affecting the optical climate should thus have consequences for the strength of predator–prey interactions through changes in piscivore foraging efficiency and prey escape behaviour. This in turn may affect lake ecosystems through higher‐order interactions.     

Feeding and Refuge Use by Small Fish in the Presence of Cyanobacteria Blooms

We studied the effect of cyanobacteria on foraging and refuge use in small fish. We measured pike larval feeding in the presence of cyanobacteria by counting leftover prey. Our results showed that feeding by pike larvae on zooplankton prey decreased significantly in the presence of non-toxic cyanobacteria. The behaviour can be due to lowered vision caused by turbidity or clogging of the gills. Further, we tested whether the three-spined stickleback use toxic cyanobacteria as a refuge against predators in a choice experiment. The choice experiment was performed in a Y-maze fluviarum, where the fish could select between two different environments. Our results support the refuge use hypothesis because the three-spined stickleback clearly preferred toxic cyanobacteria to the chemical predator signal. To conclude, cyanobacteria decrease feeding rates in fish larvae, but may function as important refuge for e.g. sticklebacks, during predation pressure in pelagic algal blooms.