Predator Traits Research Articles

Natural enemy diversity and biological control: Making sense of the context-dependency

Numerous studies have demonstrated that diverse predator assemblages can be more effective at controlling prey populations. Yet, other studies have shown no effect of predator diversity on prey mortality, or even negative effects (for example due to intraguild predation or interference). Much research emphasis has been placed on the traits of predators that maximise functional complementarity. However, comparatively less attention has been paid to the traits of the prey or habitat that may maximise predator diversity effects, even though there must be a variety of prey niches available to be partitioned in order for niche complementarity to occur. Following this logic, we review six hypotheses for when diverse enemy assemblages should be most effective: when 1) prey communities are diverse; 2) prey have complex life cycles; 3) prey are patchily distributed in space or time; 4) studies are conducted at larger spatial and temporal scales; 5) plant structures are complex; 6) prey are abundant. Many of these hypotheses lack direct tests, particularly in agricultural systems, but we find little or no direct or indirect support for hypotheses 1, 4, 5 and 6. However, previous work does provide some support for hypotheses 2 and 3. We discuss methods to test these hypotheses directly, and suggest that natural enemy diversity may only benefit the biological control of arthropods in heterogeneous systems.

Evolution towards oscillation or stability in a predator–prey system

We studied a prey-predator system in which both species evolve. We discuss here the conditions that result in coevolution towards a stable equilibrium or towards oscillations. First, we show that a stable equilibrium or population oscillations with small amplitude is likely to occur if the prey's (host's) defence is effective when compared with the predator's (parasite's) attacking ability at equilibrium, whereas large-amplitude oscillations are likely if the predator's (parasite's) attacking ability exceeds the prey's (host's) defensive ability. Second, a stable equilibrium is more likely if the prey's defensive trait evolves faster than the predator's attack trait, whereas population oscillations are likely if the predator's trait evolves faster than that of the prey. Third, when the adaptation rates of both species are similar, the amplitude of the fluctuations in their abundances is small when the adaptation rate is either very slow or very fast, but at an intermediate rate of adaptation the fluctuations have a large amplitude. We also show the case in which the prey's abundance and trait fluctuate greatly, while those of the predator remain almost unchanged. Our results predict that populations and traits in host-parasite systems are more likely than those in prey-predator systems to show large-amplitude oscillations.

Evolution in predator–prey systems

We study the adaptive dynamics of predator–prey systems modeled by a dynamical system in which the traits of predators and prey are allowed to evolve by small mutations. When only the prey are allowed to evolve, and the size of the mutational change tends to 0, the system does not exhibit long term prey coexistence and the trait of the resident prey type converges to the solution of an ODE. When only the predators are allowed to evolve, coexistence of predators occurs. In this case, depending on the parameters being varied, we see that (i) the number of coexisting predators remains tight and the differences in traits from a reference species converge in distribution to a limit, or (ii) the number of coexisting predators tends to infinity, and we calculate the asymptotic rate at which the traits of the least and most “fit” predators in the population increase. This last result is obtained by comparison with a branching random walk killed to the left of a linear boundary and a finite branching–selection particle system.

Inducible defenses in prey intensify predator cannibalism

Trophic cascades are often a potent force in ecological communities, but abiotic and biotic heterogeneity can diffuse their influence. For example, inducible defenses in many species create variation in prey edibility, and size-structured interactions, such as cannibalism, can shift predator diets away from heterospecific prey. Although both factors diffuse cascade strength by adding heterogeneity to trophic interactions, the consequences of their interactioh remain poorly understood. We show that inducible defenses in tadpole prey greatly intensify cannibalism in predatory larval salamanders. The likelihood of cannibalism was also strongly influenced by asymmetries in salamander size that appear to be most important in the presence of defended prey. Hence, variation in prey edibility and the size structure of the predator may synergistically affect predator-prey population dynamics by reducing prey mortality and increasing predator mortality via cannibalism. We also suggest that the indirect effects of prey defenses may shape the evolution of predator traits that determine diet breadth and how trophic dynamics unfold in natural systems.

Species Invasion History Influences Community Evolution in a Tri-Trophic Food Web Model

BackgroundRecent experimental studies have demonstrated the importance of invasion history for evolutionary formation of community. However, only few theoretical studies on community evolution have focused on such views.Methodology and Principal FindingsWe used a tri-trophic food web model to analyze the coevolutionary effects of ecological invasions by a mutant and by a predator and/or resource species of a native consumer species community and found that ecological invasions can lead to various evolutionary histories. The invasion of a predator makes multiple evolutionary community histories possible, and the evolutionary history followed can determine both the invasion success of the predator into the native community and the fate of the community. A slight difference in the timing of an ecological invasion can lead to a greatly different fate. In addition, even greatly different community histories can converge as a result of environmental changes such as a predator trait shift or a productivity change. Furthermore, the changes to the evolutionary history may be irreversible.Conclusions and SignificanceOur modeling results suggest that the timing of ecological invasion of a species into a focal community can largely change the evolutionary consequences of the community. Our approach based on adaptive dynamics will be a useful tool to understand the effect of invasion history on evolutionary formation of community.

The positive effects of negative interactions: Can avoidance of competitors or predators increase resource sampling by prey?

Spatial overlap between predators and prey is key to predicting their interaction strength and population dynamics. We constructed a spatially-explicit simulation model to explore how predator and prey behavioral traits and patterns of resource distribution influence spatial overlap between predators, prey, and prey resources. Predator and prey spatial association primarily followed the ideal free distribution. Departures from this model were intriguing, especially from the interactions of predator and prey behavior. When prey weakly avoided conspecifics, they associated more highly with resources when predators were present. Predators increased the rate of prey movement between patches, which increased their ability to sample their environment and aggregate in patches with high resources. When prey strongly avoided each other, predators decreased prey association with resources. That is, an increased rate of prey movement increased the probability that prey would interact and avoid each other without regard to the distribution of resources. More generally, a more highly clumped distribution of resources acted as a spatial anchor that generally increased prey, predator, and resource association. Prey tended to congregate with resources and predators generally congregated with prey.

Experimental evidence that phenotypic divergence in predators drives community divergence in prey

Studies of adaptive divergence have traditionally focused on the ecological causes of trait diversification, while the ecological consequences of phenotypic divergence remain relatively unexplored. Divergence in predator foraging traits, in particular, has the potential to impact the structure and dynamics of ecological communities. To examine the effects of predator trait divergence on prey communities, we exposed zooplankton communities in lake mesocosms to predation from either anadromous or landlocked (freshwater resident) alewives, which have undergone recent and rapid phenotypic differentiation in foraging traits (gape width, gill raker spacing, and prey size-selectivity). Anadromous alewives, which exploit large prey items, significantly reduced the mean body size, total biomass, species richness, and diversity of crustacean zooplankton relative to landlocked alewives, which exploit smaller prey. The zooplankton responses observed in this experiment are consistent with patterns observed in lakes. This study provides direct evidence that phenotypic divergence in predators, even in its early stages, can play a critical role in determining prey community structure.

TRAIT‐MEDIATED EFFECTS ON FLOWERS: ARTIFICIAL SPIDERS DECEIVE POLLINATORS AND DECREASE PLANT FITNESS

Although predators can affect foraging behaviors of floral visitors, rarely is it known if these top-down effects of predators may cascade to plant fitness through trait-mediated interactions. In this study we manipulated artificial crab spiders on flowers of Rubus rosifolius to test the effects of predation risk on flower-visiting insects and strength of trait-mediated indirect effects to plant fitness. In addition, we tested which predator traits (e.g., forelimbs, abdomen) are recognized and avoided by pollinators. Total visitation rate was higher for control flowers than for flowers with an artificial crab spider. In addition, flowers with a sphere (simulating a spider abdomen) were more frequently visited than those with forelimbs or the entire spider model. Furthermore, the presence of artificial spiders decreased individual seed set by 42% and fruit biomass by 50%. Our findings indicate that pollinators, mostly bees, recognize and avoid flowers with predation risk; forelimbs seem to be the predator trait recognized and avoided by hymenopterans. Additionally, predator avoidance by pollinators resulted in pollen limitation, thereby affecting some components of plant fitness (fruit biomass and seed number). Because most pollinator species that recognized predation risk visited many other plant species, trait-mediated indirect effects of spiders cascading down to plant fitness may be a common phenomenon in the Atlantic rainforest ecosystem.

Phenotypic Mismatches Reveal Escape from Arms-Race Coevolution

Because coevolution takes place across a broad scale of time and space, it is virtually impossible to understand its dynamics and trajectories by studying a single pair of interacting populations at one time. Comparing populations across a range of an interaction, especially for long-lived species, can provide insight into these features of coevolution by sampling across a diverse set of conditions and histories. We used measures of prey traits (tetrodotoxin toxicity in newts) and predator traits (tetrodotoxin resistance of snakes) to assess the degree of phenotypic mismatch across the range of their coevolutionary interaction. Geographic patterns of phenotypic exaggeration were similar in prey and predators, with most phenotypically elevated localities occurring along the central Oregon coast and central California. Contrary to expectations, however, these areas of elevated traits did not coincide with the most intense coevolutionary selection. Measures of functional trait mismatch revealed that over one-third of sampled localities were so mismatched that reciprocal selection could not occur given current trait distributions. Estimates of current locality-specific interaction selection gradients confirmed this interpretation. In every case of mismatch, predators were “ahead” of prey in the arms race; the converse escape of prey was never observed. The emergent pattern suggests a dynamic in which interacting species experience reciprocal selection that drives arms-race escalation of both prey and predator phenotypes at a subset of localities across the interaction. This coadaptation proceeds until the evolution of extreme phenotypes by predators, through genes of large effect, allows snakes to, at least temporarily, escape the arms race.

PREDATOR DIVERSITY AND IDENTITY DRIVE INTERACTION STRENGTH AND TROPHIC CASCADES IN A FOOD WEB

Declining predator diversity may drastically affect the biomass and productivity of herbivores and plants. Understanding how changes in predator diversity can propagate through food webs to alter ecosystem function is one of the most challenging ecological research topics today. We studied the effects of predator removal in a simple natural food web in the Sierra Nevada mountains of California (USA). By excluding the predators of the third trophic level of a food web in a full-factorial design, we monitored cascading effects of varying predator diversity and composition on the herbivorous beetle Chrysomela aeneicollis and the willow Salix orestera, which compose the first and second trophic levels of the food web. Decreasing predator diversity increased herbivore biomass and survivorship, and consequently increased the amount of plant biomass consumed via a trophic cascade. Despite this simple linear mean effect of diversity on the strength of the trophic cascade, we found additivity, compensation, and interference in the effects of multiple predators on herbivores and plants. Herbivore survivorship and predator-prey interaction strengths varied with predator diversity, predator identity, and the identity of coexisting predators. Additive effects of predators on herbivores and plants may have been driven by temporal niche separation, whereas compensatory effects and interference occurred among predators with a similar phenology. Together, these results suggest that while the general trends of diversity effects may appear linear and additive, other information about species identity was required to predict the effects of removing individual predators. In a community that is not temporally well-mixed, predator traits such as phenology may help predict impacts of species loss on other species. Information about predator natural history and food web structure may help explain variation in predator diversity effects on trophic cascades and ecosystem function.

Fear in animals: a meta-analysis and review of risk assessment

The amount of risk animals perceive in a given circumstance (i.e. their degree of 'fear') is a difficult motivational state to study. While many studies have used flight initiation distance as a proxy for fearfulness and examined the factors influencing the decision to flee, there is no general understanding of the relative importance of these factors. By identifying factors with large effect sizes, we can determine whether anti-predator strategies reduce fear, and we gain a unique perspective on the coevolution of predator and anti-predator behaviour. Based on an extensive review and formal meta-analysis, we found that predator traits that were associated with greater risk (speed, size, directness of approach), increased prey distance to refuge and experience with predators consistently amplified the perception of risk (in terms of flight initiation distance). While fish tolerated closer approach when in larger schools, other taxa had greater flight initiation distances when in larger groups. The presence of armoured and cryptic morphologies decreased perception of risk, but body temperature in lizards had no robust effect on flight initiation distance. We find that selection generally acts on prey to be sensitive to predator behaviour, as well as on prey to modify their behaviour and morphology.

Bifurcation Analysis of a Prey-Predator Coevolution Model

We show in this paper how numerical bifurcation analysis can be used to study the evolution of genetically transmitted phenotypic traits. For this, we consider the standard Rosenzweig--MacArthur prey-predator model [The American Naturalist, 97 (1963), pp. 209--223] and, following the so-called adaptive dynamics approach, we derive from it a second-order evolutionary model composed of two ODEs, one for the prey trait and one for the predator trait. Then, we perform a detailed bifurcation analysis of the evolutionary model with respect to various environmental and demographic parameters. Surprisingly, the evolutionary dynamics turn out to be much richer than the population dynamics. Up to three evolutionary attractors can be present, and the bifurcation diagrams contain numerous global bifurcations and codimension-2 bifurcation points. Interesting biological properties can be extracted from these bifurcation diagrams. In particular, one can conclude that evolution of the traits can be cyclic and easily promote prey species diversity.

Spatial Aggregation of Apple Mites (Acari: Phytoseiidae, Stigmaeidae, Tetranychidae) as Measured by a Binomial Model: Effects of Life Stage, Reproduction, Competition, and Predation

A binomial model was used to describe aggregation for 8 mite species that were collected from an experimental apple orchard in 1990–1995. They included the plant-feeding spider mites Tetranychus urticae Koch (combined with Eotetranychus sp.), Panonychus ulmi (Koch), and Bnyobia rubrioculus (Scheuten); the stigmaeid predator Zetzellia mali (Ewing); and the phytoseiid predators Amblyseius andersoni Chant, Metaseiulus occidentalis (Nesbitt), and Typhlodromus pyri Scheuten. Aggregation was compared among all species, among life stages, and for each species as its density changed yearly. We found that predators were less aggregated than spider mites, and older life stages were less aggregated than younger ones. Tetranychus urticae + Eotetranychus sp., P. ulmi , and Z. mali were more clumped when their densities were low. Aggregation of T. pyri was related to the aggregation and densities of P. ulmi and Z. mali . Explanations for observed spatial patterns are suggested based on movement, reproduction, competition, predation, and behavioral traits of each species.

The Evolution of Coloniality in Birds in Relation to Food, Habitat, Predation, and Life-History Traits: A Comparative Analysis

The Evolution of Coloniality in Birds in Relation to Food, Habitat, Predation, and Life-History Traits: A Comparative Analysis

Evolutionary responses of foraging-related traits in unstable predator–prey systems

The evolutionary responses of predators to prey and of prey to predators are analysed using models for the dynamics of a quantitative trait that determines the capture rate of prey by an average searching predator. Unlike previous investigations, the analysis centres on models and/or parameter values for which the two-species equilibrium is locally unstable. The instability in some models is driven by the predator's non-linear functional response to prey; in other models, the cycles are a direct consequence of evolutionary response to selection acting on the trait. When the values of predator and prey traits combine multiplicatively to determine the capture rate, the predator's trait shows only a transient response to changes in the prey's trait in stable systems. However, when the population densities exhibit sustained oscillations, predators often evolve an increased long-term mean capture rate in response to an increased prey escape ability. Under the multiplicative model, prey in stable systems always evolve increased escape ability in response to an increased predator capture a

Seed predation, pathogen infection and life-history traits in Brassica rapa.

Herbivory and disease can shape the evolution of plant populations, but their joint effects are rarely investigated. Families of plants of Brassica rapa (Brassicaceae) were grown from seeds collected in two naturalized populations in an experimental garden. We examined leaf infection by the fungus Alternaria, seed predation by a gall midge (Cecidomyiidae) and plant life-history traits. Plants from one population had heavier seeds, were more likely to flower, had less fungal infection, had more seed predation and were more fecund. Fungal infection score and seed predation rate increased with plant size, but large plants still had the greatest number of undamaged fruits. Spatial heterogeneity in the experimental garden was significant; seed predation rate and fecundity varied among blocks. An apparent tradeoff existed between susceptibility to disease and seed predation: plants with the highest fungal infection score had the lowest seed predation rate. Alternaria infection varied between populations, but the disease had no effect on fecundity. Seed predation did reduce fecundity. Damaged fruits had 31.4% fewer intact seeds. However, evidence for additive genetic variation in resistance to seed predation was weak. Therefore, neither disease nor seed predation was likely to be a strong agent of genetically based fecundity selection.

The influence of plant architecture on the foraging efficiencies of a suite of ladybird beetles feeding on aphids.

By manipulating plant variety and predator species, we investigated the interactions of plant and predator traits in determining predation effectiveness. The predators were all coccinellid adults (Hippodamia convergens, Hippodamia variegata, Coccinella apunctata, and Coccinella septempunctata) and the prey were cabbage aphids (Brevicoryne brassicae). Foraging behavior of the four predators was observed on four crucifers that differed widely in their structures and surface textures (Brassica oleracea caulorapa, Brassica campestris, Brassica juncea crispifolia, and Hirschfeldia incana). Predation rates were significantly influenced by plant variety, a result we attribute to direct effects of plant morphology on predator mobility, falling frequency, and prey accessibility. Predation rates did not vary significantly among the ladybirds, although the four species did exhibit distinct foraging strategies as measured by time spent actively foraging, the rate of encountering aphids, and the fraction of aphids encountered that were consumed. The coccinellids also differed in their propensity for flying away from the plant, and in the frequency with which they fell from the plant. We did not detect any significant interaction effects between plant and predator species, suggesting that the main effects of plant and predator species may overwhelm their interactions in this kind of system. Our results suggest that the level of predation upon herbivorous insects may depend more upon plant architecture than on the particular species of natural enemies present.

Trophic Linkage between Stream Centrarchids and Their Crayfish Prey

Energetic links between smallmouth bass (Micropterus dolomieu) and rock bass (Ambloplites rupestris) and their crayfish foods were examined in an Ozark stream. A trophic level energy budget was developed by enumerating food habits for different age (size) fish, estimating annual production for both fish and crayfish, and using laboratory- and literature-derived bioenergetic and gross efficiency data. Both fishes began life feeding on small invertebrates (mayflies and chironomids) but within 3 mo switched to a diet of mainly crayfish and Cyprinidae. Total annual production of smallmouth bass was 0.262 g dry weight∙m−2∙yr−1 (6344 J) and rock bass 0.148 g∙m−2∙yr−1 (3607 J). Total annual production of crayfish was 4.15 g dry weight∙m−2∙yr−1 (55 736 J) for Orconectes luteus and 5.05 g∙m−2∙yr−1 (62 394 J) for O. punctimanus. Only about half of the crayfish production was available to fish, due to size-selective predation and behavioral traits of the prey. A predator–prey model suggested that nearly one third of total crayfish production during their vulnerable period was lost to centrarchids, and that half of the existing biomass was consumed. Fish are probably the major cause of mortality in crayfish and undoubtedly influence crayfish population dynamics and energy flow through the river system.

The evolution of rates of successful and unsuccessful predation

The question, how will evolutionary change in a predator or in its prey change the ratio of the rate of successful captures to the rate of unsuccessful capture attempts is addressed. I argue that this ratio is not a good index of the predator's adaptation to prey capture, because decreased costs of capture attempts or increased assimilation efficiency (both favored by natural selection in the predator) will usually reduce the ratio. In addition, the evolution of increased ability to capture prey may lead to a reduction in the success/failure ratio. Analysis of several simple models suggests that this result is robust. The presence of unsuccessful predation does have an important influence on the evolution of predator traits that increase its rate of encounter with the prey; the presence of unsuccessful predation may cause the predator to increase its adaptations for prey detection in response to an increase in the prey's ability to avoid detection.