Correlation between Olfactory Responses, Dispersal Tendencies, and Life-history Traits of the Predatory Mite Neoseiulus Womersleyi (Acari: Phytoseiidae) of Eight Local Populations

To investigate the relationship between foraging behavior and life-history traits of the predatory mite Neoseiulus womersleyi, the olfactory responses, dispersal ratios from a prey patch, predation rates, fecundity, and developmental times in eight local populations of N. womersleyi were investigated. Significant differences among local populations were found in all these traits except fecundity. None of the life-history traits correlated with foraging behavior. A significant positive correlation was found only between the olfactory response and the dispersal ratio. These results suggested that predatory mites with low olfactory responses would stay in a prey patch longer than predatory mites with high olfactory responses.     

Genetic variation in foraging traits among inbred lines of a predatory mite

Response of predators to herbivore-induced plant volatiles can affect the length of time a predator spends in a prey patch and the probability of a predator finding a new prey patch. Variation in response to herbivore-induced plant volatiles may lead to different foraging decisions among individuals, thereby affecting both within-patch dynamics and between-patch dispersal. We found significant phenotypic and additive genetic variation in two behavioral assays of response to herbivore-induced plant volatiles among inbred isofemale lines of the predatory mite, Phytoseiulus persimilis. In wind-tunnel tests to measure patch residence time, adult female predators from certain lines left prey patches sooner than others when a distant source of herbivore-induced plant volatiles was presented; whereas such variation disappeared when no distant volatiles were presented. In a measure of patch location, certain lines were more likely than others to locate a prey-infested leaf disc; again there was no difference when uninfested leaf discs were used. Patch location was negatively correlated with patch residence. That is, lines that were more likely to leave a prey patch in the presence of distant volatiles were also more likely to find an odor source (ie, prey patch) from a distance of 20 cm. These two foraging-related behaviors are heritable. A continuous distribution of both behaviors indicated that several to many loci may be responsible for these behavioral traits. Our line-crossing experiments suggested that maternal influence could be excluded. Substantial phenotypic variation in two other foraging-related traits, consumption and oviposition, were also detected among inbred lines. Consumption and oviposition were positively correlated; however, the relationship (slope) varied among inbred lines, suggesting that predatory mites vary in food conversion efficiency. A relationship was detected between patch residence and consumption. Patch location, as one important foraging trait, appeared to be negatively related to consumption, suggesting a trade-off between searching for patches and reproduction.     

Response of a phytoseiid predator to herbivore-Induced plant volatiles: Selection on attraction and effect on prey exploitation

Bean plants infested with herbivorous spider mites emit volatile chemicals that are attractive toP. persimilis, a predator of spider mites. In Y-tube olfactometer tests we evaluated involvement of a genetic component in predator response to herbivore-induced plant volatiles. Replicated bidirectional selection resulted in a significant increase in attraction after one generation of selection, but no decrease even after three generations of selection, indicating significant, but unbalanced, additive genetic variation in predator perception of, or response to, herbivore-induced plant volatiles. Selected lines responded differently than an unselected population to food deprivation, pointing to an interaction between their internal state and response to plant volatiles. Selected lines also differed from unselected ones in behaviors associated with local prey exploitation, such as residence time, prey consumption, and reproduction. At lower prey densities,P. persimilis from both “+” lines left spider mite-infested leaves more rapidly and consumed fewer prey eggs than an unselected population. Defining olfactory components of predator search behavior is one step in understanding the effect of plant volatiles on predator foraging efficiency. By selecting lines differing in their attraction to herbivore-induced plant volatiles we may experimentally investigate the link between this behavior, predator foraging efficiency, and local and regional predator-prey population dynamics. The impact of significant additive genetic variation in predator response to plant volatiles on evolution in a tritrophic context also remains to be uncovered.     

Genetic Variation in Foraging Traits and Life-History Traits of the Predatory Mite Neoseiulus womersleyi (Acari: Phytoseiidae) among Isofemale Lines

The predatory mite Neoseiulus womersleyi shows a significant correlation between its olfactory response and dispersal tendency in different geographical populations. This study investigated the genetic background of the relationship using isofemale lines. Y-tube olfactometer tests confirmed that there was a genetic component in predator response to herbivore-induced plant volatiles. Wind tunnel tests in the absence of the herbivore-induced plant volatiles revealed that the dispersal tendencies of N. womersleyi exhibited genetic variation among isofemale lines, and other experiments revealed the existence of significant differences in prey consumption rate, fecundity, and developmental time. However, there was no genetic correlation between behavioral traits (olfactory response, innate dispersal) and the other traits, suggesting that the positive correlation between the behavioral traits was not caused by genetic factors.     

When directional selection reduces geographic variation in traits mediating species interactions

Although we often focus on the causes of geographic variation, understanding processes that act to reduce geographic variation is also important. Here, we consider a process whereby adaptive foraging across the landscape and directional selection exerted by a conifer seed predator, the common crossbill (Loxia curvirostra), potentially act to homogenize geographic variation in the defensive traits of its prey. We measured seed predation and phenotypic selection exerted by crossbills on black pine (Pinus nigra) at two sites in the Pindos Mountains, Greece. Seed predation by crossbills was over an order of magnitude higher at the site where cone scale thickness was significantly thinner, which was also the cone trait that was the target of selection at the high predation site. Additional comparisons of selection differentials demonstrate that crossbills exert selection on black pine that is consistent in form across space and time, and increases in strength with increasing seed predation. If predators distribute themselves in relation to the defensive traits of their prey and the strength of selection predators exert is proportional to the amount of predation, then predators may act to homogenize trait variation among populations of their prey in a process analogous to coevolutionary alternation with escalation.     

Direct and correlated responses to selection for longevity in Drosophila buzzatii

The possible associations between longevity, early fecundity, and stress-resistance traits were explored using artificial selection on longevity in a laboratory population of Drosophila buzzatii . Three replicated lines were selected for increased lifespan (L lines) and compared with the respective unselected controls (C lines) after the 14th generation of selection. Mean longevity exhibited a significant response to selection. The baseline mortality tended to decrease in the L lines and a negative correlated response to longevity selection was found for early fecundity. Egg-to-adult developmental time increased in L lines. Longevity selection increased stress resistance for both high and low temperatures, as measured by heat knockdown resistance and chill-coma recovery. Starvation resistance also tended to be higher in L than in C lines. The results obtained are consistent with the hypothesis of trade-offs between longevity and early fecundity, and also suggest a trade-off association between adult longevity and developmental time. Correlated selection responses were generally consistent with correlations among the traits previously inferred from altitudinal clines for longevity and stress-resistance phenotypes.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 738–748.     

Predatory responses of selected lines of developmental variants of ladybird,Propylea dissecta (Coleoptera: Coccinellidae) in relation to increasing prey and predator densities

Individuals of the same species, population and generation frequently exhibit sub-maximal and significant genetic and phenotypic variation in their rate of development, showing slow and fast developers. Fast developers commonly have higher foraging and predation rates than slow developers. The consequence of such differences and foraging for the efficacy of biocontrol species remains under-explored. Slow and fast developers from a population of the ladybird, Propylea dissecta were separated and selected experimentally for F15 generations, and the predatory response of fourth instar larvae of control and experimentally selected slow and fast developers was then assessed at differing levels of prey (pea aphid, Acyrthosiphon pisum) and conspecific predator abundance. All individuals, whether slow or fast developers, showed a Type-II functional response, decrease in proportion of prey consumed with increasing prey biomass and an increase in proportion of prey consumed with increasing predator density. The proportion of prey consumed was highest in experimental fast developers and lowest in experimental slow developers. Attack rate was highest and handling time longest in slow developers of control/experimental groups. Mutual interference was least while area of discovery was highest in experimental fast developers. Thus, selection of fast developers for F15 generations led to higher functional responses, slower attack rates and faster prey consumption. This lower mutual interference and high searching efficiency indicates that they can be experimentally selected and used for better control of the pea aphids. This study is the first attempt to evaluate predatory responses of selected lines of an aphidophagous ladybird.     

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.     

Antipredator responses in Tetranychus urticae differ with predator specialization

The behavioural response of Tetranychus urticae to chemical cues from specialist predatory mites, Phytoseiulus persimilis, or generalist predatory bugs, Orius majusculus, on either bean or strawberry was studied in experimental arenas. Predators were placed on the leaf disc for 24 h and removed before T. urticae females were introduced. After 24 h, prey fecundity (number of eggs laid) and dispersal (number of prey drowned in the water barrier) were assessed. Chemical cues from the specialist predator resulted in reduced prey fecundity, significantly different from the generalist predator and control treatments. No interaction effect was found between plant species and prey fecundity, while significantly more eggs were laid on bean than on strawberry. Predator cues irrespective of predator specialization resulted in more prey dispersal than in the control. Findings emphasize the importance of specialization in the predator species complex for the degree and type of antipredator responses and resulting biological control.     

The paradox of enrichment in an adaptive world

Paradoxically, enrichment can destabilize a predator-prey food web. While adaptive dynamics can greatly influence the stability of interaction systems, few theoretical studies have examined the effect of the adaptive dynamics of interaction-related traits on the possibility of resolution of the paradox of enrichment. We consider the evolution of attack and defence traits of a predator and two prey species in a one predator-two prey system in which the predator practises optimal diet use. The results showed that optimal foraging alone cannot eliminate a pattern of destabilization with enrichment, but trait evolution of the predator or prey can change the pattern to one of stabilization, implying a possible resolution of the paradox of enrichment. Furthermore, trait evolution in all species can broaden the parameter range of stabilization. Importantly, rapid evolution can stabilize this system, but weaken its stability in the face of enrichment.     

Predator–prey interactions in anurans of the tropical dry forests of the Colombian Caribbean: A functional approach

Anuran–prey selection might be mediated by traits, either by mismatches in predator and prey traits (preventing interactions) or by predator selection of prey traits (encouraging interactions). These effect traits could be summarized in two contrasting foraging strategies: “active” and “sit-and-wait” foragers. We evaluated whether anurans could be classified into groups of species sharing traits associated with their diet, and what is the relation between particular effect traits of anurans and their prey. We collected anurans and identified their stomach contents once during dry, minor, and major rain seasons in six dry forest sites in the Colombian Caribbean. For each of the 19 anuran species and 436 prey items, we registered six effect traits. We applied RLQ and fourth-corner methodologies to relate predator and prey traits through their interaction matrix. Predators were assigned to five groups according to their differences in locomotion, body shape, proportion of the jaw width, mode of tongue protrusion, and strata preferred. Regarding preys, species were assigned to four groups according to their gregariousness, body shape and hardness, defensive traits, and mobility. Body size of both, predators and prey, had a minor contribution in the group assignment. We found that predators using active search target low-mobility preys, whereas species using sit-and-wait strategy target highly nutritive prey that are difficult to manipulate. By linking amphibian diet with foraging strategies, we hope to contribute to the understanding of mechanisms behind anuran–prey food web patterns and to build more realistic models of functional response to changing environments.     

Costs of resistance in the Drosophila-macrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction

Genetic variation for parasite resistance occurs in most host populations. Costs of resistance, manifested as reduced fitness of resistant genotypes in the absence of parasitism, can be an important factor contributing to the maintenance of this variation. One powerful tool for detecting costs of resistance is the study of correlated responses to artificial selection. Provided that experimental lines are recently derived from large outbreeding populations, and that inbreeding is minimized during the experiment, correlated responses to selection are expected to be strong indicators of pleiotropy. We artificially selected for elevated behavioral resistance against an ectoparasitic mite (Macrocheles subbadius) in replicate populations of the fly Drosophila nigrospiracula. Resistance was modeled as a threshold trait, and the realized heritability of resistance was estimated to be 12.3% (1.4% SE) across three replicate lines recently derived from nature. We contrasted the longevity and fecundity of resistant and control (unselected) flies under a variable thermal environment. We report that reduced fecundity is a correlated response to artificial selection for increased resistance, and that the strength of this effect increases from 25 degrees to 29 degrees C. In contrast, longevity differences were not detected between resistant and control lines at either temperature. These findings are robust as they were confirmed with an independent set of experimental lines. Thus, our results identify a negative genetic correlation between ectoparasite resistance and an important life-history trait. That a correlated response was only detected for fecundity, and not longevity, suggests that the genetic correlation is attributable to pleiotropic effects with narrower effects than reallocation of a general resource pool within the organism, although other interpretations are discussed. Combined with fluctuating parasite-mediated selection and temperature, the presence of this trade-off may contribute to the maintenance of genetic variation for resistance in natural populations.     

Effects of prey quality and availability on the life history of a trap-building predator

Although generalist predators catch a great diversity of prey species, foraging theory has mostly been concerned with quantitative aspects and neglected questions about the nutrient quality of prey. Here, we test the hypothesis that the life history of a trap-building predator is affected by both prey availability and by the nutrient quality of prey. Under controlled laboratory conditions, orb-weaving spiders ( Zygiella x-notata ) were raised from hatchlings to maturity on prey of different nutrient quality and in different amounts. Both prey nutrient quality and availability had significant but different effects on many important life history traits, such as instar duration, number of instars used in the development, body weight at maturation and development time. Prey availability was especially important for growth rates whereas prey nutrient quality had the most severe effects on juvenile survivorship and female fecundity. Furthermore, while prey of low quality tended to reduce the number of instars used in the development, prey availability induced sex-specific responses in instar numbers. Thus, both prey nutrient quality and availability may be important factors shaping the evolution of life history traits in generalist predators.     

Chimpanzee and felid diet composition is influenced by prey brain size

Prey use a wide variety of anti-predator defence strategies, including morphological and chemical defences as well as behavioural traits (risk-modulated habitat use, changes in activity patterns, foraging decisions and group living). The critical test of how effective anti-predator strategies are is to relate them to relative indices of mortality across predators. Here, we compare biases in predator diet composition with prey characteristics and show that chimpanzee (Pan troglodytes) and felid show the strongest and the most consistent predator bias towards small-brained prey. We propose that large-brained prey are likely to be more effective at evading predators because they can effectively alter their behavioural responses to specific predator encounters. Thus, we provide evidence for the hypothesis that brain size evolution is potentially driven by selection for more sophisticated and behaviourally flexible anti-predator strategies.     

Can prey behaviour induce spatially synchronic aggregation of solitary predators?

Spatio-temporal patterns of predator aggregations within their settlement areas (i.e. temporary settling zones used during dispersal or, more generally, foraging patches) were studied. By integrating the main behavioural rules of juveniles of Spanish imperial eagles Aquila adalberti during dispersal with the temporal availability of the eagles' main prey, we have developed several individual-based models under different simulation scenarios. The results suggest that the spatially synchrony of the aggregation patterns that we observed were derived from a combination of behavioural responses of the prey and the distances between available settlement areas. These results are discussed in the context of predator–prey relationships, optimal foraging and self-organizing processes.     

Size-dependent predation and correlated life history traits alter eco-evolutionary dynamics and selection for faster individual growth

Age at maturation is a key life history trait influencing individual fitness, population age structure, and ecological interactions. We investigated the evolution of age at maturity through changes in the von Bertalanffy growth constant for organisms with a simple juvenile-adult life history. We used Gillespie eco-evolutionary models to uncover the role of predation in driving the evolution of the growth constant when eco-evolutionary dynamics are present. We incorporated both size-independent and size-dependent predation into our models to generate differences in selection and dynamics in the system. Our results generally support the idea that faster ontogenetic growth is beneficial when populations are growing but that predation tends to have little effect on age at maturity unless there are trade-offs with other life history traits. In particular, if faster ontogenetic growth comes at the cost of fecundity, our results suggest that predation selects for intermediate levels of growth and fecundity. Eco-evolutionary dynamics influenced the nature of selection only when growth was linked to fecundity. We also found that predators that increasingly consume larger prey tend to have higher population sizes due to the greater energy intake from larger prey, but the growth rate-fecundity trade-off reversed this pattern. Overall, our results suggest an important role for interactions between size-dependent foraging and life-history trade-offs in generating varying selection on age at maturity through underlying growth traits.     

Prey responses to fine‐scale variation in predation risk from combined predators

While it is well documented that organisms can express phenotypic plasticity in response to single gradients of environmental variation, our understanding of how organisms integrate information along multiple environmental gradients is limited in many systems. Using the freshwater snail Helisoma trivolvis and two common predators (water bugs Belostoma flumineum and crayfish Orconectes rusticus), we explored how prey integrate information along multiple predation risk gradients (i.e. caged predators fed increasing amounts of prey biomass) that induce opposing phenotypes. When exposed to single predators fed increasing amounts of prey biomass, we detected threshold responses; intermediate amounts of consumed biomass induced phenotypic responses, but higher amounts induced little additional induction. This suggests that additional increases in predator‐induced traits with greater predator risk offer minimal increases in fitness or that a limit in the response magnitude was reached. Additionally, the response thresholds were contingent on the predator and focal trait. For shell width, responses were generally detected at a lower amount of consumed biomass by water bugs compared to crayfish. Within the crayfish treatments, we found that the shell thickness response threshold was lower than the shell width response threshold. When we combined gradients of consumed biomass from both predators, we found that the magnitude of response to one predator was often reduced when the other predator was present. Interestingly, these effects were often detected at consumed biomass levels that were lower than the threshold concentration necessary to elicit a response in the single‐predator treatments. Moreover, our combined predator treatments revealed that snails shifted from discrete responses to more continuous (i.e. graded) responses. Together, our results reveal that organisms experiencing multiple environmental gradients can integrate this information to make phenotypic decisions and demonstrate the novel result that an exposure to multiple species of predators can lower the response threshold of prey.     

Costs of inducible defence along a resource gradient

In addition to having constitutive defence traits, many organisms also respond to predation by phenotypic plasticity. In order for plasticity to be adaptive, induced defences should incur a benefit to the organism in, for example, decreased risk of predation. However, the production of defence traits may include costs in fitness components such as growth, time to reproduction, or fecundity. To test the hypothesis that the expression of phenotypic plasticity incurs costs, we performed a common garden experiment with a freshwater snail, Radix balthica, a species known to change morphology in the presence of molluscivorous fish. We measured a number of predator-induced morphological and behavioural defence traits in snails that we reared in the presence or absence of chemical cues from fish. Further, we quantified the costs of plasticity in fitness characters related to fecundity and growth. Since plastic responses may be inhibited under limited resource conditions, we reared snails in different densities and thereby levels of competition. Snails exposed to predator cues grew rounder and thicker shells, traits confirmed to be adaptive in environments with fish. Defence traits were consistently expressed independent of density, suggesting strong selection from predatory molluscivorous fish. However, the expression of defence traits resulted in reduced growth rate and fecundity, particularly with limited resources. Our results suggest full defence in predator related traits regardless of resource availability, and costs of defence consequently paid in traits related to fitness.     

The effects of becoming taller: direct and pleiotropic effects of artificial selection on plant height in Brassica rapa

Plant height is an important trait for plant reproductive success. Plant height is often under pollinator‐mediated selection, and has been shown to be correlated with various other traits. However, few studies have examined the evolutionary trajectory of plant height under selection and the pleiotropic effects of plant height evolution. We conducted a bi‐directional artificial selection experiment on plant height with fast cycling Brassica rapa plants to estimate its heritability and genetic correlations, and to reveal evolutionary responses to artificial selection on height and various correlated traits. With the divergent lines obtained through artificial selection, we subsequently conducted pollinator‐choice assays and investigated resource limitation of fruit production. We found that plant height variation is strongly genetically controlled (with a realized heritability of 41–59%). Thus, plant height can evolve rapidly under phenotypic selection. In addition, we found remarkable pleiotropic effects in phenology, morphology, floral scent, color, nectar and leaf glucosinolates. Most traits were increased in tall‐line plants, but flower size, UV reflection and glucosinolates were decreased, indicating potential trade‐offs. Pollinators preferred plants of the tall selection lines over the short selection lines in both greenhouse experiments with bumblebees and field experiment with natural pollinators. We did not detect any differences in resource limitation between plants of the different selection lines. Overall, our study predicts that increased height should evolve under positive pollinator‐mediated directional selection with potential trade‐offs in floral signals and herbivore defense.     

Plastic Responses of a Sessile Prey to Multiple Predators: A Field and Experimental Study

Background

Theory predicts that prey facing a combination of predators with different feeding modes have two options: to express a response against the feeding mode of the most dangerous predator, or to express an intermediate response. Intermediate phenotypes protect equally well against several feeding modes, rather than providing specific protection against a single predator. Anti-predator traits that protect against a common feeding mode displayed by all predators should be expressed regardless of predator combination, as there is no need for trade-offs.

Principal Findings

We studied phenotypic anti-predator responses of zebra mussels to predation threat from a handling-time-limited (crayfish) and a gape-size-limited (roach) predator. Both predators dislodge mussels from the substrate but diverge in their further feeding modes. Mussels increased expression of a non-specific defense trait (attachment strength) against all combinations of predators relative to a control. In response to roach alone, mussels showed a tendency to develop a weaker and more elongated shell. In response to crayfish, mussels developed a harder and rounder shell. When exposed to either a combination of predators or no predator, mussels developed an intermediate phenotype. Mussel growth rate was positively correlated with an elongated weaker shell and negatively correlated with a round strong shell, indicating a trade-off between anti-predator responses. Field observations of prey phenotypes revealed the presence of both anti-predator phenotypes and the trade-off with growth, but intra-specific population density and bottom substrate had a greater influence than predator density.

Conclusions

Our results show that two different predators can exert both functionally equivalent and inverse selection pressures on a single prey. Our field study suggests that abiotic factors and prey population density should be considered when attempting to explain phenotypic diversity in the wild.