Molecular identification of predation by carabid beetles on exotic and native slugs in a strawberry agroecosystem

Generalist predators have the capacity to exert significant pressure on prey populations. However, integrating them into biological control programs relies on a detailed understanding of their foraging behavior and the levels of trophic connectedness with pest species. Carabid beetles are important predators of slugs, pests of agricultural, floricultural and horticultural crops worldwide, but these interactions have been rarely studied outside the Western Palearctic ecozone. Diagnostic molecular gut-content analysis was used to examine the strength of trophic pathways between a community of carabid beetles and two slug species, the exotic Deroceras reticulatum and native Deroceras laeve, in strawberry agroecosystems. Strawberries were grown according to standard horticultural practices for central Kentucky, following traditional bare ground planting or with the addition of detrital subsidies, to quantify the impact of habitat management on the abundance of pests and the strength of these trophic pathways. Following laboratory characterization of species-specific molecular markers targeting both Deroceras species, carabid beetles collected from a strawberry agroecosystem were screened for slug DNA. Field collections revealed important food web pathways existed between Harpalus pensylvanicus and D. reticulatum, with 7.2% screening positive for these prey yet none screening positive for D. laeve. In contrast, Chlaenius tricolor was found to feed on both slug species in the field, with 16% screening positive for both Deroceras. Despite below normal rainfall limiting slug densities in the field, the results presented here reveal the potential importance of carabid beetles in slug population dynamics in the Nearctic.     

Evaluating predation pressure on green treefrog larvae across a habitat gradient

The effect of a predator on the abundance of a prey species depends upon the predators abundance and its ability to capture that prey. The objectives of this research were to evaluate the community structure of predators of green treefrog (Hyla cinerea) tadpoles across habitat types and evaluate the effectiveness of individual predators on H. cinerea tadpoles. Correspondence and cluster analyses of predator frequencies across 23 aquatic habitats indicated that the majority of variance in predator communities was due to a division between permanent and temporary habitats. Experimental work demonstrated that survival of the smallest H. cinerea tadpoles was significantly lower than survival of medium and large tadpoles with the most effective predators, indicating that H. cinerea tadpoles attain a refuge from predation at larger body sizes. We combined the effectiveness of predators in experiments with the abundance of each predator species from the predator community survey to demonstrate that predation pressure on H. cinerea tadpoles is higher in temporary ponds. This pattern may explain in part why this species generally breeds successfully only in permanent habitats. It also confirms that discussions about an increasing gradient of predation pressure from temporary to permanent aquatic habitats should be restricted to individual prey species for which such a gradient has been demonstrated.     

Coexistence of multiple attractors in the coupling of an exploitative and an omnivorous food web

This work shows that the coupling of an exploitative with an omnivorous food web can generate unstable dynamics as well as multiple basins of attraction as a result of slight parameter and initial population variation. In terms of pest biological control, the results point to the need of extreme care with regard to stock assessment of the involved populations when designing strategies in biocontrol. If these requirements are not met, pest management may become quite precarious.     

Sowing of margin strips rich in floral resources improves herbivore control in adjacent crop fields

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Prey‐mediated changes in the selectivity of the predator Macrolophus pygmaeus (Heteroptera: Miridae)

When foraging in communities with mixed prey, generalist predators may be confronted with prey species that differ in quality, size and mobility and interact with one another. To examine prey selection, predation by Macrolophus pygmaeus (Heteroptera: Miridae) was recorded by providing a diet of either one or two prey species of Myzus persicae (third‐instar nymphs), Aphis gossypii (fourth‐instar nymphs), Trialeurodes vaporariorum (third‐instar nymphs) and Ephestia kuehniella (eggs). In the experiments, prey mobility, prey quality and prey biomass were considered. The biomass consumed by the predator was dependent on the combination of prey species and the quantity of biomass offered. In choice experiments with diets mixed of two prey species at equal densities, the predation to A. gossypii was significantly reduced in the presence of E. kuehniella but the rate of consumption of M. persicae, T. vaporariorum and E.kuehniella was not significantly affected by the coexistence of any other species in the mixed prey diet. When equal amounts of biomass from two prey species were provided in combination, the total consumed biomass was significantly reduced in the mixed prey diets composed of E. kuehniella eggs and aphid nymphs. Thus, under the mixed‐prey situation, prey selection by predators may be affected by interactions among prey species differing in traits such as quality, mobility and size.     

Human activities change marine ecosystems by altering predation risk

In ocean ecosystems, many of the changes in predation risk – both increases and decreases – are human‐induced. These changes are occurring at scales ranging from global to local and across variable temporal scales. Indirect, risk‐based effects of human activity are known to be important in structuring some terrestrial ecosystems, but these impacts have largely been neglected in oceans. Here, we synthesize existing literature and data to explore multiple lines of evidence that collectively suggest diverse human activities are changing marine ecosystems, including carbon storage capacity, in myriad ways by altering predation risk. We provide novel, compelling evidence that at least one key human activity, overfishing, can lead to distinct, cascading risk effects in natural ecosystems whose magnitude exceeds that of presumed lethal effects and may account for previously unexplained findings. We further discuss the conservation implications of human‐caused indirect risk effects. Finally, we provide a predictive framework for when human alterations of risk in oceans should lead to cascading effects and outline a prospectus for future research. Given the speed and extent with which human activities are altering marine risk landscapes, it is crucial that conservation and management policy considers the indirect effects of these activities in order to increase the likelihood of success and avoid unfortunate surprises.     

Measuring parasitoid movement from floral resources in a vineyard

The movement of natural enemies from floral resources is of particular importance in habitat manipulation research, as the distances that they disperse have consequences for the deployment of floral resources to improve insect natural enemy fitness. A number of marking techniques can be used to measure natural enemy movement; however, many of these are labour-intensive and not appropriate for many natural enemy species, the alternative, self-marking techniques, are less common. The aim of this study was to determine whether rubidium chloride (RbCl) could be used to measure the movement of Dolichogenidea tasmanica (Cameron) (Hymenoptera: Braconidae) from flowering buckwheat, Fagopyrum esculentum Moench plants in an organic vineyard. D. tasmanica is the most common parasitoid of leafroller larvae, a serious pest of grapevines in Australia and New Zealand. Foliar applications of rubidium chloride were made to a single strip of buckwheat in the centre of each of five vineyard areas. Sticky traps were placed in each area at distances of 0, 4, 10 and 30 m in opposite directions from the buckwheat to collect adult D. tasmanica. D. tasmanica were marked with rubidium after buckwheat plants had been sprayed with RbCl and were trapped up to 30 m from the plants within a seven-day sampling period. This study indicates that RbCl can be used to mark parasitoids to measure their movement from floral resources and may be used to inform decisions on the deployment of appropriate flowering plant species in conservation biological control.     

Use of plant resources by an omnivorous predator and the consequences for effective predation

Plant-provided food may enhance survival and establishment of omnivorous predators on target crops but on the other hand they may adversely affect predation rates and thus their potential for biological control of target pests. However, it is not known how predation is affected by plant food quality and prey density. The omnivorous predator Macrolophus pygmaeus is commonly used in augmentative releases in greenhouse crops. Experiments have shown its ability to utilize plant resources; eggplant and pepper plant leaves are the most and least suitable, respectively. In this study we searched the effects of floral resources (pollen or flower) of eggplant or pepper plant on the predation rate of M. pygmaeus. We used experiments in dishes (leaves) and cages (plants) under a range of densities of its prey, the aphid Myzus persicae. We did not find evidence that the consumption rates and the type of the functional responses of M. pygmaeus were affected by the plant leaf (eggplant vs pepper plant) or the increase in the spatial scale (leaf vs plant). However, the presence of pollen or a flower of eggplant and to a lesser extent of pepper plant reduced the plateau of the functional response to aphid density and increased the handling time per prey. The extent of prey feeding replacement by flower resources was dependent on the interaction between plant species and prey density. It seems that there is a constant rate of prey consumption replacement at intermediate and high prey densities on eggplant but only at intermediate prey densities on pepper plant. These results indicate the interactions between plant and prey resources in diets of omnivores and may be useful for its efficacy in pest control on eggplant and pepper plant.     

Effect of floral and extrafloral resources on predation of Aphis spiraecola by Harmonia axyridis on Apple

Flowering companion plants and plants producing extrafloral nectar are being proposed to enhance biological control in apple (Malus domestica Borkh.) orchards. This experiment evaluated the impact of floral and extrafloral resources on predation of spirea aphid (Aphis spiraecola Patch) on apple by adult Harmonia axyridis (Pallas) under greenhouse conditions. Predation of spirea aphids was not affected by the presence of flowering buckwheat (Fagopyrum esculentum) as compared with either buckwheat with flowers removed or an uninfested apple shoot. However, there was a significant reduction in predation of spirea aphids on an apple shoot in the presence of a peach shoot with extrafloral nectar glands compared with either a peach shoot of the same cultivar without nectar glands or an uninfested apple shoot. These findings demonstrate that alternative food resources potentially could interfere with rates of biological control and, therefore, need to be carefully evaluated before incorporating in an orchard design. More studies are needed to adequately gauge the net effects of adding floral or extrafloral resources in orchards for conservation biological control.     

Ten real‐time PCR assays for detection of fish predation at the community level in the San Francisco Estuary–Delta

The effect of predation on native fish by introduced species in the San Francisco Estuary–Delta (SFE) has not been thoroughly studied despite its potential to impact species abundances. Species‐specific quantitative PCR (qPCR) is an accurate method for identifying species from exogenous DNA samples. Quantitative PCR assays can be used for detecting prey in gut contents or faeces, discriminating between cryptic species, or detecting rare aquatic species. We designed ten TaqMan qPCR assays for fish species from the SFE watershed most likely to be affected by non‐native piscivores. The assays designed are highly specific, producing no signal from co‐occurring or related species, and sensitive, with a limit of detection between 3.2 and 0.013 pg/μL of target DNA. These assays will be used in conjunction with a high‐throughput qPCR platform to compare predation rates between native and non‐native piscivores and assess the impacts of predation in the system.     

Ground cover and floral resources in shelterbelts increase the abundance of beneficial hymenopteran families

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Reciprocal intraguild predation and predator coexistence

Intraguild predation is a mix of competition and predation and occurs when one species feeds on another species that uses similar resources. Theory predicts that intraguild predation hampers coexistence of species involved, but it is common in nature. It has been suggested that increasing habitat complexity and the presence of alternative food may promote coexistence. Reciprocal intraguild predation limits possibilities for coexistence even further. Habitat complexity and the presence of alternative food are believed to promote coexistence. We investigated this using two species of predatory mites, Iphiseiodes zuluagai and Euseius concordis, by assessing co‐occurrence in the field and on arenas differing in spatial structure in the laboratory. The predators co‐occured on the same plants in the field. In the laboratory, adults of the two mites fed on juveniles of the other species, both in the presence and the absence of a shared food source, showing that the two species are involved in reciprocal intraguild predation. Adults of I. zuluagai also attacked adults of E. concordis. This suggests limited possibilities for coexistence of the two species. Indeed, E. concordis invariably went extinct extremely rapidly on arenas without spatial structure with populations consisting of all stages of the two predators and with a shared resource. Coexistence was prolonged on host plant leaves with extra food sources, but E. concordis still went extinct. On small, intact plants, coexistence of the two species was much longer, and ended with the other species, I. zuluagai, often going extinct. These results suggest that spatial structure and the presence of alternative food increase the coexistence period of intraguild predators.     

The omnivorous predator Macrolophus pygmaeus,a good candidate for the control of both greenhouse whitefly and poinsettia thrips on gerbera plants

The poinsettia thrips Echinothrips americanus Morgan is a relatively new pest that has spread rapidly worldwide and causes serious damage in both vegetable and ornamental plants. In this study, we investigated if and how effective this pest can be controlled in gerbera by the omnivorous predator Macrolophus pygmaeus (Rambur). Because herbivores on plants can interact through a shared predator, we also investigated how poinsettia thrips control is affected by the presence of the greenhouse whitefly Trialeurodes vaporariorum (Westwood), a pest that commonly coexists with E. americanus in gerbera. In laboratory studies, we found that the predator M. pygmaeus fed on both pests when offered together. Olfactometer tests showed a clear preference of the predators for plants infested by whiteflies but not by thrips. In a greenhouse experiment, densities of both pests on single gerbera plants were reduced to very low levels by the predator, either with both pests present together or alone. Hence, predator‐mediated effects between whiteflies and thrips played only a minor role. The plant feeding of the shared predator probably reduced the dependence of predator survival and reproduction on the densities of the two pests, thereby weakening potential predator‐mediated effects. Thus, M. pygmaeus is a good candidate for biological control of both pests in gerbera. However, further research is needed to investigate pest control at larger scales, when the pests can occur on different plants.     

Functional response of Chrysoperla carnea (Neuroptera: Chrysopidae) to Helicoverpa armigera (Lepidoptera: Noctuidae): Effect of prey and predator stages

Abstract Understanding predator–prey interactions has a pivotal role in biological control programs. This study evaluated the functional response of three larval instars of the green lacewing, Chrysoperla carnea (Stephens), preying upon eggs and first instar larvae of the cotton bollworm, Helicoverpa armigera Hübner. The first and second instar larvae of C. carnea exhibited type II functional responses against both prey stages. However, the third instar larvae of C. carnea showed a type II functional response to the first instar larvae of H. armigera, but a type III functional response to the eggs. For the first instar larvae of C. carnea, the attack rate on H. armigera eggs was significantly higher than that on the larvae, whereas the attack rate of the second instar C. carnea on H. armigera larvae was significantly higher than that on the eggs. For the third instar larvae of C. carnea, the attack rate on the larvae was 1.015 ± 0.278/h, and the attack coefficient on the eggs was 0.036 ± 0.005. The handling times of the third instar larvae on larvae and eggs were 0.087 ± 0.009 and 0.071 ± 0.001 h, respectively. The highest predation rate was found for the third instar larvae of C. carnea on H. armigera eggs. Results of this study revealed that the larvae of C. carnea, especially the third instar, had a good predation potential in controlling H. armigera eggs and larvae. However, for a comprehensive estimation of the bio‐control abilities of C. carnea toward H. armigera, further field‐based studies are needed.     

The influence of landscape features on nest predation rates of grassland‐breeding waders

In Europe, lowland wet grasslands have become increasingly fragmented, and populations of waders in these fragments are subject to unsustainably high levels of nest predation. Patches of taller vegetation in these landscapes can support small mammals, which are the main source of prey for many predators. Providing such patches of habitat could potentially reduce levels of nest predation if predators preferentially target small mammals. However, predator attraction to patches of taller vegetation for foraging, shelter, perching and/or nesting could also result in local increases in predation rates, as a consequence of increased predator densities or spill‐over foraging into the surrounding area. Here we assess the influence of taller vegetation on wader nest predation rates, and the feasibility of managing vegetation structure to alter predator impacts. Between 2005 and 2011, the nest distribution and hatching success of Northern Lapwings Vanellus vanellus, which nest in the open, and Common Redshanks Tringa totanus, which conceal their nests in vegetation, were measured on a 487‐ha area of wet grassland in eastern England that is primarily managed for breeding waders. Predation rates of Lapwing nests increased significantly with distance from patches of taller vegetation, and decreased with increasing area of taller vegetation within 1 km of the nest, whereas neither variable influenced Redshank nest predation probability. These findings suggest that the distribution and activity of nest predators in lowland wet grassland landscapes may be influenced by the presence and distribution of areas of taller vegetation. For Lapwings at least, there may therefore be scope for landscape‐scale management of vegetation structure to influence levels of predation in these habitats.     

Temperature dependency of predation: Increased killing rates and prey mass consumption by predators with warming

Temperature dependency of consumer–resource interactions is fundamentally important for understanding and predicting the responses of food webs to climate change. Previous studies have shown temperature‐driven shifts in herbivore consumption rates and resource preference, but these effects remain poorly understood for predatory arthropods. Here, we investigate how predator killing rates, prey mass consumption, and macronutrient intake respond to increased temperatures using a laboratory and a field reciprocal transplant experiment. Ectothermic predators, wolf spiders (Pardosa sp.), in the lab experiment, were exposed to increased temperatures and different prey macronutrient content (high lipid/low protein and low lipid/high protein) to assess changes in their killing rates and nutritional demands. Additionally, we investigate prey mass and lipid consumption by spiders under contrasting temperatures, along an elevation gradient. We used a field reciprocal transplant experiment between low (420 masl; 26°C) and high (2,100 masl; 15°C) elevations in the Ecuadorian Andes, using wild populations of two common orb‐weaver spider species (Leucauge sp. and Cyclosa sp.) present along the elevation gradient. We found that killing rates of wolf spiders increased with warmer temperatures but were not significantly affected by prey macronutrient content, although spiders consumed significantly more lipids from lipid‐rich prey. The field reciprocal transplant experiment showed no consistent predator responses to changes in temperature along the elevational gradient. Transplanting Cyclosa sp. spiders to low‐ or high‐elevation sites did not affect their prey mass or lipid consumption rate, whereas Leucauge sp. individuals increased prey mass consumption when transplanted from the high to the low warm elevation. Our findings show that increases in temperature intensify predator killing rates, prey consumption, and lipid intake, but the responses to temperature vary between species, which may be a result of species‐specific differences in their hunting behavior and sensitivity to temperature.     

Protistan predation interferes with bacterial long‐term adaptation to substrate restriction by selecting for defence morphotypes

Bacteria that are introduced into aquatic habitats face a low substrate environment interspersed with rare productive ‘hotspots’, as well as high protistan grazing. Whereas the former condition should select for growth performance, the latter should favour traits that reduce predation mortality, such as the formation of large cell aggregates. However, protected morphotypes often convey a growth disadvantage, and bacteria thus face a trade‐off between investing in growth or defence traits. We set up an evolutionary experiment with the freshwater isolate Sphingobium sp. strain Z007 that conditionally increases aggregate formation in supernatants from a predator–prey coculture. We hypothesized that low substrate levels would favour growth performance and reduce the aggregated subpopulation, but that the concomitant presence of a flagellate predator might conserve the defence trait. After 26 (1‐week) growth cycles either with (P+) or without (P?) predators, bacteria had evolved into strikingly different phenotypes. Strains from P? had low numbers of aggregates and increased growth yield, both at the original rich growth conditions and on various single carbon sources. By contrast, isolates from the P+ treatment formed elevated proportions of defence morphotypes, but exhibited lower growth yield and metabolic versatility. Moreover, the evolved strains from both treatments had lost phenotypic plasticity of aggregate formation. In summary, the (transient) residence of bacteria at oligotrophic conditions may promote a facultative oligotrophic life style, which is advantageous for survival in aquatic habitats. However, the investment in defence against predation mortality may constrain microbial adaptation to the abiotic environment.     

Effects of density and predation risk on leaf litter processing by Phylloicus sp.

The allochthonous detritus that accumulates in the substrate of streams is used by aquatic invertebrate shredders for shelter and food. Shredders are considered rare in tropical systems, and little information is available about the role of density effects and predation risk (associated with the perception of predators by prey) in relationship to the resources used by these organisms. The aim of this study was to examine experimentally the effects of increased predation risk and of the density of Phylloicus sp. (i.e. of two types of biological relationships) on the processing of the leaf litter of Nectandra megapotamica (Spreng.) Mez. Phylloicus sp. can use leaf litter for case building and as a food resource. The density effect was measured using four treatments that differed only in the number of individuals (one, two, three or four). A second experiment with five treatments was performed to test the risk of non‐lethal predation on detritus consumption (shelter and food) by Phylloicus sp. (T1: Caddisfly; T2: Mayfly; T3: Astyanax sp./fish; T4: Damselflies; T5: Stonefly). A single Phylloicus and one other organism (a potential predator blocked with 0.5 mm fine mesh) were placed in each tank (0.002 m³ volume). We observed a negative effect of density on per capita litter consumption (experiment 1). The low density of Phylloicus may be a natural factor that decreases intraspecific competition. In the presence of fish, Phylloicus showed the lowest amount of litter processing observed in the experiment, indicating top‐down control (experiment 2). In treatments that involved the presence of invertebrates (non‐predatory and predatory), Phylloicus showed the highest amount and an intermediate amount of leaf litter processing, respectively (experiment 2). This observation also suggests that the predation effect is more probable for specific predator–prey pairs. Population density and predation risk in Phylloicus may be important factors controlling leaf litter processing.     

Shift in predation regime mediates diversification of foraging behaviour in a dragonfly genus

1. Behavioural adaptations to avoid and evade predators are common. Many studies have investigated population divergence in response to changes in predation regime within species, but studies exploring interspecific patterns are scant. Studies on interspecific divergence can infer common outcomes from evolutionary processes and highlight the role of environmental constraints in shaping species traits. 2. Species of the dragonfly genus Leucorrhinia underwent well‐studied shifts from habitats being dominated by predatory fish (fish lakes) to habitat being dominated by predatory invertebrates (dragonfly lakes). This change in top predators resulted in a set of adaptive trait modifications in response to the different hunting styles of both predator types: whereas predatory fish actively search and pursue prey, invertebrate predator follow a sit‐and‐wait strategy, not pursuing prey. 3. Here it is shown that the habitat shift‐related change in selection regime on larval Leucorrhinia caused species in dragonfly lakes to evolve increased larval foraging and activity, and results suggest that they lost the ability to recognise predatory fish. 4. The results of the present study highlight the impact of predators on behavioural trait diversification with habitat‐specific predation regimes selecting for distinct behavioural expression.     

Reversed predator–prey cycles are driven by the amplitude of prey oscillations

Ecoevolutionary feedbacks in predator–prey systems have been shown to qualitatively alter predator–prey dynamics. As a striking example, defense–offense coevolution can reverse predator–prey cycles, so predator peaks precede prey peaks rather than vice versa. However, this has only rarely been shown in either model studies or empirical systems. Here, we investigate whether this rarity is a fundamental feature of reversed cycles by exploring under which conditions they should be found. For this, we first identify potential conditions and parameter ranges most likely to result in reversed cycles by developing a new measure, the effective prey biomass, which combines prey biomass with prey and predator traits, and represents the prey biomass as perceived by the predator. We show that predator dynamics always follow the dynamics of the effective prey biomass with a classic ¼‐phase lag. From this key insight, it follows that in reversed cycles (i.e., ¾‐lag), the dynamics of the actual and the effective prey biomass must be in antiphase with each other, that is, the effective prey biomass must be highest when actual prey biomass is lowest, and vice versa. Based on this, we predict that reversed cycles should be found mainly when oscillations in actual prey biomass are small and thus have limited impact on the dynamics of the effective prey biomass, which are mainly driven by trait changes. We then confirm this prediction using numerical simulations of a coevolutionary predator–prey system, varying the amplitude of the oscillations in prey biomass: Reversed cycles are consistently associated with regions of parameter space leading to small‐amplitude prey oscillations, offering a specific and highly testable prediction for conditions under which reversed cycles should occur in natural systems.