A false‐positive food chain error associated with a generic predator gut content ELISA

Conventional prey‐specific gut content ELISA (enzyme‐linked immunosorbent assay) and PCR (polymerase chain reaction) assays are useful for identifying predators of insect pests in nature. However, these assays are prone to yielding certain types of food chain errors. For instance, it is possible that prey remains can pass through the food chain as the result of a secondary predator (hyperpredator) consuming a primary predator that had previously consumed the pest. If so, the pest‐specific assay will falsely identify the secondary predator as the organism providing the biological control services to the ecosystem. Recently, a generic gut content ELISA was designed to detect protein‐marked prey remains. That assay proved to be less costly, more versatile, and more reliable at detecting primary predation events than a prey‐specific PCR assay. This study examines the chances of obtaining a ‘false positive’ food chain error with the generic ELISA. Data revealed that the ELISA was 100% accurate at detecting protein‐marked Lygus hesperus Knight (Hemiptera: Miridae) remains in the guts of two (true) primary predators, Hippodamia convergens Guérin‐Méneville (Coleoptera: Coccinellidae) and Collops vittatus (Say) (Coleoptera: Melyridae). However, there was also a high frequency (70%) false positives associated with hyperpredators, Zelus renardii Kolenati (Hemiptera: Reduviidae), that consumed a primary predator that possessed protein‐marked L. hesperus in its gut. These findings serve to alert researchers that the generic ELISA, like the PCR assay, is susceptible to food chain errors.     

Ranking common predators of Bemisia tabaci in Georgia (USA) agricultural landscapes with diagnostic PCR: implications of primer specific post-feeding detection time

Developing a successful biological control program relies on understanding predator–prey interactions in agroecosystem field settings. Among several methods used, molecular gut content analysis (MGCA) has become a popular method to measure predator contributions to pest control services. Once MGCA is applied to diagnose predator–prey interactions, the DNA detectability half-life is often applied to adjust for differences in prey digestion time among predators. Although MGCA best practices are well established, with many primers available, further work is needed to rank among published primers for MGCA. Using a combination of laboratory feeding trials and application of diagnostic MGCA to field collected predators, we investigated Bemisia tabaci post-feeding detection times in three dominant predator functional groups (chewing, piercing/sucking, and spiders). This was based on three published B. tabaci-specific primers. These data reveal that primer choice generated significantly different B. tabaci DNA half-lives in predator gut content. The primers with longer half-life resulted in higher field predation frequency estimation. Our field data using the primer with the longest half-life suggest several abundant predators, including Hippodamia convergens, Geocoris punctipes, Orius spp., Thomisidae spider, and fire ants (Solenopsis invicta), are actively feeding on B. tabaci in cotton fields. Orius spp. and fire ants were the most abundant predator species in our study area and contributed the most to B. tabaci control. Our results suggest that primers can be classified based on their specific DNA half-lives and can be used to address different ecological questions such as how to study time-specific predation detection (nocturnal or diurnal).

     

Predator presence dramatically reduces copepod abundance through condition‐mediated non‐consumptive effects

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Prey‐specific foraging tactics in a web‐building spider

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The demographic and life‐history costs of fear: Trait‐mediated effects of threat of predation on Aedes triseriatus

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Determining the frequency of heteropteran predation on sweetpotato whitefly and pink bollworm using multiple ELISAs

The gut contents of field-collected, predaceous Heteroptera were assayed for the presence of eggs of the sweetpotato whitefly,Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) and the pink bollworm,Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae) using multiple enzyme-linked immunosorbent assays (ELISAs). Of seven species examined,Geocoris species andOrius tristicolor (Say) were the most frequent predators of sweetpotato whitefly with 32–39% of the individuals tested over the whole season scoring positive for whitefly antigens. With the exception ofLygus hesperus Knight, a major insect pest as well as a predator, the frequency of predation on pink bollworm eggs was much lower (0.7–14.3% positive over the season). Relatively few predators tested positive for both antigens (0.3–12.5%).     

Development of an immunological technique for identifying multiple predator–prey interactions in a complex arthropod assemblage

A simplified but highly effective approach for the post‐mortem evaluation of predation on several targeted members of an arthropod assemblage that does not require the development of pest‐specific enzyme‐linked immunosorbent assay (ELISA) (e.g. pest‐specific monoclonal antibodies) or PCR assays (DNA primers) is described. Laboratory feeding studies were conducted to determine if predation events could be detected from predators that consumed prey marked with foreign protein. I determined that large and small rabbit immunoglobulin G (IgG)‐marked prey can be detected by a rabbit‐IgG‐specific ELISA in the guts of chewing and piercing–sucking type predators. I then conducted multifaceted inclusion and exclusion field cage studies to qualify the degree of interguild and intraguild predation occurring among a complex arthropod assemblage during four separate light phase treatments. The field cages contained an arthropod assemblage consisting of 11 or 12 species of predaceous arthropods and three pest species. The three pests introduced into the cages included third instar Trichoplusia ni marked with rabbit IgG, third instar Lygus hesperus marked with chicken IgG and Pectinophora gossypiella sentinel egg masses. The inclusion cages allowed foraging fire ants, Solenopis xyloni, to freely enter the cages while the exclusion cages contained barriers that prevented ant entry. The results obtained using the conventional inclusion/exclusion field cage methodology revealed that there was substantial interguild and intraguild predation occurring on the majority of the arthropods in the assemblage, particularly in those cages that included ants. I then precisely identified which predators in the assemblage were feeding on the three targeted pests by conducting three post‐mortem gut content analyses on each individual predator (1503 individuals) in the assemblage. Specifically, P. gossypiella egg predation events were detected using an established P. gossypiella‐egg‐specific ELISA, and third instar T. ni and L. hesperus predation events were detected using rabbit‐IgG‐specific and chicken‐IgG‐specific ELISAs, respectively. Generally, the gut ELISAs revealed that Collops vittatus, Spanagonicus albofasciatus and Geocoris punctipes readily preyed on P. gossypiella eggs; Nabis alternatus, Zelus renardii and spiders (primarily Misumenops celer) readily preyed on marked L. hesperus nymphs, and spiders, S. albofasciatus and N. alternatus readily preyed on T. ni larvae. Furthermore, the cage methods and the post‐mortem predator gut ELISAs revealed very few distinctive patterns of predation with regard to the light cycle the assemblage was exposed to.     

Feeding preferences of an invasive Ponto‐Caspian goby for native and non‐native gammarid prey

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Turbidity amplifies the non‐lethal effects of predation and affects the foraging success of characid fish shoals

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Does a top predator reduce the predatory impact of an invasive mesopredator on an endangered rodent?

The mesopredator release hypothesis (MRH) predicts that reduced abundance of top‐order predators results in an increase in the abundance of smaller predators (mesopredators) due to a reduction in intra‐guild predation and competition. The irruption of mesopredators that follows the removal of top‐order predators can have detrimental impacts on the prey of the mesopredators. Here we investigated the mechanisms via which the presence of a top‐order predator can benefit prey species. We tested predictions made according to the MRH and foraging theory by contrasting the abundances of an invasive mesopredator (red fox Vulpes vulpes) and an endangered prey species (dusky hopping mouse Notomys fuscus), predator diets, and N. fuscus foraging behaviour in the presence and absence of a top‐predator (dingo Canis lupus dingo). As predicted by the MRH, foxes were more abundant where dingoes were absent. Dietary overlap between sympatric dingoes and foxes was extensive, and fox was recorded in 1 dingo scat possibly indicating intra‐guild predation. Notomys fuscus were more likely to occur in fox scats than dingo scats and as predicted by the MRH N. fuscus were less abundant in the absence of dingoes. The population increase of N. fuscus following rainfall was dampened in the absence of dingoes suggesting that mesopredator release can attenuate bottom‐up effects, although it remains conceivable that differences in grazing regimes associated with dingo exclusion could have also influenced N. fuscus abundance. Notomys fuscus exhibited lower giving‐up densities in the presence of dingoes, consistent with the prediction that their perceived risk of predation would be lower and foraging efficiency greater in the presence of a top‐predator. Our results suggest that mesopredator suppression by a top predator can create a safer environment for prey species where the frequency of fatal encounters between predators and prey is reduced and the non‐consumptive effects of predators are lower.     

Invasion success in communities with reciprocal intraguild predation depends on the stage structure of the resident population

The probability of individuals being targeted as prey often decreases as they grow in size. Such size‐dependent predation risk is very common in systems with intraguild predation (IGP), i.e. when predatory species interact through predation and competition. Theory on IGP predicts that community composition depends on productivity. When recently testing this prediction using a terrestrial experimental system consisting of two phytoseiid mite species, Iphiseius degenerans as the IG‐predator and Neoseiulus cucumeris as the IG‐prey, and pollen (Typha latifolia) as the shared resource, we could not find the predicted community shift. Instead, we observed that IG‐prey excluded IG‐predators when the initial IG‐prey/IG‐predator ratio was high, whereas the opposite held when the initial ratio was low, which is also not predicted by theory. We therefore hypothesized that the existence of vulnerable and invulnerable stages in the two populations could be an important driver of the community composition. To test this, we first demonstrate that IG‐prey adults indeed attacked IG‐predator juveniles in the presence of the shared resource. Second, we show that the invasion capacity of IG‐predators at high productivity levels indeed depended on the structure of resident IG‐prey populations. Third, we further confirmed our hypothesis by mimicking successive invasion events of IG‐predators into an established population of IG‐prey at high productivity levels, which consistently failed. Our results show that the interplay between stage structure of populations and reciprocal intraguild predation is decisive at determining the species composition of communities with intraguild predation.     

Real‐time PCR quantification of Bemisia tabaci (Homoptera: Aleyrodidae) B‐biotype remains in predator guts

The cotton whitefly, Bemisia tabaci (Gennadius) B‐biotype, is fed on by a wide variety of generalist predators, but there is little information on these predator–prey interactions, especially under field conditions. In this study, a real‐time polymerase chain reaction (PCR) assay was developed to quantify B. tabaci B‐biotype remains in predator gut. The B. tabaci B‐biotype genomic DNA copy number was referred to the actual amount of BT1 isolate, the B. tabaci B‐biotype specific DNA fragment. The numbers of BT1 isolate in one B. tabaci B‐biotype egg, individual adult and a single red‐eyed nymph were 2.56 × 10³, 2.56 × 10⁴, and 1.29 × 10⁴ copies, respectively. When Propylaea japonica adults fed on one, two, four, eight or 16 red‐eyed nymphs, the detected numbers of BT1 isolate ranged from 2.77 × 10⁴ to 4.05 × 10⁵ copies, forming a strong linear relationship (R² = 0.9899). Following the consumption of two red‐eyed nymphs, prey DNA was detectable in 100% of P. japonica at t = 0, decreasing to 80.0% and 60.0% after 1–4 h and 8 h of digestion, respectively, with 3.36 × 10⁴–1.25 × 10³ BT1 isolate copies. The predation by field‐collected predators, 26 larvae of P. japonica, and of Harmonia axyridis each, Chrysopa spp. larvae (Chrysopa pallens and C. formosa, 18 individuals in total), and a single adult of Scymnus hoffmanni, 19 adults of Orius sauteri and nine adult spiders (Erigonnidium graminicolum and Neoscona doenitzi), on B. tabaci B‐biotype were quantified. Of the 99 analysed predator individuals, 3.65 × 10²–4.60 × 10⁵ copies of BT1 isolate, equivalent to 0.8–18.8 red‐eyed nymphs were detected. These results suggest that TaqMan real‐time PCR technology may provide a rapid and sensitive method for quantifying B. tabaci B‐biotype remains in predator guts and will be invaluable in assessing the food web relationship between prey and arthropod predators.     

Intraguild predation of Orius tristicolor by Geocoris spp. and the paradox of irruptive spider mite dynamics in California cotton

It is paradoxical when a community of several natural enemies fails to control a pest population when it can be shown experimentally that single members of the natural enemy community are effective control agents when tested individually. This is the case for spider mites, Tetranychus spp., in California cotton. Spider mites exhibit irruptive population dynamics despite that fact that experiments have shown that there are at least four predators (Galendromus occidentalis, Frankliniella occidentalis, Orius tristicolor, and Geocoris spp.) that, when tested singly, can suppress mite populations. One possible explanation for the paradox is intraguild predation, wherein one predator consumes another. Here, I evaluate the hypothesis that intraguild predation is a strong interaction among spider mite predators. I report manipulative field experiments, focal observations of freely foraging predators in the field, and population survey data that suggest that the minute pirate bug O. tristicolor, is subject to strong predation by other members of the predator community, and in particular by Geocoris spp. These results, combined with the results of prior work, suggest that pervasive intraguild predation among spider mite predators may explain the pest status of Tetranychus spp. in cotton.     

Habitat heterogeneity and mammalian predator–prey interactions

• 1 In predator–prey theory, habitat heterogeneity can affect the relationship between kill rates and prey or predator density through its effect on the predator's ability to search for, encounter, kill and consume its prey. Many studies of predator–prey interactions include the effect of spatial heterogeneity, but these are mostly based on species with restricted mobility or conducted in experimental settings.
• 2 Here, we aim to identify the patterns through which spatial heterogeneity affects predator–prey dynamics and to review the literature on the effect of spatial heterogeneity on predator–prey interactions in terrestrial mammalian systems, i.e. in freely moving species with high mobility, in non‐experimental settings. We also review current methodologies that allow the study of the predation process within a spatial context.
• 3 When the functional response includes the effect of spatial heterogeneity, it usually takes the form of predator‐dependent or ratio‐dependent models and has wide applicability.
• 4 The analysis of the predation process through its different stages may further contribute towards identifying the spatial scale of interest and the specific spatial mechanism affecting predator–prey interactions.
• 5 Analyzing the predation process based on the functional response theory, but separating the stages of predation and applying a multiscale approach, is likely to increase our insight into how spatial heterogeneity affects predator–prey dynamics. This may increase our ability to forecast the consequences of landscape transformations on predator–prey dynamics.

     

An immunological approach to distinguish arthropod viviphagy from necrophagy

Scavenging activity of predators inhabiting agroecosystems has not been thoroughly investigated. Understanding the prevalence of necrophagy in predators is paramount to determining the effectiveness of biological control agents. A molecular predator gut content assay is described that can differentiate necrophagy from viviphagy. Cadaver sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and green lacewing, Chrysoperla rufilabris Burmeister (Neuroptera: Chrysopidae) serving as targeted prey items were marked with rabbit immunoglobulin G (IgG) protein and live prey items were marked with chicken IgG, respectively. The marked prey items were fed to convergent lady beetles, Hippodamia convergens Guérin-Méneville (Coleoptera: Coccinellidae) and soft-winged flower beetles, Collops vittatus (Say) (Coleoptera: Melyridae). The frequency of detection of the protein-marked prey items in the gut of the predaceous beetles was assessed at 0, 3, 6, 12, 24 and 48 h after feeding using a rabbit-IgG-specific or chicken-IgG-specific enzyme-linked immunosorbent assay (ELISA). Each IgG-specific ELISA detected the presence of the marker proteins in the gut of 90 % of the predators up to 12 h after prey consumption. A laboratory feeding study was also conducted to determine the propensity that each predator species engages in viviphagy and necrophagy. The laboratory feeding observations revealed that C. vittatus prefer carrion prey items. Finally, the laboratory observations of necrophagy were confirmed in a field study where C. vittatus was observed, directly and indirectly, feeding on H. convergens carcasses. The methodologies described here are useful for future studies on various aspects of insect predation.     

A review of the population dynamics of mule deer and black‐tailed deer Odocoileus hemionus in North America

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Non‐pathogenic aquatic bacteria activate the immune system and increase predation risk in damselfly larvae

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Knowing your enemies: Integrating molecular and ecological methods to assess the impact of arthropod predators on crop pests

The importance of natural enemies as the foundation of integrated pest management (IPM) is widely accepted, but few studies conduct the manipulative field experiments necessary to directly quantify their impact on pest populations in this context. This is particularly true for predators. Studying arthropod predator–prey interactions is inherently difficult: prey items are often completely consumed, individual predator–prey interactions are ephemeral (rendering their detection difficult) and the typically fluid or soft‐bodied meals cannot be easily identified visually within predator guts. Serological techniques have long been used in arthropod predator gut‐contents analysis, and current enzyme linked immunosorbent assays (ELISA) are highly specific and sensitive. Recently, polymerase chain reaction (PCR) methods for gut‐contents analysis have developed rapidly and they now dominate the diagnostic methods used for gut‐contents analysis in field‐based research. This work has identified trophic linkages within food webs, determined predator diet breadth and preference, demonstrated the importance of cannibalism and intraguild predation within and between certain taxa, and confirmed the benefits (predator persistence) and potential disadvantages (reduced feeding on pest species) of the availability of alternative nonpest prey. Despite considerable efforts to calibrate gut‐contents assays, these methods remain qualitative. Available techniques for predator gut‐contents analysis can provide rapid, accurate, cost‐effective identification of predation events. As such, they perfectly compliment the ecological methods developed to directly assess predator impacts on prey populations but which are imperfect at identifying the key predators. These diagnostic methods for gut‐contents analysis are underexploited in agricultural research and they are almost never applied in unison with the critical field experiments to measure predator impact. This paper stresses the need for a combined approach and suggests a framework that would make this possible, so that appropriate natural enemies can be targeted in conservation biological control.     

Predation yields greater population performance: what are the contributions of density‐ and trait‐mediated effects?

1. Population responses to extrinsic mortality can yield no change in the number of survivors (compensation) or an increase in the number of survivors (overcompensation) when the population is regulated by negative density‐dependence. This intriguing response has been the subject of theoretical studies, but few experiments have explored how the source of extrinsic mortality affects the response.
2. This study tests abilities of three functionally diverse predators, alone and combined, to induce (over)compensation of a prey population. Larval Aedes aegypti (Diptera: Culicidae) were exposed to predation by Mesocyclops longisetus (Crustacea: Copepoda), Anopheles barberi (Diptera: Culicidae), Corethrella appendiculata (Diptera: Corethrellidae), all three in a substitutive design, or no predation.
3. Predator treatment had no significant effect on the total number of adult survivors, nor on numbers of surviving males or females. The female development rate and a composite index of performance (r′) were greater with predation relative to no‐predator control. No differences were detected between diverse and single‐species predator treatments.
4. Sensitivity analyses indicated predation effects on the number of female adults produced, despite not being affected significantly, was the largest contributing factor to significant treatment effects on the demographic index r′. While predation did not significantly increase the production of adults, it did release survivors from density‐dependent effects sufficiently to increase population performance. This study provides an empirical test of mechanisms by which predation may yield positive mortality effects on victim populations, a phenomenon predicted to occur across many taxa and food webs.

     

Additive effects of predator diversity on pest control caused by few interactions among predator species

1. Studies of the impact of predator diversity on biological pest control have shown idiosyncratic results. This is often assumed to be as a result of differences among systems in the importance of predator–predator interactions such as facilitation and intraguild predation. The frequency of such interactions may be altered by prey availability and structural complexity. A direct assessment of interactions among predators is needed for a better understanding of the mechanisms affecting prey abundance by complex predator communities. 2. In a field cage experiment, the effect of increased predator diversity (single species vs. three‐species assemblage) and the presence of weeds (providing structural complexity) on the biological control of cereal aphids were tested and the mechanisms involved were investigated using molecular gut content analysis. 3. The impact of the three‐predator species assemblages of aphid populations was found to be similar to those of the single‐predator species treatments, and the presence or absence of weeds did not alter the patterns observed. This suggests that both predator facilitation and intraguild predation were absent or weak in this system, or that these interactions had counteracting effects on prey suppression. Molecular gut content analysis of predators provided little evidence for the latter hypothesis: predator facilitation was not detected and intraguild predation occurred at a low frequency. 4. The present study suggests additive effects of predators and, therefore, that predator diversity per se neither strengthens nor weakens the biological control of aphids in this system.