Alteration of sensory abilities regulates the spatial scale of nonlethal predator effects

Many studies have shown that nonlethal predator effects such as trait-mediated interactions (TMIs) can have significant impacts on the structure and function of communities, but the role that environmental conditions play in modulating the scale and magnitude of these effects has not been carefully investigated. TMIs occur when prey exhibit behavioral or physiological responses to predators and may be more prevalent when abiotic conditions increase prey reactions to consumers. The purpose of this study was to determine if turbulence would alter the distance over which prey in aquatic systems respond to chemical cues emitted by predators in nature, thus changing the scales over which nonlethal predator effects occur. Using hard clams and blue crabs as a model predator–prey system, we investigated the effects of turbulence on clam reactive distance to predatory blue crabs in the field. Results suggest that turbulence diminishes clam reactions to predators and that the environmental context must be considered when predicting the extent of indirect predator effects in natural systems.     

The ubiquity of intraguild predation among predatory arthropods

Intraguild predation (IGP) occurs when one predator species attacks another predator species with which it competes for a shared prey species. Despite the apparent omnipresence of intraguild interactions in natural and managed ecosystems, very few studies have quantified rates of IGP in various taxa under field conditions. We used molecular analyses of gut contents to assess the nature and incidence of IGP among four species of coccinellid predators in soybean fields. Over half of the 368 predator individuals collected in soybean contained the DNA of other coccinellid species indicating that IGP was very common at our field site. Furthermore, 13.2% of the sampled individuals contained two and even three other coccinellid species in their gut. The interaction was reciprocal, as each of the four coccinellid species has the capacity to feed on the others. To our knowledge, this study represents the most convincing field evidence of a high prevalence of IGP among predatory arthropods. The finding has important implications for conservation biology and biological control.     

Non-consumptive effects of predatory mites on thrips and its host plant

Recent reviews on trait-mediated interactions in food webs suggest that trait-mediated effects are as important in triggering top–down trophic cascades as are density-mediated effects. Trait-mediated interactions between predator and prey result from non-consumptive predator effects changing behavioural and/or life history traits of prey. However, in biological control the occurrence of trait-mediated interactions between predators, prey and plants has been largely ignored. Here, we show that non-consumptive predator effects on prey cascade down to the plant in an agro-ecological food chain. The study system consisted of the predatory mites P. persimilis and N. californicus , the herbivorous non-target prey western flower thrips F. occidentalis and the host plant bean. Irrespective of predator species and risk posed to prey, the presence of predator eggs led to increased ambulation, increased mortality and decreased oviposition of thrips. Furthermore, the presence of predator eggs reduced leaf damage caused by thrips. To our knowledge this is the first experimental evidence suggesting a positive trophic cascade triggered by non-consumptive predator effects on non-target prey in an augmentative biological control system.     

Tradeoffs involved in site selection and foraging in a wolf spider: effects of substrate structure and predation risk

Understanding how animals weigh habitat features, exposure to predators and access to resources is important to determining their life history and distribution across the landscape. For example, when predators accumulate in structurally complex habitats, they face an environment with different competitive interactions, foraging opportunities and predatory risks. The wolf spider Pardosa milvina inhabits the soil surface of highly disturbed habitats such as agricultural fields throughout eastern North America. Pardosa displays effective antipredator behavior in the presence of chemical cues produced by a larger coexisting wolf spider, Hogna helluo . We used those cues to simulate predation risk in laboratory and field experiments designed to test the effects of habitat substrate and predation risk on site selection and prey consumption of Pardosa . In general, Pardosa preferred more complex substrates over bare dirt but those preferences were eliminated or reversed when cues from Hogna were present. Feeding trials revealed that substrate alone had few effects on Pardosa prey consumption, which we measured by documenting the change in the abdomen width. Although the presence of Hogna cues reduced prey consumption overall in field feeding trials, the negative effect of predation risk on prey consumption was only observed in grass and bare dirt substrates in the laboratory. We also found that prey capture was negatively affected by habitat complexity for both spider species but that same complexity offered Pardosa protection from predation by Hogna. This study provides insight into how two predator species interact to balance site selection and feeding in order to avoid predation. Shifts in foraging and distributional patterns of predators can have profound implications for their role in the food web.     

Free‐living nematodes as prey for higher trophic levels of forest soil food webs

Nematodes are the most abundant invertebrates in soils and are key prey in soil food webs. Uncovering their contribution to predator nutrition is essential for understanding the structure of soil food webs and the way energy channels through soil systems. Molecular gut content analysis of consumers of nematodes, such as soil microarthropods, using specific DNA markers is a novel approach for studying predator–prey interactions in soil. We designed new specific primer pairs (partial 18S rDNA) for individual soil‐living bacterial‐feeding nematode taxa (Acrobeloides buetschlii, Panagrellus redivivus, Plectus velox and Plectus minimus). Primer specificity was tested against more than 100 non‐target soil organisms. Further, we determined how long nematode DNA can be traced in the gut of predators. Potential predators were identified in laboratory experiments including nine soil mite (Oribatida, Gamasina and Uropodina) and ten springtail species (Collembola). Finally, the approach was tested under field conditions by analyzing five mite and three collembola species for feeding on the three target nematode species. The results proved the three primer sets to specifically amplify DNA of the respective nematode taxa. Detection time of nematode DNA in predators varied with time of prey exposure. Further, consumption of nematodes in the laboratory varied with microarthropod species. Our field study is the first definitive proof that free‐living nematodes are important prey for a wide range of soil microarthropods including those commonly regarded as detritivores. Overall, the results highlight the eminent role of nematodes as prey in soil food webs and for channelling bacterial carbon to higher trophic levels.     

A rapid technique for analysing diets of invertebrate predators by electrophoresis

A technique has been developed for the rapid determination of some species of prey consumed by mites and insects. The method detects prey enzymes within the gut of a predator by polyacrylamide gradient gel electrophoresis and subsequent staining for esterase activity. It is sufficiently sensitive to detect fruit tree red spider mite (Panonychus ulmi) esterases within the gut of a single predacious mite (Typhlodromus pyri) for at least 31 h after feeding. The method has been used to demonstrate feeding relationships among a range of insect and mite predator and prey species in the laboratory and in the field.     

Well-informed foraging: damage-released chemical cues of injured prey signal quality and size to predators

Predators use a variety of information sources to locate potential prey, and likewise prey animals use numerous sources of information to detect and avoid becoming the meal of a potential predator. In freshwater environments, chemosensory cues often play a crucial role in such predator/prey interactions. The importance of chemosensory information to teleost fish in marine environments is not well understood. Here, we tested whether coral reef fish predators are attracted to damage-released chemical cues from already wounded prey in order to find patches of prey and minimize their own costs of obtaining food. Furthermore, we tested if these chemical cues would convey information about status of the prey. Using y-maze experiments, we found that predatory dottybacks, Pseudochromis fuscus, were more attracted to skin extracts of damselfish, Pomacentrus amboinensis, prey that were in good condition compared to prey in poor body condition. Moreover, in both the laboratory and field, we found that predators could differentiate between skin extracts from prey based on prey size, showing a greater attraction to extracts made from prey that were the appropriate size to consume. This suggests that predators are not attracted to any general substance released from an injured prey fish instead being capable of detecting and distinguishing relatively small differences in the chemical composition of the skin of their prey. These results have implications for understanding predator foraging strategies and highlights that chemical cues play a complex role in predator–prey interactions in marine fish.     

Decomposing Predation: Testing for Parameters that Correlate with Predatory Performance by a Social Bacterium

Predator–prey interactions presumably play major roles in shaping the composition and dynamics of microbial communities. However, little is understood about the population biology of such interactions or how predation-related parameters vary or correlate across prey environments. Myxococcus xanthus is a motile soil bacterium that feeds on a broad range of other soil microbes that vary greatly in the degree to which they support M. xanthus growth. In order to decompose predator–prey interactions at the population level, we quantified five predation-related parameters during M. xanthus growth on nine phylogenetically diverse bacterial prey species. The horizontal expansion rate of swarming predator colonies fueled by prey lawns served as our measure of overall predatory performance, as it incorporates both the searching (motility) and handling (killing and consumption of prey) components of predation. Four other parameters—predator population growth rate, maximum predator yield, maximum prey kill, and overall rate of prey death—were measured from homogeneously mixed predator–prey lawns from which predator populations were not allowed to expand horizontally by swarming motility. All prey species fueled predator population growth. For some prey, predator-specific prey death was detected contemporaneously with predator population growth, whereas killing of other prey species was detected only after cessation of predator growth. All four of the alternative parameters were found to correlate significantly with predator swarm expansion rate to varying degrees, suggesting causal interrelationships among these diverse predation measures. More broadly, our results highlight the importance of examining multiple parameters for thoroughly understanding the population biology of microbial predation.     

Assessing changes in arthropod predator–prey interactions through DNA‐based gut content analysis—variable environment,stable diet

Analysing the structure and dynamics of biotic interaction networks and the processes shaping them is currently one of the key fields in ecology. In this paper, we develop a novel approach to gut content analysis, thereby deriving a new perspective on community interactions and their responses to environment. For this, we use an elevational gradient in the High Arctic, asking how the environment and species traits interact in shaping predator–prey interactions involving the wolf spider Pardosa glacialis. To characterize the community of potential prey available to this predator, we used pitfall trapping and vacuum sampling. To characterize the prey actually consumed, we applied molecular gut content analysis. Using joint species distribution models, we found elevation and vegetation mass to explain the most variance in the composition of the prey community locally available. However, such environmental variables had only a small effect on the prey community found in the spider's gut. These observations indicate that Pardosa exerts selective feeding on particular taxa irrespective of environmental constraints. By directly modelling the probability of predation based on gut content data, we found that neither trait matching in terms of predator and prey body size nor phylogenetic or environmental constraints modified interaction probability. Our results indicate that taxonomic identity may be more important for predator–prey interactions than environmental constraints or prey traits. The impact of environmental change on predator–prey interactions thus appears to be indirect and mediated by its imprint on the community of available prey.     

The roles of top and intermediate predators in herbivore suppression: contrasting results from the field and laboratory

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Testing the validity of functional response models using molecular gut content analysis for prey choice in soil predators

Analysis of predator–prey interactions is a core concept of animal ecology, explaining structure and dynamics of animal food webs. Measuring the functional response, i.e. the intake rate of a consumer as a function of prey density, is a powerful method to predict the strength of trophic links and assess motives of prey choice, particularly in arthropod communities. However, due to their reductionist set‐up, functional responses, which are based on laboratory feeding experiments, may not display field conditions, possibly leading to skewed results. Here, we tested the validity of functional responses of centipede predators and their prey by comparing them with empirical gut content data from field‐collected predators. Our predator–prey system included lithobiid and geophilomorph centipedes, abundant and widespread predators of forest soils and their soil‐dwelling prey. First, we calculated the body size‐dependent functional responses of centipedes using a published functional response model in which we included natural prey abundances and animal body masses. This allowed us to calculate relative proportions of specific prey taxa in the centipede diet. In a second step, we screened field‐collected centipedes for DNA of eight abundant soil‐living prey taxa and estimated their body size‐dependent proportion of feeding events. We subsequently compared empirical data for each of the eight prey taxa, on proportional feeding events with functional response‐derived data on prey proportions expected in the gut, showing that both approaches significantly correlate in five out of eight predator–prey links for lithobiid centipedes but only in one case for geophilomorph centipedes. Our findings suggest that purely allometric functional response models, which are based on predator–prey body size ratios are too simple to explain predator–prey interactions in a complex system such as soil. We therefore stress that specific prey traits, such as defence mechanisms, must be considered for accurate predictions.     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR

Gut-content analyses using molecular techniques are an effective approach to quantifying predator-prey interactions. Predation is often assumed but scavenging is an equally likely route by which animal DNA enters the gut of a predator/scavenger. We used PCR (polymerase chain reaction) to detect scavenged material in predator gut homogenates. The rates at which DNA in decaying slugs (Mollusca: Pulmonata) and aphids (Homoptera: Aphididae) became undetectable were estimated. The detectability of DNA from both carrion types in the guts of the generalist predator Pterostichus melanarius (Coleoptera: Carabidae) was then determined. The effects of carrion age and weight, as well as beetle sex, on detection periods, were quantified. Laboratory trials measured prey preference of beetles between live and decaying prey. Further experiments measured, for the first time, feeding by P. melanarius on dead slugs and aphids directly in the field. In both field and laboratory, P. melanarius preferentially fed on dead prey if available, but preference changed as the prey became increasingly decayed. Disappearance rates for slug carrion in wheat fields and grasslands were estimated and P. melanarius was identified as the main scavenger. Comparison of the retention time for dead slugs in the field, with the detection period for decaying slug material in the guts of the predators, showed that PCR-based techniques are not able to distinguish between predated and scavenged food items. This could potentially lead to overestimation of the impact of predation on slugs (and other prey) by carabids. Possible implications of facultative scavenging by invertebrate predators for biocontrol and food-web research are discussed.     

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.     

Self-organization, scale and stability in a spatial predator-prey interaction

Simple predator-prey models often predict extreme instability in interactions where the prey are depressed well below their carrying capacity. Although the behaviour of some laboratory systems conforms to this pattern, field and mesocosm studies generally show prolonged co-existence of prey and predator. Prominent among the possible causes of this discrepancy are the effects of spatial heterogeneity. In this paper we show that both discrete and continuous representations of the spatial Rosenzweig-McArthur model with immobile prey can be stabilized by self-organized prey heterogeneity. This concordance of behaviour closely parallels that which we have previously established in the context of invasion waves. We use the continuous model variant to calculate the characteristic spatial scales of the self-organized structures. The discrete variant forms the basis of a simulation study demonstrating the variety of stable structures and elucidating their relation to the history of the system. We note that all stable prey distributions take the form of a network of occupied patches separated by prey-free regions, and liken the process which generates such assemblages to the formation of a landscape mozaic.     

Piscivore-Prey Fish Interactions: Mechanisms behind Diurnal Patterns in Prey Selectivity in Brown and Clear Water

Environmental change may affect predator-prey interactions in lakes through deterioration of visual conditions affecting foraging success of visually oriented predators. Environmental change in lakes includes an increase in humic matter causing browner water and reduced visibility, affecting the behavioural performance of both piscivores and prey. We studied diurnal patterns of prey selection in piscivorous pikeperch (Sander lucioperca) in both field and laboratory investigations. In the field we estimated prey selectivity and prey availability during day and night in a clear and a brown water lake. Further, prey selectivity during day and night conditions was studied in the laboratory where we manipulated optical conditions (humic matter content) of the water. Here, we also studied the behaviours of piscivores and prey, focusing on foraging-cycle stages such as number of interests and attacks by the pikeperch as well as the escape distance of the prey fish species. Analyses of gut contents from the field study showed that pikeperch selected perch (Perca fluviatilis) over roach (Rutilus rutilus) prey in both lakes during the day, but changed selectivity towards roach in both lakes at night. These results were corroborated in the selectivity experiments along a brown-water gradient in day and night light conditions. However, a change in selectivity from perch to roach was observed when the optical condition was heavily degraded, from either brown-stained water or light intensity. At longer visual ranges, roach initiated escape at distances greater than pikeperch attack distances, whereas perch stayed inactive making pikeperch approach and attack at the closest range possible. Roach anti-predatory behaviour decreased in deteriorated visual conditions, altering selectivity patterns. Our results highlight the importance of investigating both predator and prey responses to visibility conditions in order to understand the effects of degrading optical conditions on piscivore-prey interaction strength and thereby ecosystem responses to brownification of waters.     

Prey bacteria shape the community structure of their predators

Although predator–prey interactions among higher organisms have been studied extensively, only few examples are known for microbes other than protists and viruses. Among the bacteria, the most studied obligate predators are the Bdellovibrio and like organisms (BALOs) that prey on many other bacteria. In the macroscopical world, both predator and prey influence the population size of the other''s community, and may have a role in selection. However, selective pressures among prey and predatory bacteria have been rarely investigated. In this study, Bacteriovorax, a predator within the group of BALOs, in environmental waters were fed two prey bacteria, Vibrio vulnificus and Vibrio parahaemolyticus. The two prey species yielded distinct Bacteriovorax populations, evidence that selective pressures shaped the predator community and diversity. The results of laboratory experiments confirmed the differential predation of Bacteriovorax phylotypes on the two bacteria species. Not only did Bacteriovorax Cluster IX exhibit the versatility to be the exclusive efficient predator on Vibrio vulnificus, thereby, behaving as a specialist, but was also able to prey with similar efficiency on Vibrio parahaemolyticus, indicative of a generalist. Therefore, we proposed a designation of versatilist for this predator. This initiative should provide a basis for further efforts to characterize the predatory patterns of bacterial predators. The results of this study have revealed impacts of the prey on Bacteriovorax predation and in structuring the predator community, and advanced understanding of predation behavior in the microbial world.     

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).

     

By their genes ye shall know them: genomic signatures of predatory bacteria

Predatory bacteria are taxonomically disparate, exhibit diverse predatory strategies and are widely distributed in varied environments. To date, their predatory phenotypes cannot be discerned in genome sequence data thereby limiting our understanding of bacterial predation, and of its impact in nature. Here, we define the ‘predatome,'' that is, sets of protein families that reflect the phenotypes of predatory bacteria. The proteomes of all sequenced 11 predatory bacteria, including two de novo sequenced genomes, and 19 non-predatory bacteria from across the phylogenetic and ecological landscapes were compared. Protein families discriminating between the two groups were identified and quantified, demonstrating that differences in the proteomes of predatory and non-predatory bacteria are large and significant. This analysis allows predictions to be made, as we show by confirming from genome data an over-looked bacterial predator. The predatome exhibits deficiencies in riboflavin and amino acids biosynthesis, suggesting that predators obtain them from their prey. In contrast, these genomes are highly enriched in adhesins, proteases and particular metabolic proteins, used for binding to, processing and consuming prey, respectively. Strikingly, predators and non-predators differ in isoprenoid biosynthesis: predators use the mevalonate pathway, whereas non-predators, like almost all bacteria, use the DOXP pathway. By defining predatory signatures in bacterial genomes, the predatory potential they encode can be uncovered, filling an essential gap for measuring bacterial predation in nature. Moreover, we suggest that full-genome proteomic comparisons are applicable to other ecological interactions between microbes, and provide a convenient and rational tool for the functional classification of bacteria.     

Biotic resistance of impact: a native predator (<Emphasis Type="Italic">Chaoborus</Emphasis>) influences the impact of an invasive predator (<Emphasis Type="Italic">Bythotrephes</Emphasis>) in temperate lakes

Introduced predators have caused some of the largest documented impacts of non-native species. Interactions among predators can have complex effects, leading to both synergistic and antagonistic outcomes. Complex interactions with native predators could play an important role in mediating the impact of non-native predators. We explore the role of the native predator context on the effect of the introduced predatory cladoceran Bythotrephes longimanus. While post-invasion impacts have been well described, studies have largely ignored the role of native predators. We used a field mesocosm experiment to determine whether Bythotrephes’ impact on prey communities is influenced by the presence of the ubiquitous native predatory insect larvae Chaoborus. The two predators exhibited niche complementarity as no change in total zooplankton prey abundance was detected across predator treatments. Rather, copepod abundances increased with decreasing abundances of Chaoborus, while cladocerans decreased with increasing abundances of Bythotrephes. Thus, the replacement of Chaoborus with Bythotrephes led to changes in the overall community structure of the zooplankton prey, but had little effect on prey total abundance. More interestingly, we found evidence of biotic resistance of impact, that is, the impact of Bythotrephes on the cladoceran community was altered when the two predators co-occurred. Specifically, the predation effect of Bythotrephes was more restricted to the shallower regions of the water column in the presence of Chaoborus, leading to a reduced impact on deeper dwelling prey taxa. Overall, our results demonstrate that the native predator context is important when trying to understand the effect of non-native predators and that variation in native predator abundances and assemblages could explain variation in impact across invaded habitats.