Prey Patch Patterns Predict Habitat Use by Top Marine Predators with Diverse Foraging Strategies

Spatial coherence between predators and prey has rarely been observed in pelagic marine ecosystems. We used measures of the environment, prey abundance, prey quality, and prey distribution to explain the observed distributions of three co-occurring predator species breeding on islands in the southeastern Bering Sea: black-legged kittiwakes (Rissa tridactyla), thick-billed murres (Uria lomvia), and northern fur seals (Callorhinus ursinus). Predictions of statistical models were tested using movement patterns obtained from satellite-tracked individual animals. With the most commonly used measures to quantify prey distributions - areal biomass, density, and numerical abundance - we were unable to find a spatial relationship between predators and their prey. We instead found that habitat use by all three predators was predicted most strongly by prey patch characteristics such as depth and local density within spatial aggregations. Additional prey patch characteristics and physical habitat also contributed significantly to characterizing predator patterns. Our results indicate that the small-scale prey patch characteristics are critical to how predators perceive the quality of their food supply and the mechanisms they use to exploit it, regardless of time of day, sampling year, or source colony. The three focal predator species had different constraints and employed different foraging strategies – a shallow diver that makes trips of moderate distance (kittiwakes), a deep diver that makes trip of short distances (murres), and a deep diver that makes extensive trips (fur seals). However, all three were similarly linked by patchiness of prey rather than by the distribution of overall biomass. This supports the hypothesis that patchiness may be critical for understanding predator-prey relationships in pelagic marine systems more generally.     

Encounters between aphids and their predators: the relative frequencies of disturbance and consumption

Ecologists may wish to evaluate the potential for predators to suppress prey populations through the costs of induced defensive behaviors as well as through consumption. In this paper, we measure the ratio of non‐consumptive, defense‐inducing encounters relative to consumptive encounters (henceforth the ‘disturbed : consumed ratio’) for two species of aphids and propose that these disturbed : consumed ratios can help evaluate the potential for behaviorally mediated prey suppression. For the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), the ratio of induced disturbances to consumption events was high, 30 : 1. For the cotton aphid, Aphis gossypii (Glover) (Homoptera: Aphididae), the ratio of induced disturbances to consumption events was low, approximately 1 : 14. These results indicate that the potential for predators to suppress pea aphid populations through induction of defensive behaviors is high, whereas the potential for predators to suppress cotton aphid populations through induced behaviors is low. In measuring the disturbed : consumed ratios of two prey species, this paper makes two novel points: it highlights the variability of the disturbed : consumed ratio, and it offers a simple statistic to help ecologists draw connections between predator–prey behaviors and predator–prey population dynamics.     

Growth and development of immature life stages ofPropylaea 14-punctata L. andCoccinella 7-punctata L. [Col.: Coccinellidae] simulated by the metabolic pool model

The conversion of aphid prey tissue (Acyrthosiphon pisum Harris) into predator biomass (immature life stages ofPropylaea 14-punctata L. andCoccinella 7-punctata L.) is calculated by plotting weight gain against assimilation (i.e. consumption minus egestion). This concept is added to the metabolic pool model byGutierrez et al. (1981) that enables the simulation of growth and development of a predator on a physiological basis. Physiological time is expressed in daydegrees above lower development thresholds for both species. Visual examination of observed and calculated values showed that the model satisfactorily describes the growth patterns of the above predators.      

Diversity of protists and bacteria determines predation performance and stability

Predation influences prey diversity and productivity while it effectuates the flux and reallocation of organic nutrients into biomass at higher trophic levels. However, it is unknown how bacterivorous protists are influenced by the diversity of their bacterial prey. Using 456 microcosms, in which different bacterial mixtures with equal initial cell numbers were exposed to single or multiple predators (Tetrahymena sp., Poterioochromonas sp. and Acanthamoeba sp.), we showed that increasing prey richness enhanced production of single predators. The extent of the response depended, however, on predator identity. Bacterial prey richness had a stabilizing effect on predator performance in that it reduced variability in predator production. Further, prey richness tended to enhance predator evenness in the predation experiment including all three protists predators (multiple predation experiment). However, we also observed a negative relationship between prey richness and predator production in multiple predation experiments. Mathematical analysis of potential ecological mechanisms of positive predator diversity—functioning relationships revealed predator complementarity as a factor responsible for both enhanced predator production and prey reduction. We suggest that the diversity at both trophic levels interactively determines protistan performance and might have implications in microbial ecosystem processes and services.     

Variation in the population demographics of <Emphasis Type="Italic">Scolopsis bilineatus</Emphasis> in response to predators

Predatory fishes play critical roles in the trophodynamics of coral reefs, and the biomass of predatory fish can be a strong determinant of the structure of reef fish assemblages. In this study, we used variations in predator biomass between management zones on the Great Barrier Reef to examine how predators influence the biomass, mortality, condition, and reproductive potential of a common prey species Scolopsis bilineatus (bridled monocle bream; Nemipteridae). Despite no numerical differences in biomass or mortality, we found significant differences in a variety of demographic traits for S. bilineatus between multiple areas of high and low predator biomass. The size-at-age, condition, and reproductive potential of fish were reduced in marine reserves where predator biomass was high. The response of fish to predators was highly sex dependent; females suffered the greatest reductions in condition and reproductive potential. This study supports the notion that predators can play important roles in regulating prey dynamics and emphasises the importance of understanding top-down control by predators when considering fisheries management techniques and conservation strategies.     

Buying time for colony mates: the anti-predatory function of soldiers in the eusocial aphid Ceratovacuna japonica (Homoptera, Hormaphidinae)

Eusocial aphids produce sterile individuals (soldiers) that specialize in colony protection. Killing predators is often considered the main function of soldiers. In this study, we tested the effect of harassment by soldiers of a eusocial aphid, Ceratovacuna japonica (Homoptera, Hormaphidinae), on predation by this species’ natural enemy, the larvae of Atkinsonia ignipicta (Lepidoptera, Stathmopodidae). We experimentally introduced some aphids and a predator to petri dishes and compared the survivorship of first-instar reproductives in the presence and absence of soldiers. We showed that soldiers can reduce the rate of predation on their colony mates without killing the predators. When predators encountered soldiers, they did not attempt to prey on them. Instead, they evaded them and often started to make a nest by spinning silken threads. The soldiers, in contrast, waved their forelegs and attacked the predator, and they sometimes succeeded in grasping the predator’s body. Because the predator used its mandibles to remove any soldier that succeeded in grasping its body, the soldier did not kill the predator. The reduction of predation was apparently caused by the delay of predation resulting from the harassment behavior of the soldiers. In eusocial aphids, a defensive strategy that delays predation may buy the soldiers’ colony mates time to reproduce or to escape from the predator.     

Feeding Fitness and Quality of Domesticated and Feral Predators: Effects of Long-Term Rearing on Artificial Diet

Predatory geocorids, Geocoris punctipes Say (Geocoridae: Hemiptera), that had been reared (domesticated) for over 6 years (60 continuous generations) on an artificial diet were compared with feral (F₁) counterparts to determine possible domestication-associated losses in predatory capabilities. Using adult female predators provided with either tobacco budworm larvae, Heliothis virescens F., or pea aphids, Acyrthosiphon pisum Harris, as prey, I measured predator weights, handling time with a single prey, amount extracted, consumption rate, and feeding (gut) capacity. Domesticated females were significantly smaller than ferals, weighing 4.53 mg versus 5.09 mg, respectively. Domestication did not significantly influence handling times, which averaged 131 (domesticated) and 122 min (feral) for predators feeding on H. virescens larvae and 106 (domesticated) and 94 min (feral) for G. punctipes feeding on A. pisum. Although there were significant differences in the weights of the two kinds of prey (H. virescens larvae being about twice as heavy as the A. pisum), both prey species exceeded the ingestion capacity of the predators. Amounts extracted by predators were 1.12 to 1.20 mg and were not significantly influenced by rearing background, prey biomass, or prey type. Consumption rates of 11.86 and 12.91 μg/min were nearly identical for both domesticated and feral predators regardless of prey species.     

Responses of Episyrphus balteatus DeGeer (Diptera: Syrphidae) in relation to prey density and predator size

Laboratory experiments were conducted to determine the functional and numerical responses of the aphidophagous hover fly Episyrphus balteatus DeGeer (Diptera: Syrphidae) to different densities of 4th instar black bean aphids, Aphis fabae Scopoli (Homoptera: Aphididae), on broad bean, Vicia faba L. (Fabaceae). Two different-sized larvae of predators were tested in different densities of similar-sized prey to determine whether functional response parameters depended on the body sizes of predator and prey. In numerical response experiments, gravid E. balteatus females were exposed individually to different densities of 4th instars of A. fabae on cut sections of the broad bean plant, V. faba L. Logistic regression suggested a type II functional response for both larval sizes of E. balteatus. The searching efficiency (a) of the larger larvae was higher than that of the smaller ones. Prey consumption was higher, and handling time (T_h) was lower for larger larvae than smaller ones. The theoretical maximum number of A. fabae nymphs eaten by the different-sized larvae was 125 and 269 nymphs per day. Larger E. balteatus larvae are more efficient predators for aphid management strategies. The reproductive numerical response, in terms of the number of eggs laid, increased curvilinearly with increasing prey density, but the proportion of eggs laid (egg number/prey density) decreased as the initial density of prey increased.     

Do phytoseiid mites select the best prey species in terms of reproductive success?

Optimal foraging theory predicts that predators prefer those prey species that are most rewarding in terms of reproductive success, which is dependent on prey quality and prey availability. To investigate which selection pressures may have moulded prey preference in an acarine system consisting of two prey species and three predator species, we tested whether prey preference of the predators is matched by the associated reproductive success.The predators involved areAmblyseius finlandicus (Oudemans),Am. potentillae (Garman) andTyphlodromus pyri Scheuten. The prey species are the apple rust mite (Aculus schlechtendali (Nalepa)) and the fruit-tree red spider mite (Panonychus ulmi (Koch)).Reproductive success was assessed in terms of intrinsic rate of increase and for one predator also in terms of diapause induction. All three predator species reached highest reproductive success on the same prey species: apple rust mite. This was most pronounced for the predatorAm. finlandicus, because its larval stage suffered severe mortality when feeding onP. ulmi.An independent study on prey preference of the three predator species (Dicke et al., 1988) revealed thatAm. finlandicus prefersAc. schlechtendali toP. ulmi, whereas the other two predator species have the reverse preference.Thus, on the basis of current data, prey preference ofAm. finlandicus can be understood in terms of reproductive success. However, this is not so for prey preference ofT. pyri andAm. potentillae. Investigations needed for a better understanding of prey preference of the last-named two predator species are discussed.     

Irreversible prey diapause as an optimal strategy of a physiologically extended Lotka–Volterra model

We propose an optimal control framework to describe intra-seasonal predator–prey interactions, which are characterized by a continuous-time dynamical model comprising predator and prey density, as well as the energy budget of the prey over the length of a season. The model includes a time-dependent decision variable for the prey, representing the portion of the prey population in time that is active, as opposed to diapausing (a state of physiological rest). The predator follows autonomous dynamics and accordingly it remains active during the season. The proposed model is a generalization of the classical Lotka–Volterra predator–prey model towards non-autonomous dynamics that furthermore includes the effect of an energy variable. The model has been inspired by a specific biological system of predatory mites (Acari: Phytoseiidae) and prey mites (so-called fruit-tree red spider mites) (Acari: Tetranychidae) that feed on leaves of apple trees—its parameters have been instantiated based on laboratory and field studies. The goal of the work is to understand the decisions of the prey mites to enter diapause (a state of physiological rest) given the dynamics of the predatory mites: this is achieved by solving an optimization problem hinging on the maximization of the prey population contribution to the next season. The main features of the optimal strategy for the prey are shown to be that (1) once in diapause, the prey does not become active again within the same season and hence diapause is an irreversible process; (2) for the vast majority of parameter space, the portion of prey individuals entering diapause within the season does not decrease in time; (3) with an increased number of predators, the optimal population strategy for the prey is to start diapause earlier and to enter diapause more gradually. This optimal population strategy will be studied for its ESS properties in a sequel to the work presented in this article.     

Parasitism-mediated prey selectivity in laboratory conditions and implications for biological control

In agroecosystems, parasitoids and predators may exert top-down regulation and predators for different reasons may avoid or give preference to parasitised prey, i.e., become an intraguild predator. The success of pest suppression with multiple natural enemies depends essentially on predator–prey dynamics and how this is affected by the interplay between predation and parasitism. We conducted a simple laboratory experiment to test whether predators distinguished parasitised prey from non-parasitised prey and to study how parasitism influenced predation. We used a host-parasitoid system, Spodoptera frugiperda and one of its generalist parasitoids, Campoletis flavicincta, and included two predators, the stinkbug Podisus nigrispinus and the earwig Euborellia annulipes. In the experiment, predators were offered a choice between non-parasitised and parasitised larvae. We observed how long it took for the predator to attack a larva, which prey was attacked first, and whether predators opted to consume the other prey after their initial attack. Our results suggest that, in general, female predators are less selective than males and predators are more likely to consume non-parasitised prey with this likelihood being directly proportional to the time taken until the first prey attack. We used statistical models to show that males opted to consume the other prey with a significantly higher probability if they attacked a parasitised larva first, while females did so with the same probability irrespective of which one they attacked first. These results highlight the importance of studies on predator–parasitoid interactions, as well as on coexistence mechanisms in agroecosystems. When parasitism mediates predator choice so that intraguild predation is avoided, natural enemy populations may be larger, thus increasing the probability of more successful biological control.     

Density-dependent effects of multiple predators sharing a common prey in an endophytic habitat

Multiple predator species feeding on a common prey can lead to higher or lower predation than would be expected by simply combining their individual effects. Such emergent multiple predator effects may be especially prevalent if predators share feeding habitat. Despite the prevalence of endophagous insects, no studies have examined how multiple predators sharing an endophytic habitat affect prey or predator reproduction. We investigated density-dependent predation of Thanasimus dubius (Coleoptera: Cleridae) and Platysoma cylindrica (Coleoptera: Histeridae) on a bark beetle prey, Ips pini (Coleoptera: Scolytidae), in a laboratory assay. I. pini utilize aggregation pheromones to group-colonize and reproduce within the stems of conifers. T. dubius and P. cylindrica exploit these aggregation pheromones to arrive simultaneously with the herbivore. Adult T. dubius prey exophytically, while P. cylindrica adults enter and prey within the bark beetle galleries. Larvae of both predators prey endophytically. We used a multiple regression analysis, which avoids confounding predator composition with density, to examine the effects of varying predator densities alone and in combination on herbivore establishment, herbivore reproduction, and predator reproduction. Predators reduced colonization success by both sexes, and decreased I. pini reproduction on a per male and per female basis. The combined effects of these predators did not enhance or reduce prey establishment or reproduction in unexpected manners, and these predators were entirely substitutable. The herbivores net replacement rate was never reduced significantly below one at prey and predator densities emulating field conditions. Similar numbers of each predator species emerged from the logs, but predator reproduction suffered from high intraspecific interference. The net replacement rate of P. cylindrica was not affected by conspecifics or T. dubius. In contrast, the net replacement rate of T. dubius decreased with the presence of conspecifics or P. cylindrica. Combinations of both predators led to an emergent effect, a slightly increased net replacement rate of T. dubius. This may have been due to predation by larval T. dubius on pupal P. cylindrica, as P. cylindrica develops more rapidly than T. dubius within this shared habitat.     

Studies on predation of the mosquito Culex fatigans by Rana tigrina tadpoles

Satiated predation, predation rate and prey preference of different weight groups of Rana tigrina (Daud) tadpoles on different larval and pupal stages of Culex fatigans were studied. Irrespective of the prey and predator size, the satiation time remained more or less equal. There exists a mass-dependent predation: Calculated predation rates or predatory constants (Kpr) showed that I instar prey was preyed upon at about equal rate, while other instars and pupa showed an increasing trend with increasing body weight of the predator. The prey preference assessed using the Kpr, revealed that prey size is an important parameter in predation. The R. tigrina tadpole is a more efficient pupal predator than other mosquito predators.     

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.     

Female blue tits with brighter yellow chests transfer more carotenoids to their eggs after an immune challenge

Predicting the consequences of predator biodiversity loss on prey requires an understanding of multiple predator interactions. Predators are often assumed to have independent and additive effects on shared prey survival; however, multiple predator effects can be non-additive if predators foraging together reduce prey survival (risk enhancement) or increase prey survival through interference (risk reduction). In marine communities, juvenile reef fish experience very high mortality from two predator guilds with very different hunting modes and foraging domains—benthic and pelagic predator guilds. The few previous predator manipulation studies have found or assumed that mortality is independent and additive. We tested whether interacting predator guilds result in non-additive prey mortality and whether the detection of such effects change over time as prey are depleted. To do so, we examined the roles of benthic and pelagic predators on the survival of a juvenile shoaling zooplanktivorous temperate reef fish, Trachinops caudimaculatus, on artificial patch reefs over 2 months in Port Phillip Bay, Australia. We observed risk enhancement in the first 7 days, as shoaling behaviour placed prey between predator foraging domains with no effective refuge. At day 14 we observed additive mortality, and risk enhancement was no longer detectable. By days 28 and 62, pelagic predators were no longer significant sources of mortality and additivity was trivial. We hypothesize that declines in prey density led to reduced shoaling behaviour that brought prey more often into the domain of benthic predators, resulting in limited mortality from pelagic predators. Furthermore, pelagic predators may have spent less time patrolling reefs in response to declines in prey numbers. Our observation of the changing interaction between predators and prey has important implications for assessing the role of predation in regulating populations in complex communities.     

On the role of sinigrin (mustard oil) in a tritrophic context: plant–aphid–aphidophagous hoverfly

1. Plant secondary metabolites can govern prey–predator interactions by altering the diet breadth of predators and sometimes provide an ecological refuge to prey. Brassicaceae plants and their specialist pests can be used as a model system for understanding the role of chemically mediated effects restricting the diet breadth of natural enemies, and consequently the occurrence of enemy‐free space for the specialist pest. 2. The objective of the present study was to test the performance of the generalist predator Episyrphus balteatus De Geer (Diptera: Syrphidae) fed on the specialist herbivore Brevicoryne brassicae L.(Homoptera: Aphididae), reared on two different brassica species: black mustard (Brassica nigra), a wild species with high levels of sinigrin; and canola (Brassica napus), a cultivated species without sinigrin. 3. The preference and performance of the predator and the performance of the prey were measured. Sinigrin was quantified by high‐performance liquid chromatography in both leaf samples and aphids reared on the two host plants. 4. The cabbage aphid performed better on canola than on black mustard. The performance of the predator on this aphid when reared on canola was clearly better than when reared on black mustard. Females had a higher overall preference for cabbage aphids reared on canola than on black mustard. 5. The ability of aphids reared on plants with high glucosinolate content to reduce the performance of their generalist predators indicates that the presence of B. nigra may provide enemy‐free space for the cabbage aphid from its predator, a concept that has useful application in the context of biological control for agricultural systems.     

Zebra mussels affect benthic predator foraging success and habitat choice on soft sediments

The introduction of zebra mussels (Dreissena spp.) to North America has resulted in dramatic changes to the complexity of benthic habitats. Changes in habitat complexity may have profound effects on predator-prey interactions in aquatic communities. Increased habitat complexity may affect prey and predator dynamics by reducing encounter rates and foraging success. Zebra mussels form thick contiguous colonies on both hard and soft substrates. While the colonization of substrata by zebra mussels has generally resulted in an increase in both the abundance and diversity of benthic invertebrate communities, it is not well known how these changes affect the foraging efficiencies of predators that prey on benthic invertebrates. We examined the effect of zebra mussels on the foraging success of four benthic predators with diverse prey-detection modalities that commonly forage in soft substrates: slimy sculpin (Cottus cognatus), brown bullhead (Ameirus nebulosus), log perch (Percina caprodes), and crayfish (Orconectes propinquus). We conducted laboratory experiments to assess the impact of zebra mussels on the foraging success of predators using a variety of prey species. We also examined habitat use by each predator over different time periods. Zebra mussel colonization of soft sediments significantly reduced the foraging efficiencies of all predators. However, the effect was dependent upon prey type. All four predators spent more time in zebra mussel habitat than in either gravel or bare sand. The overall effect of zebra mussels on benthic-feeding fishes is likely to involve a trade-off between the advantages of increased density of some prey types balanced against the reduction in foraging success resulting from potential refugia offered in the complex habitat created by zebra mussels.     

Predation behavior of Podisus nigrispinus on Spodoptera eridania

The behavior and effective predation time can affect the prey death in pest biological control programs. This work studied the Podisus nigrispinus (Dallas, 1851) (Heteroptera: Pentatomidae) behavior on Spodoptera eridania (Cramer, 1782) (Lepidoptera: Noctuidae) caterpillars, and its implications in case of prey escape. The preference bioassay (B1) aimed to verify the caterpillars body region (anterior: head and thorax; median and posterior) preferred by the predator and its implication in prey mortality. The predation duration bioassay considered the following effective predation times: 1, 2, 4, 8, 16, 32, 64 and 128 min; the caterpillars were removed after each predation time, to simulate prey escape, and the dead were counted until the seventh day. This experiment was performed in two ways: with randomly selected and not repeated predators (B2); and with the same predators in successive times (B3). The predator preferred to attack the caterpillars anterior region. The caterpillars mortality increased with increasing effective predation time. The mortality was 90% after 64 min under B2. This value was estimated for 16 min under B3. The P. nigrispinus prefers to attack the caterpillars anterior region and mortality of S. eridania caterpillars was favored in predators that have suffered predation interruption.     

Small stonefly predators affect microbenthic and meiobenthic communities in stream leaf packs

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Phenotypic plasticity in anti-intraguild predator strategies: mite larvae adjust their behaviours according to vulnerability and predation risk

Interspecific threat-sensitivity allows prey to maximize the net benefit of antipredator strategies by adjusting the type and intensity of their response to the level of predation risk. This is well documented for classical prey-predator interactions but less so for intraguild predation (IGP). We examined threat-sensitivity in antipredator behaviour of larvae in a predatory mite guild sharing spider mites as prey. The guild consisted of the highly vulnerable intraguild (IG) prey and weak IG predator Phytoseiulus persimilis, the moderately vulnerable IG prey and moderate IG predator Neoseiulus californicus and the little vulnerable IG prey and strong IG predator Amblyseius andersoni. We videotaped the behaviour of the IG prey larvae of the three species in presence of either a low- or a high-risk IG predator female or predator absence and analysed time, distance, path shape and interaction parameters of predators and prey. The least vulnerable IG prey A. andersoni was insensitive to differing IGP risks but the moderately vulnerable IG prey N. californicus and the highly vulnerable IG prey P. persimilis responded in a threat-sensitive manner. Predator presence triggered threat-sensitive behavioural changes in one out of ten measured traits in N. californicus larvae but in four traits in P. persimilis larvae. Low-risk IG predator presence induced a typical escape response in P. persimilis larvae, whereas they reduced their activity in the high-risk IG predator presence. We argue that interspecific threat-sensitivity may promote co-existence of IG predators and IG prey and should be common in predator guilds with long co-evolutionary history.