Predators marked with chemical cues from one prey have increased attack success on another prey species

1. To reduce the risk of being eaten by predators, prey alter their morphology or behaviour. This response can be tuned to the current danger if chemical or other cues associated with predators inform the prey about the risks involved. 2. It is well known that various prey species discriminate between chemical cues from predators that fed on conspecific prey and those that fed on heterospecific prey, and react stronger to the first. It is therefore expected that generalist predators are more successful in capturing a given prey species when they are contaminated with chemical cues from another prey species instead of cues from the same prey species. 3. Here, a generalist predatory mite was studied that feeds on thrips larvae as well as on whitefly eggs and crawlers. Mites were marked with cues (i.e. body fluids) of one of these two prey species and were subsequently offered thrips larva. 4. Predators marked with thrips cues killed significantly fewer thrips than predators marked with whitefly cues, even though the predator's tendency to attack was the same. In addition, more thrips larvae sought refuge in the presence of a predatory mite marked with thrips cues instead of whitefly cues. 5. This suggests that generalist predators may experience improved attack success when switching prey species.     

Network structure, predator–prey modules, and stability in large food webs

Large, complex networks of ecological interactions with random structure tend invariably to instability. This mathematical relationship between complexity and local stability ignited a debate that has populated ecological literature for more than three decades. Here we show that, when species interact as predators and prey, systems as complex as the ones observed in nature can still be stable. Moreover, stability is highly robust to perturbations of interaction strength, and is largely a property of structure driven by predator–prey loops with the stability of these small modules cascading into that of the whole network. These results apply to empirical food webs and models that mimic the structure of natural systems as well. These findings are also robust to the inclusion of other types of ecological links, such as mutualism and interference competition, as long as consumer–resource interactions predominate. These considerations underscore the influence of food web structure on ecological dynamics and challenge the current view of interaction strength and long cycles as main drivers of stability in natural communities. Electronic Supplementary Material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Antagonistic and Synergistic Interactions Among Predators

The structure and dynamics of food webs are largely dependent upon interactions among consumers and their resources. However, interspecific interactions such as intraguild predation and interference competition can also play a significant role in the stability of communities. The role of antagonistic/synergistic interactions among predators has been largely ignored in food web theory. These mechanisms influence predation rates, which is one of the key factors regulating food web structure and dynamics, thus ignoring them can potentially limit understanding of food webs. Using nonlinear models, it is shown that critical aspects of multiple predator food web dynamics are antagonistic/synergistic interactions among predators. The influence of antagonistic/synergistic interactions on coexistence of predators depended largely upon the parameter set used and the degree of feeding niche differentiation. In all cases when there was no effect of antagonism or synergism (a _ij =1.00), the predators coexisted. Using the stable parameter set, coexistence occurred across the range of antagonism/synergism used. However, using the chaotic parameter strong antagonism resulted in the extinction of one or both species, while strong synergism tended to coexistence. Whereas using the limit cycle parameter set, coexistence was strongly dependent on the degree of feeding niche overlap. Additionally increasing the degree of feeding specialization of the predators on the two prey species increased the amount of parameter space in which coexistence of the two predators occurred. Bifurcation analyses supported the general pattern of increased stability when the predator interaction was synergistic and decreased stability when it was antagonistic. Thus, synergistic interactions should be more common than antagonistic interactions in ecological systems.     

Predators induce interspecific herbivore competition for food in refuge space

Resource competition among herbivorous arthropods has long been viewed as unimportant because herbivore populations are controlled by predators. Although recently resurrected as an organizing force in arthropod communities on plants, there is still general agreement that resource competition among herbivores is reduced by predators. Here we show the reverse: predators induce interspecific resource competi-tion among herbivores. We found that thrips larvae ( Frankliniella occidentalis ) use the web produced and inhabited by the spider mite Tetranychus urticae as a refuge from predation by the phytoseiid mite Neoseiulus cucumeris . Thrips larvae prefer clean plant parts, but move into the web upon perceiving volatile cues associated with thrips and predators. This behaviour leads to lower predation risk, but also to reduced developmental rate and lower production of thrips larvae due to competition with spider mites. In addition, thrips larvae consume spider-mite eggs. Thus, predators induce interspecific competition and intraguild predation among herbivores within refuge space, even when host plants have an overall green appearance.     

Spatial heterogeneity in predator activity, nest survivorship, and nest-site selection in two forest thrushes

The ability of prey to find and use predator-free space has far-reaching consequences for their persistence and interactions with their predators. We tested whether nest survivorship of the ground-nesting veery (Catharus fuscescens) and shrub-nesting wood thrush (Hylocichla mustelina) was related to the local absence of a major nest predator, the white-footed mouse (Peromyscus leucopus). Mouse-free space was defined by trap stations that failed to trap a mouse during the avian breeding season (~May through July). In addition, mouse activity was quantified at individual trap stations based on the number of captures during the same period (six 2.25-ha trapping grids, each containing 121 trap stations trapped repeatedly throughout the summer between 1998 and 2002.) Annual mouse-free space was correlated with other measures of mouse activity based on trapping data. Both mouse-free space and activity metrics were significantly related to annual rates of nest predation (i.e., nest daily mortality rate) in veery but not wood thrush. Likewise, mouse-free space and mouse activity within the nest neighborhood (~30×30 m² surrounding each nest) was significantly related to nest survivorship in veery but not wood thrush. More trap stations had consistently greater (hotspots) and lesser (coldspots) mouse activity than expected by chance, and veeries were significantly more likely to nest near stations that had below the grid-average trapping success. Our study thus documented significant spatial variability in predator activity and its relationship to nest predation and nest-site selection in a ground-nesting songbird.     

Habitat complexity and sex-dependent predation of mosquito larvae in containers

Studies in aquatic systems have shown that habitat complexity may provide refuge or reduce the number of encounters prey have with actively searching predators. For ambush predators, habitat complexity may enhance or have no effect on predation rates because it conceals predators, reduces prey detection by predators, or visually impairs both predators and prey. We investigated the effects of habitat complexity and predation by the ambush predators Toxorhynchites rutilus and Corethrella appendiculata on their mosquito prey Aedes albopictus and Ochlerotatus triseriatus in container analogs of treeholes. As in other ambush predator-prey systems, habitat complexity did not alter the effects of T. rutilus or C. appendiculata whose presence decreased prey survivorship, shortened development time, and increased adult size compared to treatments where predators were absent. Faster growth and larger size were due to predator-mediated release from competition among surviving prey. Male and female prey survivorship were similar in the absence of predators, however when predators were present, survivorship of both prey species was skewed in favor of males. We conclude that habitat complexity is relatively unimportant in shaping predator-prey interactions in this treehole community, where predation risk differs between prey sexes.     

Changes in trophic level of Squatina guggenheim with increasing body length: relationships with type, size and trophic level of its prey

The occurrence of changes in the trophic level (TL) of sharks with growth has not been quantified until now. Here length-related changes on Squatina guggenheim Marini trophic level were determined, and shifts in type, size and trophic level of its prey were analysed. Sampling took place during five bottom trawl surveys conducted in the Argentine–Uruguayan Common Fishing Zone during spring (December/1995, October/1997) and fall (March/1997, March–April/1998, May–June/1998), using an Engel bottom-trawl net to capture the sharks. Three length groups were defined based on diet composition and using a cluster analysis (group I, 23–60 cm; group II, 61–80 cm; group III, 81–91 cm L _T). An ANOSIM procedure detected significant differences (P < 0.05) in the diet spectrum between the three length groups. The smallest sharks (group I) ingested fish prey ranging from 5 to 21 cm L _T, medium sharks (group II) fed on fish prey between 11 and 35 cm L _T, and largest sharks (group III) preyed on fish between 13 and 40 cm L _T. Diet structure of length groups were discriminated by almost the same prey taxa that characterized them. The increase of S. guggenheim body length promoted a decrease in the relative importance of small pelagic fishes. Contrarily, prey as medium benthopelagic fishes, medium pelagic squid and medium benthopelagic fishes showed an inverse tendency, indicating a broad diet spectrum of adults. Predator-length and prey-length relationship indicated a trend where 44.8% of S. guggenheim diet was integrated by prey <20% of their own body length and 32.8% of their diet was composed by prey >30% of their own length. The increase of mean prey weight was associated with the increase of predator weight and length. Smallest sharks (group I) were identified as secondary consumers (TL < 4) whereas medium sharks (group II) and largest sharks (group III) were placed as tertiary consumers (TL > 4). The study revealed an increase in S. guggenheim TL with shark growth as a consequence of changes on type, size and TL of prey ingested.     

Plankton motility patterns and encounter rates

Many planktonic organisms have motility patterns with correlation run lengths (distances traversed before direction changes) of the same order as their reaction distances regarding prey, mates and predators (distances at which these organisms are remotely detected). At these scales, the relative measure of run length to reaction distance determines whether the underlying encounter is ballistic or diffusive. Since ballistic interactions are intrinsically more efficient than diffusive, we predict that organisms will display motility with long correlation run lengths compared to their reaction distances to their prey, but short compared to the reaction distances of their predators. We show motility data for planktonic organisms ranging from bacteria to copepods that support this prediction. We also present simple ballistic and diffusive motility models for estimating encounter rates, which lead to radically different predictions, and we present a simple criterion to determine which model is the more appropriate in a given case.     

The predatory behavior of wintering <Emphasis Type="Italic">Accipiter</Emphasis> hawks: temporal patterns in activity of predators and prey

Studies focused on how prey trade-off predation and starvation risk are prevalent in behavioral ecology. However, our current understanding of these trade-offs is limited in one key respect: we know little about the behavior of predators. In this study, we provide some of the first detailed information on temporal patterns in the daily hunting behavior of bird-eating Accipiter hawks and relate that to their prey. During the winters of 1999–2004, twenty-one sharp-shinned hawks (A. striatus) and ten Cooper’s hawks (A. cooperii) were intensively radio tracked in rural and urban habitats in western Indiana, USA. Cooper’s hawks left roost before sunrise and usually returned to roost around sunset, while sharp-shinned hawks left roost at sunrise or later and returned to roost well before sunset. An overall measure of Cooper’s-hawk-induced risk (a composite variable of attack rate and activity patterns) generally reflected the timing of prey activity, with peaks occurring around sunrise and sunset. In contrast, risk induced by the smaller sharp-shinned hawk did not strongly reflect the activity of their prey. Specifically, an early morning peak in prey activity did not correspond to a period with intense hawk activity. The lack of early morning hunting by sharp-shinned hawks may reflect the high risk of owl-induced predation experienced by these hawks. The net effect of this intraguild predation may be to “free” small birds from much hawk-induced predation risk prior to sunrise. This realization presents an alternative to energetics as an explanation for the early morning peak in small bird activity during the winter.     

Evaluation of the importance of roe deer fawns in the spring–summer diet of red foxes in southeastern Norway

Red fox Vulpes vulpes predation on roe deer Capreolus capreolus fawns has the potential to strongly affect prey population dynamics, but it is unclear whether this relationship is symmetrical or not. We analysed the spring–summer diet of adult foxes and of their cubs in a fragmented agricultural area of southeastern Norway, where a parallel study showed that the predator kills annually 25% of the radio-monitored roe deer fawns. The overall diet was highly varied and was dominated by small mammals (33% volume), especially Microtus agrestis, and medium-large mammals (25%), largely represented by fawns. The frequency of occurrence (FO) of fawns in the diet of adult foxes was highest in early spring, thus, supporting previous studies showing that the predator started actively hunting for fawns from the very beginning of the birth season. During the summer, the FO of both fawns and small mammals markedly declined, while that of berries and invertebrates increased. As expected for central-place foragers, cubs consumed a higher proportion of large prey items compared to adults. In particular, 25% of scats from cubs—versus 9% from adults—contained roe deer remains, suggesting a high profitability of fawns for vixens raising offspring. However, considering the wide food spectrum and the availability of several large prey items in our study area, it seems unlikely that the importance of fawns to the diet and population dynamics of red foxes could be as great as the impact of the predator on roe deer populations. This asymmetrical relationship implies that there are unlikely to be any stabilising feedback mechanisms in the predator–prey relationship.     

Predation processes: behavioural interactions between red fox and roe deer during the fawning season

Predation by red fox (Vulpes vulpes) is the most important mortality cause for neonatal roe deer (Capreolus capreolus) in Scandinavia. With the objective of investigating how the fox finds fawns and how antipredatory behaviour of roe deer females influences choice of hunting method, I analysed observations of interactions between red fox and roe deer females. The observations were collected over 14 years in a mixed forest/agricultural landscape in Sweden. Of 49 fox–doe encounters, the doe attacked the fox in 59%. In 90% of these attacks the fox was successfully deterred. In two observations a doe saved a fawn attacked by a fox. Two hunting methods used by the fox were discerned. In 28 cases foxes searched the ground, and in 18 cases they surveyed open areas, often from a forest edge. The latter behaviour seemed more directed at fawns and was seen leading to a capture attempt. Searching seemed less efficient and also difficult to conduct due to the aggressiveness of does. A surveying sit-and-wait type of hunting method thus appeared as the most successful. The possibility to use this method could explain why roe deer fawns are more vulnerable to fox predation in open habitats.     

Consumption of aphids by spiders and the effect of additional prey: evidence from microcosm experiments

Spiders are common generalist predators in agroecosystems and have been suggested to lower herbivore abundance in crops. It is not clear, however, if spiders can effectively suppress pest populations, and if so, by what mechanisms. In a microcosm experiment, we examined the consumption of the bird cherry-oat aphid, Rhopalosiphum padi L. (Homoptera: Aphididae), a pest species in wheat fields, by three spider species that differ in their hunting methods. We then tested the effect of additional prey type on the ability of erigonid spiders to reduce aphids. In a 48-h experiment Mermessus denticulatus (Banks) (Araneae: Linyphiidae; Erigoninae) consumed more aphids than did Enoplognatha gemina Bosmans and Van Keer (Araneae: Theridiidae) and Bathyphantes cf. extricatus (O·P.-Cambridge) (Araneae: Linyphiidae; Linyphiinae). This difference may be due to the ability of erigonids to forage actively on the vegetation in addition to using their webs to catch prey. In a 7-week experiment, we provided springtails (Collembola) in high and low densities as additional prey to mated erigonids, prior to aphid introduction. Spiders in the low-density springtail treatment built more webs on the vegetation, and caused a 50% reduction in aphid populations. There were significantly fewer aphids in the low-density springtail treatment, but not in the high-density treatment, in comparison to the control (high-density springtails without spiders). The results suggest that additional prey density affects predatory interactions between M. denticulatus and R. padi and that erigonids, which occur in high densities in wheat fields in the Negev desert, may be involved in aphid suppression in these agroecosystems.

Population dynamics of thrips prey and their mite predators in a refuge

Prey refuges are expected to affect population dynamics, but direct experimental tests of this hypothesis are scarce. Larvae of western flower thrips Frankliniella occidentalis use the web produced by spider mites as a refuge from predation by the predatory mite Neoseiulus cucumeris. Thrips incur a cost of using the refuge through reduced food quality within the web due to spider mite herbivory, resulting in a reduction of thrips developmental rate. These individual costs and benefits of refuge use were incorporated in a stage-structured predator-prey model developed for this system. The model predicted higher thrips numbers in presence than in absence of the refuge during the initial phase. A greenhouse experiment was carried out to test this prediction: the dynamics of thrips and their predators was followed on plants damaged by spider mites, either with or without web. Thrips densities in presence of predators were higher on plants with web than on unwebbed plants after 3 weeks. Experimental data fitted model predictions, indicating that individual-level measurements of refuge costs and benefits can be extrapolated to the level of interacting populations. Model-derived calculations of thrips population growth rate enable the estimation of the minimum predator density at which thrips benefit from using the web as a refuge. The model also predicted a minor effect of the refuge on the prey density at equilibrium, indicating that the effect of refuges on population dynamics hinges on the temporal scale considered.     

An island-wide predator manipulation reveals immediate and long-lasting matching of risk by prey

Anti-predator behaviour affects prey population dynamics, mediates cascading effects in food webs and influences the likelihood of rapid extinctions. Predator manipulations in natural settings provide a rare opportunity to understand how prey anti-predator behaviour is affected by large-scale changes in predators. Here, we couple a long-term, island-wide manipulation of an important rodent predator, the island fox (Urocyon littoralis), with nearly 6 years of measurements on foraging by deer mice (Peromyscus maniculatus) to provide unequivocal evidence that prey closely match their foraging behaviour to the number of fox predators present on the island. Peromyscus maniculatus foraging among exposed and sheltered microhabitats (a measure of aversion to predation risk) closely tracked fox density, but the nature of this effect depended upon nightly environmental conditions known to affect rodent susceptibility to predators. These effects could not be explained by changes in density of deer mice over time. Our work reveals that prey in natural settings are cognizant of the dynamic nature of their predators over timescales that span many years, and that predator removals spanning many generations of prey do not result in a loss of anti-predator behaviour.     

Wasp Attacks and Spider Defence in the Orb Weaving Species <Emphasis Type="Italic">Zygiella x-notata</Emphasis>

Predator–prey relationships are generally based on arm-race. Wasps and spiders are both predators, which could be potential prey for each other. The orb weaver spider Zygiella x-notata is sometimes a prey for the wasp Vespula germanica. We observed the wasp hunting behaviour under natural conditions, and we tested the influence of the spider’s behaviour on the wasp attack success. Wasps were active predators during the reproductive period of the spider. Results showed that wasps located more easily male spiders than females particularly when they were engaged in mate guarding. Female location depended on the presence of a web, but also of prey or prey remains in the web. On the other hand, their location depend neither on the characteristics and the position of the retreat in the environment nor on the size of the web. After location, males were more often captured than females whatever their behaviour (mate guarding or not). Presence of prey remains or prey in the web did not increase the risk for the spider to be captured. There was also no influence of the retreat’s characteristics or of its position in the habitat on the risk for the spider to be captured; but wasp successful attacks were less numerous when silk was present around the entrance of the retreat or when the spider was completely inside. As prey and prey remains favoured location of spiders by the wasps, we tested spider web cleaning behaviour as a response to wasp predatory pressure. By throwing small polystyrene pellets in the webs, we observed that more 80% of the spiders rejected the pellets in less than one minute. Our data indicated that wasps were significant predators of Z. x-notata and wasp attack could have been a selective pressure that had favoured spider defensive behaviours such as web cleaning.     

Invasive plant architecture alters trophic interactions by changing predator abundance and behavior

As primary producers, plants are known to influence higher trophic interactions by initiating food chains. However, as architects, plants may bypass consumers to directly affect predators with important but underappreciated trophic ramifications. Invasion of western North American grasslands by the perennial forb, spotted knapweed (Centaurea maculosa), has fundamentally altered the architecture of native grassland vegetation. Here, I use long-term monitoring, observational studies, and field experiments to document how changes in vegetation architecture have affected native web spider populations and predation rates. Native spiders that use vegetation as web substrates were collectively 38 times more abundant in C. maculosa-invaded grasslands than in uninvaded grasslands. This increase in spider abundance was accompanied by a large shift in web spider community structure, driven primarily by the strong response of Dictyna spiders to C. maculosa invasion. Dictyna densities were 46–74 times higher in C. maculosa-invaded than native grasslands, a pattern that persisted over 6 years of monitoring. C. maculosa also altered Dictyna web building behavior and foraging success. Dictyna webs on C. maculosa were 2.9–4.0 times larger and generated 2.0–2.3 times higher total prey captures than webs on Achillea millefolium, their primary native substrate. Dictyna webs on C. maculosa also captured 4.2 times more large prey items, which are crucial for reproduction. As a result, Dictyna were nearly twice as likely to reproduce on C. maculosa substrates compared to native substrates. The overall outcome of C. maculosa invasion and its transformative effects on vegetation architecture on Dictyna density and web building behavior were to increase Dictyna predation on invertebrate prey ≥89 fold. These results indicate that invasive plants that change the architecture of native vegetation can substantially impact native food webs via nontraditional plant → predator → consumer linkages.     

Neophobia affects choice of food-item size in group-foraging common ravens (Corvus corax)

Individuals foraging in groups should develop behavioural tactics to optimise their gain. In novel feeding situations, predation risk and pressure of kleptoparasites may be particularly high and hence may constrain optimal foraging. To create a novel feeding situation, we offered common ravens (Corvus corax) equal numbers of either small (40 g) or large (160 g) pieces of meat on successive days, always in combination with the same novel object. During the first weeks, when ravens were still neophobic, small pieces were taken in larger numbers than large pieces. Intraspecific kleptoparasitism was more likely to occur when ravens carried large food items. It seems that initiating foragers were mainly innovative subdominants. Preference for small items might have decreased with increasing habituation because more dominants were then feeding directly at the source and hence were less likely to resort to kleptoparasitism as an alternative foraging tactic. Electronic Publication     

Chemical cues related to conspecific size in pintado catfish, Pseudoplatystoma coruscans

The pintado (Pseudoplatystoma coruscans) is a ferocious carnivorous catfish with evident cannibalistic behaviour; its nocturnal habits are related to its ability to use predominately chemical sensorial modalities. This study investigated whether the pintado distinguishes conspecifics of different body sizes using chemical cues, which may reflect different physiological conditions such as hunger or stress. Pintados were observed when receiving water conditioned by either larger or similar-size conspecifics. A control group consisted of pintados receiving unconditioned water. Twelve repetitions were used for each condition. Feeding-like behaviours were investigated in the receiver fish and showed that they responded only to the conditioned water. Furthermore, a higher frequency of responses occurred when the water was conditioned by a similar-size conspecific. Thus, it is concluded that pintados are able to recognize conspecific size by chemical cues related to size and that this ability contributes to the individual's decision making on whether to approach or to avoid the conspecific.     

Red foxes (Vulpes vulpes) use rabbit (Oryctolagus cuniculus) scent marks as territorial marking sites

One of the functions of chemical communication is territorial signalling. To achieve this, animals should mark their territories in a manner that increases the detectability of the marks, thereby maximising the probability that other animals detect the scent marks. In this study, we focused on the scent-marking behaviour of red foxes in relation to the abundance of their main prey, the European rabbit, in a suburban forest in Madrid, Spain. Our results reveal that foxes scent-marked more and increased the detectability of their marks in areas of higher rabbit density. It would appear that foxes defend food resources from competitors by increasing the number and the detectability of their scent marks.     

Size dependent predation risk in cryptic and conspicuous insects

It is not clear which selective pressures balance the strong fecundity advantage associated with large female body size in insects. A positively size-dependent mortality risk could provide a solution. In aviary experiments with artificial larvae, we studied if larger larvae of folivorous insects are more readily found (= detectability) and/or attacked (= acceptability) by birds. As size and colouration are likely to interact in determining birds’ responses, both cryptic and conspicuous prey items were used. As detectability is likely to be context-dependent, both simple (smooth) and complex (plants) backgrounds were used in respective experiments. In the conspicuous larvae, acceptability correlated negatively with prey size. However, their detectability was context dependent, being positively correlated with size on the simple background, whereas no significant effect was found on the complex background. Surprisingly, cryptic larvae showed no correlation between detectability and size, and there was only a weak tendency for birds to attack large larvae more readily. On the basis of a quantitative model, we conclude that the effect of positively size dependent bird predation, as a single factor, is not likely to counterbalance the fecundity advantage in cryptic species, and may thus not be crucial in determining the optimum for body sizes in these insects. In conspicuous species, there is a potential for different outcomes, because detectability and acceptability affect survival in different directions. The net outcome is, therefore, likely to be highly context-dependent. Furthermore, our results provide an explanation for the recently reported absence of systematic body-size differences between cryptic and conspicuous Lepidopteran larvae: although conspicuous larvae benefit from increasing their warning signal when growing larger, they also suffer a much sharper rise in detectability. Estonian Science Foundation grant # 5746; Centre for International Mobility (Finland).