Patterns of exclusion in an intraguild predator-prey system depend on initial conditions

1. When intraguild (IG)-prey are superior to IG-predators in competing for a shared resource, theory predicts coexistence of the IG-prey or the IG-predator with the resource depending on the productivity level: (a) resource and IG prey coexist when productivity is low; (b) IG-predator and resource coexist at high productivity; (c) if IG-prey and IG-predators can coexist, it is only at intermediate productivity levels. 2. We tested the existence of productivity-dependent regions of coexistence using an experimental system of two predatory mites and a shared food source (pollen). 3. At high levels of pollen supply (i.e. high productivity), the IG-predator excluded the IG-prey in most, but not all, cases. The same pattern of exclusion was observed at low productivity, at which the IG-prey was expected to exclude the IG-predator. Therefore, species composition could not be predicted by productivity levels. Instead, our results show that initial conditions affected strongly the outcome of the interaction. 4. We emphasize the need for theory on IG-predation that takes the effects of stage structure, initial conditions and transient dynamics into account.     

Diet of a polyphagous arthropod predator affects refuge seeking of its thrips prey

Antipredator behaviour of prey costs time and energy, at the expense of other activities. However, not all predators are equally dangerous to all prey; some may have switched to feeding on another prey species, making them effectively harmless. To minimize costs, prey should therefore invest in antipredator behaviour only when dangerous predators are around. To distinguish these from harmless predators, prey may use cues related to predation on conspecifics, such as odours released by a predator that has recently eaten conspecific prey or alarm pheromones released by attacked prey. We studied refuge use by a herbivorous/omnivorous thrips, Frankliniella occidentalis, in response to odours associated with a generalist predatory bug, Orius laevigatus, fed either with conspecific thrips or with other prey. The refuge used by thrips larvae is the web produced by its competitor, the two-spotted spider mite, Tetranychus urticae, where thrips larvae experience lower predation risk because the predatory bug is hindered by the web. Thrips larvae moved into this refuge when odours associated with predatory bugs that had previously fed on thrips were present, whereas odours from predatory bugs that had fed on other prey had less effect. We discuss the consequences of this antipredator behaviour for population dynamics. Copyright 2000 The Association for the Study of Animal Behaviour.     

Prey preference,intraguild predation and population dynamics of an arthropod food web on plants

The theory of intraguild predation (IGP) largely studies effects on equilibrium densities of predators and prey, while experiments mostly concern transient dynamics. We studied the effects of an intraguild (IG) predator, the bug Orius laevigatus, on the population dynamics of IG-prey, the predatory mite Phytoseiulus persimilis, and a shared prey, the phytophagous two-spotted spider mite Tetranychus urticae, as well as on the performance of cucumber plants in a greenhouse. The interaction of the predatory mite and the spider mite is highly unstable, and ends either by herbivores overexploiting the plant or predators exterminating the herbivores. We studied the effect of IGP on the transient dynamics of this system, and compared the dynamics with that predicted by a simple population-dynamical model with IGP added. Behavioural studies showed that the predatory bug and the predatory mite were both attracted to plants infested by spider mites and that the two predators did not avoid plants occupied by the other predator. Observations on foraging behaviour of the predatory bug showed that it attacks and kills large numbers of predatory mites and spider mites. The model predicts strong effects of predation and prey preference by the predatory bugs on the dynamics of predatory mites and spider mites. However, experiments in which the predatory bug was added to populations of predatory mites and spider mites had little or no effect on numbers of both mite species, and cucumber plant and fruit weight.     

Infochemical-mediated intraguild interactions among three predatory mites on cassava plants

Carnivorous arthropods exhibit complex intraspecific and interspecific behaviour among themselves when they share the same niche or habitat and food resources. They should simultaneously search for adequate food for themselves and their offspring and in the meantime avoid becoming food for other organisms. This behaviour is of great ecological interest in conditions of low prey availability. We examined by means of an olfactometer, how volatile chemicals from prey patches with conspecific or heterospecific predators might contribute to shaping the structure of predator guilds. To test this, we used the exotic predatory mites Typhlodromalus manihoti and T. aripo, and the native predatory mite Euseius fustis, with Mononychellus tanajoa as the common prey species for the three predatory mite species. We used as odour sources M. tanajoa-infested cassava leaves or apices with or without predators. T. manihoti avoided patches inhabited by the heterospecifics T. aripo and E. fustis or by conspecifics when tested against a patch without predators. Similarly, both T. aripo and E. fustis females avoided patches with con- or heterospecifics when tested against a patch without predators. When one patch contained T. aripo and the other T. manihoti, females of the latter preferred the patch with T. aripo. Thus, T. manihoti is able to discriminate between odours from patches with con- and heterospecifics. Our results show that the three predatory mite species are able to assess prey patch profitability using volatiles. Under natural conditions, particularly when their food sources are scarce, the three predatory mite species might be involved in interspecific and/or intraspecific interactions that can substantially affect population dynamics of the predators and their prey.     

Predator-induced neophobia in juvenile cichlids

Predation is an important but often fluctuating selection factor for prey animals. Accordingly, individuals plastically adopt antipredator strategies in response to current predation risk. Recently, it was proposed that predation risk also plastically induces neophobia (an antipredator response towards novel cues). Previous studies, however, do not allow a differentiation between general neophobia and sensory channel-specific neophobic responses. Therefore, we tested the neophobia hypothesis focusing on adjustment in shoaling behavior in response to a novel cue addressing a different sensory channel than the one from which predation risk was initially perceived. From hatching onwards, juveniles of the cichlid Pelvicachromis taeniatus were exposed to different chemical cues in a split-clutch design: conspecific alarm cues which signal predation risk and heterospecific alarm cues or distilled water as controls. At 2 months of age, their shoaling behavior was examined prior and subsequent to a tactical disturbance cue. We found that fish previously exposed to predation risk formed more compact shoals relative to the control groups in response to the novel disturbance cue. Moreover, the relationship between shoal density and shoal homogeneity was also affected by experienced predation risk. Our findings indicate predator-induced, increased cross-sensory sensitivity towards novel cues making neophobia an effective antipredator mechanism.     

Order of invasion affects the spatial distribution of a reciprocal intraguild predator

When intraguild predation is reciprocal, i.e. two predator species kill and feed on each other, theory predicts that well-mixed populations of the two species cannot coexist. At low levels of the shared resource, only the best competitor exists, whereas if the level of the common resource is high, the first species to arrive on a patch can reach high numbers, which prevents the invasion of the second species through intraguild predation. The order of invasion may therefore be of high importance in systems with reciprocal intraguild predation with high levels of productivity, with the species arriving first excluding the other species. However, natural systems are not well mixed and usually have a patchy structure, which gives individuals the possibility to choose patches without the other predator, thus reducing opportunities for intraguild predation. Such avoidance behaviour can cause spatial segregation between predator species, which, in turn, may weaken the intraguild interaction strength and facilitate their co-occurrence in patchy systems. Using a simple set-up, we studied the spatial distribution of two reciprocal intraguild predators when either of them was given priority on a patch with food. We released females of two predatory mite species sequentially and found that both species avoided patches on which the other species was resident. This resulted in partial spatial segregation of the species and thus a lower chance for the two species to encounter each other. Such behaviour reinforces segregation, because heterospecifics avoid patches with established populations of the other species. This may facilitate coexistence of two intraguild predators that would exclude each other in well-mixed populations.     

Role of kin recognition in oviposition preference and cannibalism by the predatory mite <Emphasis Type="Italic">Gynaeseius liturivorus</Emphasis>

Animals often select oviposition sites to minimize the predation risk for eggs and juveniles, which are more vulnerable to predation than adults. When females produce eggs in clusters, the eggs and juveniles are likely to suffer from cannibalism. Although cannibalism among siblings is known to be lower than among non-siblings, there have been few investigations into the possibility that females select oviposition sites that reduce the risk of cannibalism for the offspring. To test this possibility, we examined oviposition preference by adult females of the predatory mite Gynaeseius liturivorus in response to the presence of her own eggs and to eggs of other females, offering plastic discs as oviposition substrates. Although females did not clearly show a preference for plastic discs on which they had oviposited, they avoided plastic discs on which other females had oviposited. When eggs of other females were artificially placed on clean plastic discs, adult female mites avoided these discs, suggesting that the eggs were used as cues for oviposition preference. Cannibalism among juvenile siblings was lower than among non-siblings. These observations show that adult females and juveniles of G. liturivorus discriminate kin relationships among conspecific individuals. Therefore, oviposition preference by adult female G. liturivorus may lead to the reduced risk of cannibalism among offspring.     

Intraguild Interactions Between the Predatory Mites Neoseiulus californicus and Phytoseiulus persimilis

Species at the same trophic level may interact through competition for food, but can also interact through intraguild predation. Intraguild predation is widespread at the second and third trophic level and the effects may cascade down to the plant level. The effects of intraguild predation can be modified by antipredator behaviour in the intraguild prey. We studied intraguild predation and antipredator behaviour in two species of predatory mite, Neoseiulus californicus and Phytoseiulus persimilis, which are both used for control of the two-spotted spider mite in greenhouse and outdoor crops. Using a Y-tube olfactometer, we assessed in particular whether each of the two predators avoids odours emanating from prey patches occupied by the heterospecific predator. Furthermore, we measured the occurrence and rate of intraguild predation of different developmental stages of P. persimilis and N. californicus on bean leaves in absence or in presence of the shared prey. Neither of the two predator species avoided prey patches with the heterospecific competitor, both when inexperienced with the other predator and when experienced with prey patches occupied by the heterospecific predator. Intraguild experiments showed that N. californicus is a potential intraguild predator of P. persimilis. However, P. persimilis did not suffer much from intraguild predation as long as the shared prey was present. This is probably because N. californicus prefers to feed on two-spotted spider mites rather than on its intraguild prey.     

Antipredator Behaviour and Suppressed Aggression by Convict Cichlids in response to Injury-released Chemical Cues of Conspecifics but not to those of an Allopatric Heterospecific

In aquatic environments, chemical cues serve as an important source of information for the detection of predation risk. Here, we investigate the response of convict cichlids, Cichlasoma nigrofasciatum, to injury-released chemical cues. We exposed pairs of juvenile convict cichlids first to dechlorinated tap water (control), then later to one of two test stimuli: 1. chemical cues from injured convict cichlids; or 2. chemical cues from injured mosquito fish, Gambusia affinis. Gambusia are allopatric and phylogenetically unrelated to convict cichlids. Gambusia skin was used to control for a general response to injured fish. In response to conspecific cues, convict cichlids significantly increased time spent near the bottom of test aquaria and time under a shelter object. In response to Gambusia skin, convict cichlids tended to increase time spent near the tank bottom but did not increase use of the shelter object. There was a trade-off between antipredator and agonistic behaviours. In response to convict cichlid cues, there was a significant reduction in the frequency of approaches and bites. Gambusia skin extract had no significant effect on aggressive behaviour. These data suggest a species-specific antipredator response to conspecific alarm pheromones in a New World cichlid fish and demonstrate a trade-off between predator avoidance and intraspecific aggression. Further, the presence of an alarm response in this model species sets the stage for the use of chemical cues as a research tool to manipulate predation risk in studies of the interaction between predation risk and reproductive behaviour.     

Spider mite web mediates anti-predator behaviour

Herbivores suffer significant mortality from predation and are therefore subject to natural selection on traits promoting predator avoidance and resistance. They can employ an array of strategies to reduce predation, for example through changes in behaviour, morphology and life history. So far, the anti-predator response studied most intensively in spider mites has been the avoidance of patches with high predation risk. Less attention has been given to the dense web produced by spider mites, which is a complex structure of silken threads that is thought to hinder predators. Here, we investigate the effects of the web produced by the red spider mite, Tetranychus evansi Baker & Pritchard, on its interactions with the predatory mite, Phytoseiulus longipes Evans. We tested whether female spider mites recognize predator cues and whether these can induce the spider mites to produce denser web. We found that the prey did not produce denser web in response to such cues, but laid more eggs suspended in the web, away from the leaf surface. These suspended eggs suffered less from predation by P. longipes than eggs that were laid on the leaf surface under the web. Thus, by altering their oviposition behaviour in response to predator cues, females of T. evansi protect their offspring.     

Size-mediated response to public cues of predation risk in a tropical stream fish

In order to investigate any size-dependent differences between behavioural patterns, wild-caught Hart's rivulus Rivulus hartii of varying sizes were exposed to chemical alarm cues extracted from the skin of conspecifics or heterospecific Poecilia reticulata, or a tank water control, in a series of laboratory trials. In response to conspecific alarm cues, R. hartii subjects of the range of body sizes tested exhibited consistent, size-independent antipredator behaviours that were characterized by decreased locomotory activity and foraging levels and increased refuging behaviour. Conversely, focal R. hartii demonstrated significant size-dependent trends in response to heterospecific alarm cues, with smaller individuals exhibiting antipredator responses and larger individuals shifting their behaviour to increased levels of activity consistent with a foraging, or predatory, response. These results show that the behavioural responses of individual R. hartii to publicly available chemical alarm cues from heterospecifics are mediated by the size of the receiver.     

Antipredator behaviour of invasive geckos in response to chemical cues from snakes

Antipredator behaviours and the ability to appropriately assess predation risk contribute to increased fitness. Predator avoidance can be costly; however, so we expect prey to most strongly avoid predators that pose the greatest risk (i.e., prey should show threat sensitivity). For invasive species, effectively assessing the relative risk posed by predators in the new environment may help them establish in new environments. We examined the antipredator behaviour of introduced Asian house geckos, Hemidactylus frenatus (Schlegel), by determining if they avoided shelters scented with the chemical cues of native predatory snakes (spotted pythons, Antaresia maculosa [Peters]; brown tree snakes, Boiga irregularis [Merrem]; common tree snakes, Dendrelaphis punctulata [Grey]; and carpet pythons, Morelia spilota [Lacépède]). We also tested if Asian house geckos collected from vegetation vs. anthropogenic substrates (buildings) responded differently to the chemical cues of predatory snakes. Asian house geckos did not show a generalised antipredator response, that is, they did not respond to the chemical cues of all snakes in the same way. Asian house geckos avoided the chemical cues of carpet pythons more strongly than those of other snake species, providing some support for the threat‐sensitivity hypothesis. There was no difference in the antipredator behaviour of Asian house geckos collected from buildings vs. natural vegetation, suggesting that individuals that have invaded natural habitats have not changed their antipredator behaviour compared to urban individuals. Overall, we found some evidence indicating Asian house geckos are threat‐sensitive to some Australian predacious snakes.     

Predator (<Emphasis Type="Italic">Carcinus maenas</Emphasis>) nonconsumptive limitation of prey (<Emphasis Type="Italic">Nucella lapillus</Emphasis>) feeding depends on prey density and predator cue type

Predators often have nonconsumptive effects (NCEs) on prey. For example, upon detection of predator cues, prey can reduce feeding activities to hamper being detected by predators. Previous research showed that waterborne chemical cues from green crabs (Carcinus maenas, predator) limit the dogwhelk (Nucella lapillus, prey) consumption of barnacles regardless of dogwhelk density, even though individual predation risk for dogwhelks decreases with conspecific density. Such NCEs might disappear with dogwhelk density if dogwhelks feed on mussels, as mussel stands constitute better antipredator refuges than barnacle stands. Through a laboratory experiment, we effectively found that crab chemical cues limit the per-capita consumption of mussels by dogwhelks at low dogwhelk density but not at high density. The combination of tactile and chemical cues from crabs, however, limited the dogwhelk consumption of mussels at both dogwhelk densities. The occurrence of such NCEs at both dogwhelk densities could have resulted from tactile cues indicating a stronger predation risk than chemical cues alone. Overall, the present study reinforces the notions that prey evaluate conspecific density when assessing predation risk and that predator cue type affects their perception of risk.     

Trophic omnivory across a productivity gradient: intraguild predation theory and the structure and strength of species interactions

Intraguild predation theory centres on two predictions: (i) for an omnivore and an intermediate predator (IG-prey) to coexist on shared resources, the IG-prey must be the superior resource competitor, and (ii) increasing resource productivity causes the IG-prey''s equilibrium abundance to decline. I tested these predictions with a series of species-rich food webs along New Zealand''s rocky shores, focusing on two predatory whelks, Haustrum haustorium, a trophic omnivore, and Haustrum scobina, the IG-prey. In contrast to theory, the IG-prey''s abundance increased with productivity. Furthermore, feeding rates and allometric considerations indicate a competitive advantage for the omnivore when non-shared prey are considered, despite the IG-prey''s superiority for shared prey. Nevertheless, clear and regular cross-gradient changes in network structure and interaction strengths were observed that challenge the assumptions of current theory. These insights suggest that the consideration of consumer-dependent functional responses, non-equilibrium dynamics, the dynamic nature of prey choice and non-trophic interactions among basal prey will be fruitful avenues for theoretical development.     

Detection of conspecific and heterospecific alarm signals by juvenile pumpkinseed under weak acidic conditions

Under neutral (pH 7·0) conditions, juvenile pumpkinseed Lepomis gibbosus exhibited significant antipredator responses, of similar intensities, to the chemical alarm cues of conspecifics, an allopatric congener the green sunfish Lepomis cyanellus and the artificial alarm cue of a sympatric prey guild member (Cyprinidae, hypoxanthine-3- N -oxide). Under weakly acidic conditions (pH 6·0), however, no increase in antipredator behaviour was seen in response to hypoxanthine-3- N -oxide and a quantitatively weaker response was found in response to conspecific and congener cues, suggesting that the use of chemical alarm cues by some prey fishes may be impaired by acid precipitation.     

Is there a fish alarm cue? Affirming evidence from a wild study

Chemical alarm cues released from injured tissue are not released under any other context and therefore reliably inform nearby prey of the presence of a predator. Laboratory and field studies have demonstrated that most aquatic taxa show antipredator responses to chemical alarm cues. Ostariophysan fish (e.g. minnows) possess specialized skin cells that contain an alarm chemical. Magurran et al. (1996, Proceedings of the Royal Society of London, Series B,263, 1551-1556) were the first to use underwater video to carefully document the behavioural response of free-ranging wild populations of minnows to minnow alarm cues. They found no evidence of an antipredator response, and challenged the assumption that the contents of these cells indicate risk in the field. They proposed that alarm responses are context dependent in that they are an artefact of enclosed environments such as laboratory aquaria and field traps. Here, we repeat their experiment on free-swimming field populations of littoral fish and report a significant decrease in the number of fish in areas where chemical alarm cues of blacknose shiners, Notropis heterolepis (Ostariophysi: Cyprinidae) were released. The effect of these chemical cues was equal in magnitude to the effect of the presentation of a model predator. The response to the approach of a model predator (visual cue) was intensified by pre-exposure to chemical alarm cues. We corroborated this interaction between chemical and visual indicators of predation risk in a laboratory study using glowlight tetras, Hemigrammus erythrozonus (Ostariophysi: Characidae). Response to the visual stimulus of a predator was significantly intensified by previous exposure to conspecific chemical alarm cues. We conclude that ostariophysan skin indeed contains an alarm cue that (1) informs nearby prey of imminent predation risk, (2) induces some form of antipredator behaviour in most contexts, and (3) affects subsequent behavioural responses to stimuli in other sensory modalities.     

Survival Benefit to Antipredator Behavior in the Amphipod Gammarus minus (Crustacea: Amphipoda) in Response to Injury-released Chemical Cues from Conspecifics and Heterospecifics

A wide range of aquatic taxa use environmental chemical cues for the assessment of predation risk. We examined whether Gammarus minus (Crustacea: Amphipoda) exhibit antipredator behavior in response to injury-released chemicals from conspecifics or heterospecifics (Crustacea: Isopoda). We then examined whether behavioral responses to these cues conferred survival benefits to the amphipods. In the first part of this study, we tested the behavioral response of G. minus to the following treatments: 1. water containing injury-released cues of conspecifics; 2. water containing injury-released cues of a sympatric isopod crustacean, Lirceus fontinalis; or 3. water containing no cues (control). Relative to the control, Gammarus responded to the conspecific cue by moving to the substratum and decreasing activity. In contrast, Gammarus responded to the heterospecific cue by moving up into the water column and increasing activity. In the second part of this study, we tested if the behavioral response to these cues confers a survival benefit to Gammarus when exposed to a predator. A green sunfish ( Lepomis cyanellus ) was retained behind a partition in the test tanks. Two minutes after the introduction of the chemical cues in the first test, the barrier was lifted and predation events recorded. Relative to the control, the time to the first attack increased for Gammarus exposed to conspecific cues and decreased for those exposed to heterospecific cues. These data indicate that Gammarus distinguish between chemical cues from conspecific and heterospecific crustaceans, and that the antipredator response to conspecific cues confers a fitness benefit (i.e. increased survival due to increased time to the first attack).     

Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles

Antipredator behaviour is an important factor influencing survival probability of prey animals, and it may evolve rapidly as a response to changes in predator regime. I studied antipredator behaviour of common frog ( Rana temporaria ) tadpoles from three populations that differ in predator regimes. In the first experiment, tadpoles obtained from four natural matings in each population were subjected to chemical cues from either European perch ( Perca fluviatilis ) or from larvae of the dragonfly Aeshna juncea . Tadpoles decreased their activity in response to both predators, but the spatial behaviour of tadpoles differed between the two predator treatments. In general, there were no differences in behaviours among the populations, but in three out of four studied behaviours there were differences between parentages within the populations suggesting that these behaviours may be genetically determined. The lack of a significant Predator×Population interaction suggests no differences in plastic antipredator behaviour among the populations, while the lack of significant Predator×Parentage interaction suggests no genetic variance within the populations for plastic antipredator behaviour. In the second experiment, tadpoles from the three populations were exposed to predation by a free-ranging A. juncea . In line with the first experiment, there were no differences in survival rate between the populations. R. temporaria tadpoles seem to rely heavily on plastic antipredator behaviour as their main response to predator chemical cues. There was very little indication of local behavioural differentiation and the possible reasons for the lack of divergence among populations are discussed.     

Tadpoles of the bronze frog (Rana temporalis) assess predation risk before evoking antipredator defense behavior

Predation threat-associated behavioral response was studied in Rana temporalis tadpoles to discover the importance of predators’ visual and chemical cues (kairomones and diet-derived metabolites of consumed prey) in evoking antipredator behavior. The caged predators (dragonfly larvae) fed on prey tadpoles or insects (Notonecta spp.) and water conditioned with the predators provided the threat stimuli to the tadpole prey. The predators’ visual cues were ineffective in evoking antipredator behaviors in the tadpole prey. However, exposure to caged tadpole-fed predators or water conditioned with tadpole-fed predators elicited predator avoidance behavior in the tadpoles; they stayed away from the predators, significantly reduced swimming activity (swimming time and distance traveled), and increased burst speed. Interestingly, exposure to water conditioned with starved predators did not elicit any antipredator behavior in the prey. Further, the antipredator responses of predator-experienced tadpoles were significantly greater than those exhibited by predator-na?ve tadpoles. The study shows that R. temporalis tadpoles assess predation threat based exclusively on chemical cues emanating from the predators’ dietary metabolites and that the inclusion of conspecific prey items in the diet of the predators is perceived as a threat. The study also shows that antipredator behavior in these tadpoles is innate and is enhanced during subsequent encounters with the predators.     

Olfactory response of the predator <Emphasis Type="Italic">Zetzellia mali</Emphasis> to a prey patch occupied by a conspecific predator

While searching for food, predators may use volatiles associated with their prey, but also with their competitors for prey. This was tested for the case of Zetzellia mali (Ewing) (Acari: Stigmaeidae), an important predator of the hawthorn spider mite, Amphitetranychus viennensis (Zacher) (Acari: Tetranychidae), in black-cherry orchards in Baraghan, Iran. Using a Y-tube olfactometer, the response of this predatory mite was tested to odour from black-cherry leaves with a conspecific female predatory mite, either with or without a female of the hawthorn spider mite when the alternative odour came from black-cherry leaves with the hawthorn spider mite only. Female predators avoided odours from leaves with both a hawthorn spider mite and a conspecific predator, as well as leaves with a conspecific predator only. We discuss whether avoidance emerges in response to cues from the competitor/predator, the herbivore/prey or the herbivore-damaged plant.