Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues

1. Olfactory predator search processes differ fundamentally to those based on vision, particularly when odour cues are deposited rather than airborne or emanating from a point source. When searching for visually cryptic prey that may have moved some distance from a deposited odour cue, cue context and spatial variability are the most likely sources of information about prey location available to an olfactory predator. 2. We tested whether the house mouse (Mus domesticus), a model olfactory predator, would use cue context and spatial variability when searching for buried food items; specifically, we tested the effect of varying cue patchiness, odour strength, and cue-prey association on mouse foraging success. 3. Within mouse- and predator-proof enclosures, we created grids of 100 sand-filled Petri dishes and buried peanut pieces in a set number of these patches to represent visually cryptic 'prey'. By adding peanut oil to selected dishes, we varied the spatial distribution of prey odour relative to the distribution of prey patches in each grid, to reflect different levels of cue patchiness (Experiment 1), odour strength (Experiment 2) and cue-prey association (Experiment 3). We measured the overnight foraging success of individual mice (percentage of searched patches containing prey), as well as their foraging activity (percentage of patches searched), and prey survival (percentage of unsearched prey patches). 4. Mouse foraging success was highest where odour cues were patchy rather than uniform (Experiment 1), and where cues were tightly associated with prey location, rather than randomly or uniformly distributed (Experiment 3). However, when cues at prey patches were ten times stronger than a uniformly distributed weak background odour, mice did not improve their foraging success over that experienced when cues were of uniform strength and distribution (Experiment 2). 5. These results suggest that spatial variability and cue context are important means by which olfactory predators can use deposited odour cues to locate visually cryptic prey. They also indicate that chemical crypsis can disrupt these search processes as effectively as background matching in visually based predator-prey systems.     

Predator pheromone elicits a temporally dependent non-consumptive effect in prey

1. The influence of predator cues on the behaviour of prey is well supported in the literature; however, a clear understanding of how predator cues affect prey in variable environmental conditions and over longer time scales is needed to better understand the underlying mechanisms. Here, we measure how predator odors affect herbivore colonization, abundance, oviposition, and plant damage across two growing seasons.
2. The study system consisted of Leptinotarsa decemlineata (Colorado potato beetle) as prey, and the aggregation pheromone of live Podisus maculiventris (spined soldier bug) as the predator cue in a potato field.
3. In 2016, the amount of feeding damage by early beetle colonists was lower in predator odor-treated plots, reducing plant damage by 22%. Larval abundance was also reduced in treated plots in 2016. Beetle abundance and damage in 2017 was similar in the treatment and control plots. Two mechanisms were investigated to better understand why prey response to the predator odor treatment weakened over the first season, including changes in predator odor cue strength and prey habituation. Predator odor cue strength emerged as a likely explanation, as dispensers, which released a synthetic predator pheromone over the entire season, reduced the probability of finding damage more consistently than the live predator treatment.
4. These results suggest that temporal patterns of predator cue release and strength may drive prey response across the season, underscoring the importance of cue release-rate and consistency in both species interactions and for the future application of modifying insect behaviour using non-consumptive effects in agricultural systems.

     

Patch residence time and patch preference of the predatory mite <Emphasis Type="Italic">Amblyseius swirskii</Emphasis> in relation to prey diversity

Patch-related behaviour of a generalist predator may be influenced by patch prey diversity and result in more time being spent in patches with more than one prey species to increase the benefits of mixed diet. To examine if generalist predators are able to discern differences in prey diversity in and among patches, we examined the patch-related behaviour of the predatory mite Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae). Three lab experiments using clean, single-prey or mixed-prey patches were conducted, using whiteflies and spider mites as prey. The experiments were: (1) patch leaving tendency and residence time in absence and (2) presence of another patch, (3) patch preference. A. swirskii recognized prey-inhabited patches from a distance and showed a preference for mixed-prey patches over single-prey patches. The patch-related behaviour of A. swirskii, which seems tuned to exploiting the fitness gains of a mixed diet, is influenced by both local and distant cues.     

Chemical interaction between the larva of a dipteran parasitoid and its coleopteran host: a case of exploitation of the communication system during the searching behaviour?

The robber fly Mallophora ruficauda is one of the principal apicultural pests in the Pampas region of Argentina. As adults, the flies prey on honey bees and other insects; while, as larvae, they parasitize scarab beetle larvae. Females of M. ruficauda lay eggs away from the host in tall grasses. After being dispersed by the wind, larvae drop to the ground, where they dig in search of their hosts. It is known that second instar larvae of M. ruficauda exhibit active host searching behaviour towards its preferred host, third instar larva of Cyclocephala signaticollis, using host-related chemical cues. Furthermore, previous works show that these chemical cues are produced in the posterior body half of hosts. However, the precise anatomical origin of these cues and whether they mediate any behaviour of C. signaticollis larvae remains yet unknown. In order to determine the precise origin of the chemical cue, we carried out olfactometer assays with different stimuli of extracts of the posterior C. signaticollis body half. Additionally, we tested whether C. signaticollis is attracted to any of the same extracts as in the previous experiments. We found that both second instar of M. ruficauda and third instar of C. signaticollis are attracted to extracts of the fermentation chamber (proctodeum). This is the first report of attraction of conspecific larvae in scarab beetles. We discuss a possible case of system communication exploitation in an immature parasitoid-host system.     

Presampling sensory information and prey density assessment by wolf spiders (Araneae, Lycosidae)

Decisions regarding foraging patch residence time and the assessmentof patch quality may be mediated by various sources of information.This study examined the use of sensory cues by hunting spidersto assess prey density in the absence of prey capture. Adultfemale wolf spiders [Schizocosa ocreata (Hentz); Lycosidae]had food withheld for 4 days and then were exposed to artificialforaging patches containing four densities of crickets (0, 3,10, 20) with different sensory stimuli (visual and vibratoryinformation, visual only, and vibratory only). The spiders werenot allowed to feed during trials, and patch residence timewas recorded. The spiders varied patch residence time basedon sensory cues alone and spent more time in patches with higherprey density. With visual information only, spiders could apparentlydistinguish among prey densities almost as well as with visualand vibratory cues combined, but residence time did not differamong prey densities when only vibratory information was presented.Measurements of vibration levels produced by cricket activityunder experimental sensory treatments conform to test results,suggesting that visual detection of crickets is important inpatch assessment used in determining patch residence time.     

Prey discrimination by a generalist coccinellid predator: effect of prey age or parasitism?

1. Patterns of prey discrimination by the generalist predatory coccinellid Coleomegilla maculata lengi Timb. (Coleoptera: Coccinellidae) were studied in relation to prey quality, under laboratory conditions. 2. Choice experiments were performed in which second‐ and fourth‐instar coccinellids had the choice between Trichoplusia ni (Lepidoptera: Noctuidae) eggs that were young or old, unparasitised or parasitised by Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). 3. Coleomegilla maculata larvae did not exhibit any preference for parasitised or unparasitised eggs at a similar stage of development but always preferred younger eggs, regardless of whether or not they were parasitised. Furthermore, the percentage of rejection was higher and handling time longer on the less preferred egg type. Pre‐imaginal development time, food intake to reach adulthood, and survival of coccinellid immatures were altered when coccinellid larvae were fed with parasitised and old unparasitised eggs. 4. These results indicate that C. maculata larvae select eggs based on their stage of development regardless of parasitism, and that prey quality of aged prey is lower. 5. Fourth‐instar coccinellid larvae spent less time in patches containing solely parasitised old eggs, and their level of exploitation was greatly reduced, compared with homogeneous patches containing unparasitised young eggs. This suggests that C. maculata larvae respond to variable patch quality by using flexible decision rules that reflect the payoff of the patch.     

Sex differences in foraging behaviour and oviposition site preference in an insect predator, Orius sauteri

The effects of patch quality on the foraging behaviour of an anthocorid predator Orius sauteri (Poppius) were compared between sexes. Prior experience in patches was also studied to determine whether this was a factor affecting oviposition decisions. Patch quality affected patch residence time differently for the two sexes; females stayed much longer in a patch with prey (60 Thrips palmi larvae) than a patch without prey, while males did not remain in any patch for extended periods. Most of the females remained in or moved to patches with prey, whereas males dispersed, irrespective of patch quality. Both females released in patches with prey and females released in patches without prey deposited more eggs per hour in patches with prey than in patches without prey. Females released in patches without prey laid eggs in patches with prey at higher rates than did females released in patches with prey. Causes for the sex difference in patch residence time and allocation are discussed in relation to optimal foraging theory. The significance of selective oviposition and the role of experience in oviposition decisions within heterogeneous environments are also discussed.     

Attraction of the predator,Harmonia axyridis (Coleoptera: Coccinellidae), to its prey,Myzus persicae (Hemiptera: Aphididae), feeding on Chinese cabbage

The predatory multicolored Asian lady beetle, Harmonia axyridis, was attracted to volatiles released from Chinese cabbage infested by the green peach aphid, Myzus persicae, in T-tube olfactometer choice tests. However, lady beetle adults and larvae did not respond to clean air, Chinese cabbage alone or green peach aphid alone. Of different prey densities, H. axyridis adults were most attracted to Chinese cabbage infested by 60 M. persicae adults after 24 h. However, H. axyridis larvae were not attracted to Chinese cabbage infested by M. persicae. Mechanically damaged Chinese cabbage attracted neither lady beetle adults nor larvae. Predatory adults were attracted to 60 M. persicae adults after 24 and 48 h, and to 90 M. persicae adults after 12 h, suggesting that the predatory response depends on the prey density. Lady adult beetles did not prefer the volatiles induced by Diamondback moth, Plutella xylostella, indicating that specific host insect specificity attracts respective natural enemies. It can be explained that the volatile compounds emitted from the host plant as a result of herbivore attack preferred by the specific insect species.     

Age and Sex-Based Differences in the Use of Prey Sensory Cues in Wolf Spiders (Araneae: Lycosidae)

Differences in foraging patterns mediated by sensory cues were examined between adult and juvenile male and female wolf spiders (Schizocosa rovneri; Lycosidae). Patch residence time for thirty-one spiders were tested among juveniles and adults in artificial foraging patches. Patches varied in sensory information provided by live prey (crickets) as follows: visual stimuli alone; vibratory stimuli alone; visual and vibratory stimuli together; and control (no stimuli). Spiders moved between patches for one hour, but could not feed. Adult Schizocosa rovneri use primarily visual information to determine patch residence time, but juveniles use vibratory cues as well. Significant age and sex-based differences in the use of sensory cues suggest that observed divergent foraging strategies are partly due to the use of different perceptual cues in prey detection.     

The importance of location and visual cues during foraging in the German wasp (Vespula germanica F.) (Hymenoptera: Vespidae)

Abstract

The way in which foraging wasps use cues for prey location and choice appears to depend on both the context and on the type of prey. Vespula germanica is an opportunistic, generalist prey forager, and individual wasp foragers often return to hunt at sites of previous hunting success. In this paper, we studied which cues are used by this wasp when relocating a food source. Particularly we analysed the response to a displaced visual cue versus a foraging location at which either honey or cat food had been previously presented. We conclude that location is used over a displaced visual cue for directing wasp hovering, although the landing response is directed differently according to bait type. When wasps are exploiting cat food, location also elicits landing, but if they are exploiting honey, a displaced visual cue elicits landing more frequently than location.     

Use of odours by Cycloneda sanguinea to assess patch quality

Adult ladybirds are likely to encounter various species of prey when foraging for oviposition sites. Optimal oviposition theory predicts that females should lay eggs in those sites that are the most suitable for offspring development. Therefore, factors that directly affect offspring mortality, such as the presence of predators and food, are expected to play an important role in the assessment of patch profitability by ladybird predators. Using a Y‐tube olfactometer, we tested whether the predatory ladybird Cycloneda sanguinea L. (Coleoptera: Coccinellidae) can use volatile cues to assess patch profitability and avoid predator‐rich patches. We assessed the foraging behaviour of C. sanguinea in response to odours associated with tomato plants infested with a superior prey, Macrosiphum euphorbiae Thomas (Homoptera: Aphididae), and with an inferior prey, Tetranychus evansi Baker and Pritchard (Acari: Tetranychidae), in the presence or absence of the heterospecific predator Eriopis connexa Mulsant (Coleoptera: Coccinellidae). Females of C. sanguinea significantly preferred plants infested by M. euphorbiae to plants infested by T. evansi and avoided odours emanating from plants on which E. connexa females were present. Our results show that C. sanguinea use volatile cues to assess patch profitability and to avoid patches with heterospecific competitors or intraguild predators.     

Behavioral responses in prey location of the predatory stink bug, Eocanthecona furcellata, to chemical cues in the larvae of Spodoptera litura

Behavioral responses of the predatory stink bug Eocanthecona furcellata (Wolff) (Heteroptera: Pentatomidae) towards Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) larvae were observed in olfactometers. In single-and dual-tube olfactometers, adult bugs were observed to approach and stretch their proboscis toward the odor source. These types of behavior were also observed toward the control odor source in the dual-tube olfactometer. However, the frequency of these phases toward the control odor was significantly lower than that toward the odors from intact or dead larvae. The solvent extracts of larvae elicited these similar behavioral phases significantly more frequently and for significantly longer duration than the control. In a linear track olfactometer, E. furcellata nymphs were observed to be attracted to the fraction eluted with hexane from silica gel chromatography but proboscis-protruding behavior was not observed. The other fraction, 15%-ether-in-hexane from silica gel chromatography, elicited the proboscis-protruding behavior by a simple behavioral assay using a Pasteur pipette. These findings therefore indicate the presence of at least two different chemical cues in prey location.     

Behavioral responses to light gradients,olfactory cues,and prey in larvae of two North Pacific gadids (<Emphasis Type="Italic">Gadus macrocephalus</Emphasis> and <Emphasis Type="Italic">Theragra chalcogramma</Emphasis>)

The growth and survival of larvae can be significantly enhanced through close association with patches of high prey concentration. However, the taxis and kinesis responses used by larvae to locate and maintain residence in micro-patches remains poorly understood. In this study, the behavioral responses of Pacific cod (Gadus macrocephalus) and walleye pollock (Theragra chalcogramma) larvae (45–100 dph) to light, prey scent, and prey were examined. Both species displayed an ontogenetic shift in response to a horizontal light gradient, with small larvae (11–13 mm SL) exhibiting a positive phototaxis and large larvae (23–32 mm SL) exhibiting a negative phototaxis. Whether this reversal is related to ontogenetically appropriate foraging cues or some other aspect of the environment remains to be determined. Neither species displayed significant behavioral responsiveness to the introduction of olfactory prey cues at either size. The aggregating (taxis) response of large larvae to introduction of live prey was stronger than that of small larvae, possibly due to increased reaction distances and encounter rates. In addition, both species exhibited a kinesis response of reducing the frequency of swimming bouts in response to introduction of live prey. These results suggest that the scale of prey patchiness and the physical factors that determine patch encounter rates are a significant determinant of larval growth and survival in the early feeding stages of marine fishes.     

Cues of intraguild predators affect the distribution of intraguild prey

Theory on intraguild (IG) predation predicts that coexistence of IG-predators and IG-prey is only possible for a limited set of parameter values, suggesting that IG-predation would not be common in nature. This is in conflict with the observation that IG-predation occurs in many natural systems. One possible explanation for this difference might be antipredator behaviour of the IG-prey, resulting in decreased strength of IG-predation. We studied the distribution of an IG-prey, the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae), in response to cues of its IG-predator, the predatory mite Iphiseius degenerans. Shortly after release, the majority of IG-prey was found on the patch without cues of IG-predators, suggesting that they can rapidly assess predation risk. IG-prey also avoided patches where conspecific juveniles had been killed by IG-predators. Because it is well known that antipredator behaviour in prey is affected by the diet of the predator, we also tested whether IG-prey change their distribution in response to the food of the IG-predators (pollen or conspecific juveniles), but found no evidence for this. The IG-prey laid fewer eggs on patches with cues of IG-predators than on patches without cues. Hence, IG-prey changed their distribution and oviposition in response to cues of IG-predators. This might weaken the strength of IG-predation, possibly providing more opportunities for IG-prey and IG-predators to co-exist.     

Hide-and-seek strategies and post-contact immobility

To understand why an animal might gain by playing dead, or more precisely, exhibit post-contact immobility (PCI), we consider the context in which this behaviour occurs. Is it, for example, a method by which a potential victim encourages a predator to direct its attention elsewhere? We investigate this possibility by using the marginal value theorem to analyse predator behaviour in the context of this defence strategy by potential prey. We consider two models. In the first, (random revisiting) the predator may return to sites it has already depleted within the patch. In the second, (systematic search) the predator goes only to new sites within the patch. The results of the two models are qualitatively extremely similar. We show that when prey occur in patches, PCI favours prey survival. Indeed, certain antlion larvae have PCI durations characterized by very long half-lives. These appear to be of such long durations that further increases would convey no substantial benefits in redirecting potential predators to other antlions within the patch and subsequently to other patches.     

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.     

How predatory mites find plants with whitefly prey

We investigated the searching behaviour of two species of predatory mites, Typhlodromips swirskii (Athias-Henriot) and Euseius scutalis (Athias-Henriot), both known to feed on immature stages of the whitefly Bemisia tabaci Gennadius. When released in a greenhouse inside a circle of cucumber plants that were alternatingly clean or infested with immature whiteflies, the mites took several days to find plants. Both species were recaptured significantly more on plants with whiteflies. This suggests that the mites are able to discriminate between plants with and without whiteflies. The predators may either have been attracted to plants with whiteflies from a distance or arrested on plants with whiteflies. Typhlodromips swirskii that had previously fed on whitefly immatures on cucumber leaves were significantly attracted by volatiles from cucumber plants with whiteflies in a Y-tube olfactometer. This suggests that the mites use volatile cues to discriminate between infested and clean plants. However, this response waned rapidly; if predators, experienced as above, were starved for 3–4 h in absence of cucumber leaves, they no longer preferred volatiles of infested plants to clean plants. Furthermore, T. swirskii that had no experience with immature whiteflies on cucumber plants also did not prefer odours of infested plants to those of clean plants. Because the release experiment with this species in the greenhouse was done with inexperienced predators, this suggests that the aggregation of mites on plants with whiteflies was mainly caused by differential arrestment of mites on plants with prey and clean plants. For T. swirskii, this was in agreement with the finding that the fraction of predators on plants with prey increased with time to levels higher than 70%. A less clear trend was found for E. scutalis, for which the fraction of predators on plants with prey stabilized soon after release to levels from 54–70%. Hence, the predatory mites may find plants with prey by random searching, but they are subsequently arrested on these plants. An earlier study showed that 87% of all whiteflies released in a set-up as used here were recaptured within 1 day. Hence, the effectiveness with which predatory mites locate plants with whiteflies is low compared with that of their prey. We expect this to generate spatial patterns in the dynamics of predator and prey and this may have consequences for biological control of whiteflies with predatory mites.     

Handling time, prey preference, and functional response for Chrysoperla rufilabris in the laboratory

The predaceous larvae of Chrysoperla rufilabris (Burmeister) exhibited some success-motivated searching, particularly when feeding on Heliothis virescens (F.) eggs, but handling time did not decrease with experience. Handling time for H. virescens larvae was more than twice that for eggs. H. virescens larvae were preferred to cotton aphids (Aphis gossypii (F.)) while aphids were preferred to H. virescens eggs. C. rufilabris larvae exhibited a linear functional response to the three prey types tested, over the prey densities tested.USDA, ARS, Retire. Present address: 200 Highland, College Station, TX 77840, USA     

Response of predators to prey abundance: separating the effects of prey density and patch size

We tested the relative and combined effects of prey density and patch size on the functional response (number of attacks per unit time and duration of attacks) of a predatory reef fish (Cheilodactylus nigripes (Richardson)) to their invertebrate prey. Fish attacked prey at a greater rate and for longer time in large than small patches of prey, but large patches had naturally greater densities of prey. We isolated the effects of patch size and prey density by reducing the density of prey in larger patches to equal that of small patches; thereby controlling for prey density. We found that the intensity at which fish attacked prey (combination of attack rate and duration) was primarily a response to prey density rather than the size of patch they occupied. However, there was evidence that fish spent more time foraging in larger than smaller patches independent of prey density; presumably because of the greater total number of prey available. These experimental observations suggest that fish can distinguish between different notions of prey abundance in ways that enhance their rate of consumption. Although fish may feed in a density dependent manner, a critical issue is whether their rate of consumption outstrips the rate of increase in prey abundance to cause density dependent mortality of prey.     

Foraging for intermittently refuged prey: theory and field observations of a parasitoid

Many insect herbivores feed in concealed locations but become accessible intermittently, creating windows of greater vulnerability to attack, and generating a proportion of the prey population that is readily accessible to foraging natural enemies. We incorporated accessible prey into an extant optimal foraging model, and found that this addition allowed opportunistic exploitation of prey that have already emerged from refugia (the leaving strategy) as a viable strategy, in addition to waiting at refugia for prey to emerge (the waiting strategy). We parameterized the model empirically for the parasitoid Macrocentrus grandii and its host, Ostrinia nubilalis, under field conditions. The model predicted that M. grandii should adopt a leaving strategy when host patch density is high (travel time between patches is short), but a waiting strategy when host patch density is low (travel time between patches is long). Field observations of M. grandii patch tenure were consistent with model predictions, indicating that M. grandii exhibited flexible behaviour based on experience within a foraging bout, and that these behavioural shifts improved foraging efficiency. Behaviour of M. grandii was responsive to heterogeneity in host emergence rates, and appeared to be driven by the relatively small proportion of the host population that became accessible at a fast rate. Therefore understanding forager responses to intermittently refuged prey may require characterization of the behaviour of a subset of the prey population, rather than the average prey individual. The model can potentially be used as a framework for comparative studies across forager taxa, to understand when foragers on intermittently accessible prey should adopt fixed waiting or leaving strategies vs. a flexible strategy that is responsive to the current environment.